GRANULOMATOUS COLITIS: SIGNIFICANCE OF INVOLVEMENT OF THE TERMINAL ILEUM
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1 GASTROENTEROLOGY 64: , 1973 Copyright 1973 by The Williams & Wilkins Co. Vol. 64, No.6 Printed in U.S.A. GRANULOMATOUS COLITIS: SIGNIFICANCE OF INVOLVEMENT OF THE TERMINAL ILEUM JAMES A. NELSON, M.D., ALEXANDER R. MARGULIS, M.D., HENRY I. GOLDBERG, M.D., AND THOMAS L. LAWSON, M.D. Department of Radiology, University of California School of Medicine, San Francisco, California Review of surgical, histological, and roentgenographic findings in this series disclosed that granulomatous colitis without involvemen.t of the terminal ileum was relatively uncommon. All roentgenographic findings for involvement of the terminal ileum were substantiated histologically and surgically. Several cases, however, had involvement of the terminal ileum which was not detectable on roentgenograms but which was subsequently proved histologically and surgically. Cecal involvement in the presence of disease of the terminal ileum was universal in this series. Preoperative fistulae and local postoperative complications occurred as often in those patients with as in those without disease of the terminal ileum. This study therefore would not support the concept that granulomatous colitis with ileal involvement is a more "benign" process. In this series, extensive small bowel disease was associated with a higher incidence of malabsorption, duodenal ulcer, and duodenal regional enteritis. Among the 8 patients with pathologically proved granulomatous colitis and a normal terminal ileum, 4 were elderly men who had an underlying disease which may have led to an ischemic colitis which appeared to be clinically, roentgenographically, and histologically indistinguishable from granulomatous colitis.. With the typical roentgenographic picture of Crohn's disease of the small bowel with a narrow, stiff, deeply ulcerated, or fistulated terminal ileum, any associated roentgenographic evidence of colitis can be accepted as granulomatous colitis-regardless of the roentgenographic features of the colitis. Granulomatous colitis without disease of the terminal ileum, however, is difficult to diagnose clinically and roentgenographically.. Lindner et al. 1 found that patients with granulomatous colitis do "relatively well." Received September 21, Accepted November 15, Address requests for reprints to: Dr. J. A. Nelson, Department of Radiology, University of California, San Francisco, San Francisco, California Dr. Nelson is a Trainee, Veterans Administration Training Program Marshak and Lindner 2 state that patients with granulomatous colitis seem to fall into two categories: those in whom the disease follows a benign clinical course and others who experience multiple problems associated with the colonic disease. Recently, McGovern and Goulston 3 reported a series of cases of granulomatous colitis in which they separated the cases into those with and those without involvement of the terminal ileum. They concluded that granulomatous colitis with involvement of the terminal ileum behaves in a more benign manner. Considering these findings, we decided to review a series of cases of pathologically proved granulomatous colitis in order to determine if there is a significant difference in its clinical and roentgenographic course when the terminal ileum is involved.
2 1072 NELSON ET AL. Vol. 64, No.6 Materials and Methods Thirty cases of granulomatous colitis with well documented clinical records and barium enema examinations were selected; the clinical records were the primary basis for selection. In all but 1 case, histological diagnoses were made on resected colon, small bowel, or both. The exception was a classic case of Crohn's disease determined by means of small bowel examination and by disclosure of an abnormal rectosigmoid on barium enema examination; in this case granulomatous colitis was diagnosed as a result of a rectal biopsy. The histological criteria for diagnosis of granulomatous colitis have been described. 4 Since we selected patients who required bowel resection, nearly all of them would fit Marshak and Lindner's category of patients with unremitting, severe disease. 2 Age of onset of symptoms of granulomatous colitis was determined from the initial history of present illness. The period of clinical follow-up ranged from 2 to 27 years, with a mean of 8 years and a mode of 5 years. All operative and pathological reports were carefully reviewed. Involvement of the terminal ileum was assessed from those films of the roentgenographic examination that showed the colonic disease in its most severe state. Site and extent of gastrointestinal involvement were noted as were incidence of preoperative fistulae, local operative wound complications and fistulae, presence of peptic ulcer, gallstones, malabsorption, and arthritis. Data were tabulated and compared (tables 1 and 2). Data regarding age of onset were analyzed with the Student's t-test for unpaired data. Results and Discussion Our material for this analysis consisted of 30 cases of granulomatous colitis-22 cases with involvement of the terminal ileum and 8 cases in which the terminal ileum was normal. Prior to colectomy, 16 patients showed both roentgenographic and histological evidence of ileal disease, whereas 14 had no roentgenographic evidence of involvement of the terminal ileum. At the time of the operation, however, there was surgical and histological confirmation of mild involvement of the terminal ileum in 6 of these TABLE 1. Incidence of complications in 27 of 30 patients with granulomatous colitis (Ge) Malab- Peptic Gall- sorption ulcer stones Preoperative fistulae Postoperative complica tion or recurrence Other GC without involvement 4/8 5/8 0/8 0/8 1/8 1 Arteriosclerotic cardioof the terminal ileum vascular disease (8 patients) 1 Systemic lupus erythematosis 1 Ankylosing spondylitis GC with involvement 12/22 11/22 3/22 5/22 a 1/22 1 Aseptic necrosis ofthe of the terminal ileum right femoral head (22 patients) a Four of these 5 cases of peptic ulcer were associated with concurrent steroid therapy. All 30 patients in this series received steroids some time during their treatment. TABLE 2. Incidence of duodenal and segmental colonic involvement in 30 patients with granulomatous colitis Duodenum Cecum Ascending Transverse Descending colon colon colon Sigmoid Rectum Without involvement of 0 4/8 5/8 6/8 6/8 8/8 6/8 the terminal ileum (8 patients) With involvement of the 3/22 22/22 20/22 18/22 16/22 17/22 17/22 terminal ileum (22 patients)
3 June GRANULOMATOUS COLITIS 1073 latter 14 patients (fig. 1). Therefore, normal terminal ileum was only established in the 8 remaining patients (fig. 2). This is similar to the false-negative radiographic appearance of disease of the terminal ileum recently reported by Korelitz et al. 5 Preoperative fistulae and postoperative wound complications occurred in 27 of the 30 patients in this series. These complications appeared with equal frequency in patients with and without involvement of the terminal ileum (table 1). The high incidence of such problems in this series reflects the severity of the disease in patients referred to our large medical center (fig. 3). The occurrence of malabsorption and peptic ulcer more often in patients with involvement of the terminal ileum (table 1) merely reflects the difference in the degree of small bowel involvement. FIG. 1. Roentgenographically normal terminal ileum. At time of operation, several days after this examination, the terminal 8 cm of the ileum showed gross and histological evidence of regional enteritis.
4 1074 NELSON ET AL. Vol. 64, No. 6 FIG. 2. Severe granulomatous colitis with a terminal ileum proved roentgenographically and histologically to be normal. Table 2 summarizes the data characterizing the site of gastrointestinal involvement in the two groups. The universal cecal involvement in patients with disease of the terminal iltmm is notable. We have no roentgenographic evidence for progression of disease across the ileocecal valve and can state only that there was simultaneous involvement of the terminal ileum and the cecum at the time of roentgenographic examination. Only 4 of the 8 cases of granulomatous colitis without involvement of the terminal ileum had cecal involvement. Of the 22 patients with disease of the terminal ileum, the bowel resection was elective and was preceded by emergency decompression colostomy in only 1 patient. Three patients with disease of the terminal ileum had previously undergone appendectomies, but these procedures were not related to the bowel resection upon which diagnosis of granulomatous colitis was established.
5 June 1973 GRANULOMATOUS COLITIS 1075 FIG. 3. Severe granulomatous colitis with disease of the terminal ileum and multiple fistulae. Differences in age of onset between the two groups were not statistically significant (P > 0.2). Four of the 8 patients with a normal terminal ileum had acute surgical abdominal symptoms just prior to colonic resection, when the histological specimen was obtained (table 3). These 4 patients were elderly men with an average age of 61 at onset of gastrointestinal symptoms. This is significantly greater (P < 0.01) than the average age at onset of the remaining 4 patients with a normal terminal ileum. Although the acute abdomen in these 4 patients may have been related to underlying granulomatous colitis, it is possible that the roentgenographic and histological findings of granulomatous colitis might represent a nonspecific response to vascular compromise (fig. 4, A and B). These patients, as indeed other patients with roent-
6 1076 NELSON ET AL. Vol. 64, No. 6 A FIG. 4. A, granulomatous colitis in an elderly patient who had colostomy performed previously for perforation. B, roentgenogram of the ascending colon of the same patient shows the terminal ileum and cecum to be normal. TABLE 3. Pertinent history and possible predisposing factors in 4 of 8 patients with granulomatous colitis (Ge) and no involvement of the terminal ileum Age at onset y r Possible predisposing factors Appendicial perforation 10 yr before diagnosis of GC; colonic perforation, treated by colostomy, before roentgenographic diagnosis of GC and colectomy. Development of colonic obstruction after hemorrhoidectomy; after treatment for the obstruction, development of symptoms of GC requiring anterior sigmoid resection. Prior appendicostomy at age 66; colonic obstruction and cecostomy at age of 75; colectomy after colostomy; generalized arteriosclerotic cardiovascular disease. Colostomy performed for " perforated diverticulum"; syphilis; severe hypertension; anterior sigmoid resection performed for sigmoid involvement by granulomatous colitis which was detected after the initial colostomy. Patient died 1 yr after operation. At autopsy, the remaining intestinal tract was normal. genographic and histological findings of granulomatous colitis without involvement of the small bowel, may not have Crohn's disease at all. REFERENCES 1. Lindner AE, Marshak RH. Wolf BS, et al: Granulomatous colitis: a clinical study. N Engl J Med 269: , Marshak RH, Lindner AE: Radiology of the Small Intestine. Philadelphia, WB Saunders Co, McGovern VJ, Goulston SJM: Crohn's disease of the colon. Gut 9: , Margulis AR, Goldberg HI, Lawson TL, et al: The overlapping spectrum of ulcerative and granulomatous colitis: A roentgenographic-pathologic study. Am J Roentgenol 113: , Korelitz BI. Present DH, Alpert L1, et al: Recurrent regional ileitis after ileostomy and colectomy for granulomatous colitis. N Engl J Med 287: , 1972
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