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An Unusual Case of Ischemic Enteritis Mimicking Regional Enteritis
Vol. 59. No. 6 Printed in U.S.A.
GASTROENTEROLOGY
Copyright © 1970 by The Williams & Wilkins Co.
CASE REPORT AN UNUSUAL CASE OF ISCHEMIC ENTERITIS MIMICKING REGIONAL ENTERITIS RONALD R. FAGIN, M.D. , FRANCIS H . STRAUS, II, M.D. , EDWIN APRIL, M .D., AND JOSEPH B. KIRSNER, M.D.
Departments of Gastroenterology, Pathology, and Radiology, Billings H ospital , University of Chicago , Chicago, fllinois
A patient treated for regional enteritis, 6 months later, was found to have ischemic enteritis secondary to infiltrative adenocarcinoma of the colon. The reversal of the abnormal small bowel pattern on X-ray was the first clue to the altered diagnosis. At surgery, compression of the mesenteric vessels by the tumor was found to be the pathogenesis of the ischemic change. Sudden occlusion of a major branch of the superior mesenteric artery may initiate massive infarction and an acute abdominal emergency. Occlusion of a smaller segmental branch may produce a lesser extent of infarction resulting in a fibrotic stricture. However, the development of collateral circulation may allow for nearly complete reversible changes. When confined to segmental branches of the superior mesenteric artery supplying the distal small bowel, an acute occlusion can result in a clinical and radiological presentation similar to regional enteritis. 1 This has been reported most commonly with an embolus from a fibrillating atrium. 1 - 3 This report describes a patient diagnosed and treated for regional enteritis before presenting to our gastroenterology service. Examination and subsequent operation indicated that the disease process was an ischemic enteritis caused by tumor involving the small and medium sized arteries of a segment of distal small bowel. Received April17, 1970. Accepted June 22, 1970. Address requests for reprints to: Dr. Joseph B. Kirsner, Department of Medicine, University of Chicago, Pritzker School of Medicine, 950 East 59th Street, Chicago, lllinois 60637. The authors gratefully acknowledge Mr. Leroy Cockerham for his technical assistance. 917
Case History A 40-year-old white female had been well until August 1968 when she noted a pressure sensation in the region of the lower back and loose, bloody stools. In October 1968, these symptoms began to alternate with episodes of constipation and abdominal cramping. She treated herself with a " bland diet" and rest. There was no history of melena, nausea, or vomiting but the patient had lost about 10 lb. In February 1969, she experienced a series of severe and diffuse abdominal pains and was admitted to another hospital. An upper gastrointestinal and small bowel study was reported as "suggestive of regional ileitis" (see below) . She was treated with prednisolone 60 mg per day, intravenous fluids, clear liquids, and finally · a low residue diet, with subsidence of symptoms and was discharged 2 weeks later. Over the next 4 months prior to admission, the patient again developed bloody diarrhea alternating with episodes of constipation and abdominal cramps and was treated with varying dosages of prednisolone and diphenoxylate hydrochloride. She was referred and admitted to the University of Chicago Billings Hospital, on August 15, 1969, for further evaluation. On admission the physical examination was normal including the pertinent negative findings of a nontender abdomen, no organomegaly or palpable masses, and normal bowel sounds. Laboratory data included a hematocrit33%, white blood count-11 ,200 per mm 3 , sedimentation rate-45 mm per hr, and three guaiac-positive stools. Proctoscopic examina-
918
CASE REPORT
Vol. 59, No.6
tion was normal. Following the radiological studies (see below), an operation was performed and demonstrated a carcinoma in the sigmoid colon, with a segment of adherent small bowel. Two metastases, 4 em in diameter, were noted in the left lobe of the liver. A palliative segmental resection was performed and the patient recovered from the operation uneventfully. Radiological studies. February 27, 1969films taken 6 months prior to admission (fig. 1). The gastroduodenal examination was normal. The small bowel showed evidence of hypersecretion with several loops of dilated small bowel in the right lower quadrant. In this region, several loops were separated by edematous thickened walls. The distal ileal mucosal pattern was distorted, manifesting coarse irregularities suggesting a "thumbprint" abnormality. Although these original films were interpreted as suggestive of regional enteritis, the pronounced edema, mucosal irregularity, separation of loops, and "thumbprinting" were compatible with ischemic bowel disease. August 20, 1969-University of Chicago (fig. 2). This second examination of the small bowel indicated striking improvement of the previously abnormal small bowel pattern. The separation of bowel loops was no longer evident and except for minimal mucosal irregularity in the extreme distal ileum, this study was interpreted as normal. A colon examination 3 days later revealed an annular constricting lesion in the sigmoid compatible with a carcinoma (fig. 3). FIG. 3. Colon examination (August 23, 1969) revealing annular constricting lesion in sigmoid compatible with carcinoma .
FIG. 1. Small bowel examination (February 27, 1969) demonstrating edema, mucosal irregularity, separation of loops and thumbprinting (arrows) compatible with ischemic enteritis.
Pathology of operative specimen. The resected sigmoid consisted of a 22-cm segment containing a 7-cm firm, white annular, ulcerated adenocarcinoma penetrating the colon wall and involving 8 to 10 em of the attached ileal mesentery. The ileal segment measured 35 em overall. The adenocarcinoma was composed of irregular papillary and branching glands. It extended through the colon wall into ileal mesentery, but did not penetrate the muscularis propria of the ileum. In the mesentery the adenocarcinoma compressed and occluded small and medium arteries (fig. 4). Ahead of the advancing neoplastic infiltration there was fibrosis, chronic inflammatory cell infiltration, and arteriosclerotic changes in small arteries (fig. 5). The muscularis of the ileum was thin
December 1970
CASE REPORT
919
without flbrosis. The submucosa was of usual thickness with considerable fibrosis and di lated as well as proliferative blood vessels. The mucosa showed a normal villous pattern in the troughs between the circular plicae, but on the apices the villi were short and plump and contained marked lymphocytic infiltrates within the lamina propria (fig. 6).
FIG. 4. Adenocarcinoma (C) compressing and occluding a small artery in the ileal mesentery (Verhoeff-Van Giesen, X 100).
FIG. 5. Adenocarcinoma (C) invading ileal mesentery ahead of which is a band of chronic inflammation and fibrosis (B), a foreign body granuloma (G) and an arteriosclerotic artery (A) (H & E, X 30) .
Discussion The patient's initial symptoms of bloody diarrhea alternating with constipation were a prelude to the series of diffuse abdominal pains necessitating her first hospitalization elsewhere in February 1969. At that time, the small bowel series was interpreted as "suggestive of regional ileitis," for which she was treated with steroids. This acute episode subsided and the increasing obstructive symptoms and recurrent rectal bleeding led to her referral and second hospitalization in August 1969. At this time, the small bowel appeared almost completely normal in radiological appearance and a carcinoma of
FIG. 6. Lymphocyte aggregation and vein dilatation of serosal connective tissue (L), submucosal fibrosis and vessel ectasia (F), mild blunting of villi with lymphocyte infiltration of the lamina propria (H & E, X 30) .
920
CASE REPORT
the colon then was demonstrated on barium enema. Although the findings during the initial hospitalization were compatible with an extensive regional enteritis, it seemed unlikely that complete reversal of this process could take place over a 6-month period, as total healing in this disease is exceedingly rare. 2 For similar reasons, infiltration of the mucosa of the small bowel by tumor is not possible in view of the subsequent recovery of the radiological abnormalities; furthermore, the mucosa was not infiltrated in the operative specimen. This case, therefore, appears to illustrate an ischemic enteritis which had spontaneously recovered over a 6-month period. The initial radiological findings of mucosal wall thickening, due to edema, separation of loops of bowel, and segmental dilation are nonspecific. 2 However, the "thumbprinting," a result of submucosal hemorrhages, is a characteristic mucosal abnormality of ischemic bowel disease. 4 If the ischemic insult is extensive and alternate pathways are inadequate to maintain viability, healing with fibrosis and stricturing may follow. 5 When adequate oxygenation is maintained by these alternate routes preventing extensive necrosis, the hemorrhage and edema may resolve with cdinplete reversibility. 1 ' 2 ' 6 If necrosis affects only the mucosa, the area most vunerable to anoxia, complete regeneration to a normal radiological small bowel pattern usually is the rule. 6 ' 7 Such was the case in our patient, whose small bowel pattern was improved greatly in 6 months. The submucosal fibrosis with relatively intact mucosa are similar to the findings of de Villiers. 7 In his dog experiments, isolated loops of bowel rendered anoxic for 3 hr developed edema, congestion, and ulceration of the mucosa, but over a period of 30 days reverted to normal. The submucosa demonstrated moderate fibrosis, and the muscularis propria and serosa were least affected. The mechanism in the present case presumes slow occlusion of the afferent arteries by tumor while col-
Vol. 59, No. 6
lateral circulation developed simultaneously. The alternate routes prevented long term anoxia; thus most of the changes were reversible. The causes of ischemic enteritis include embolus (e.g., rheumatic heart disease), thrombosis, vasculitis (e.g., HenochSchoenlein purpura), drug-induced (e.g., enteric-coated potassium chloride tablets), bleeding diatheses (e.g., thrombocytopenia or hemophilia), nonocclusive diseases (low flow states), and mechanical problems (e.g., volvulus and incarcerated hernia). In some of these categories, reversibility of abnormal radiological findings also has been reported. 2 ' 3 ' 5 To this list one should add vascular occlusion secondary to carcinomatous infiltration. Even in retrospect, it would have been difficult to differentiate ischemic enteritis from regional enteritis on the initial series of X-rays. The marked reversal to a normal small bowel pattern 6 months later proved to be the first clue that ischemia was operative in this case. This phenomenon of pronounced reversibility of an abnormal mucosal pattern strongly points to ischemic enteritis in a patient with a small bowel pattern originally suggesting regional enteritis. REFERENCES 1. Wang CC, Reeves JD: Mesenteric vascular diseases. Arner J Roentgen 83:895-908, 1960 2. Marshak RH, Lindner AE: Vascular disease of the small bowel and colon, chap 47, Alimentary Tract Roentgenology. Edited by AR Margolis, HJ Burhenne. St Louis, CV Mosby Co, 1968, p 11461170 3. Kodsi BE: Extensive ischemic damage of the small bowel with spontaneous recovery. New Eng J Med 281:309-310, 1969 4. Schwartz S, Boley S, Lash J, et al: Roentgenologic aspects of reversible vascular occlusion of the colon and its relationship to ulcerative colitis. Radiology 80:625-635, 1963 5. Wolf BS, Marshak RH: Segmental infarction of the small bowel. Radiology 66:701-706, 1956 6. Schwartz S, Boley S, Schultz L, et al: A survey of vascular diseases of the small intestine. Sem Roentgen 1:178-218, 1966 7. deVilliers R: Ischemia of the colon: An experimental study. Brit J Surg 53:497-503, 1966
GASTROENTEROLOGY
Copyright © 1970 by The Williams & Wilkins Co.
CASE REPORT AN UNUSUAL CASE OF ISCHEMIC ENTERITIS MIMICKING REGIONAL ENTERITIS RONALD R. FAGIN, M.D. , FRANCIS H . STRAUS, II, M.D. , EDWIN APRIL, M .D., AND JOSEPH B. KIRSNER, M.D.
Departments of Gastroenterology, Pathology, and Radiology, Billings H ospital , University of Chicago , Chicago, fllinois
A patient treated for regional enteritis, 6 months later, was found to have ischemic enteritis secondary to infiltrative adenocarcinoma of the colon. The reversal of the abnormal small bowel pattern on X-ray was the first clue to the altered diagnosis. At surgery, compression of the mesenteric vessels by the tumor was found to be the pathogenesis of the ischemic change. Sudden occlusion of a major branch of the superior mesenteric artery may initiate massive infarction and an acute abdominal emergency. Occlusion of a smaller segmental branch may produce a lesser extent of infarction resulting in a fibrotic stricture. However, the development of collateral circulation may allow for nearly complete reversible changes. When confined to segmental branches of the superior mesenteric artery supplying the distal small bowel, an acute occlusion can result in a clinical and radiological presentation similar to regional enteritis. 1 This has been reported most commonly with an embolus from a fibrillating atrium. 1 - 3 This report describes a patient diagnosed and treated for regional enteritis before presenting to our gastroenterology service. Examination and subsequent operation indicated that the disease process was an ischemic enteritis caused by tumor involving the small and medium sized arteries of a segment of distal small bowel. Received April17, 1970. Accepted June 22, 1970. Address requests for reprints to: Dr. Joseph B. Kirsner, Department of Medicine, University of Chicago, Pritzker School of Medicine, 950 East 59th Street, Chicago, lllinois 60637. The authors gratefully acknowledge Mr. Leroy Cockerham for his technical assistance. 917
Case History A 40-year-old white female had been well until August 1968 when she noted a pressure sensation in the region of the lower back and loose, bloody stools. In October 1968, these symptoms began to alternate with episodes of constipation and abdominal cramping. She treated herself with a " bland diet" and rest. There was no history of melena, nausea, or vomiting but the patient had lost about 10 lb. In February 1969, she experienced a series of severe and diffuse abdominal pains and was admitted to another hospital. An upper gastrointestinal and small bowel study was reported as "suggestive of regional ileitis" (see below) . She was treated with prednisolone 60 mg per day, intravenous fluids, clear liquids, and finally · a low residue diet, with subsidence of symptoms and was discharged 2 weeks later. Over the next 4 months prior to admission, the patient again developed bloody diarrhea alternating with episodes of constipation and abdominal cramps and was treated with varying dosages of prednisolone and diphenoxylate hydrochloride. She was referred and admitted to the University of Chicago Billings Hospital, on August 15, 1969, for further evaluation. On admission the physical examination was normal including the pertinent negative findings of a nontender abdomen, no organomegaly or palpable masses, and normal bowel sounds. Laboratory data included a hematocrit33%, white blood count-11 ,200 per mm 3 , sedimentation rate-45 mm per hr, and three guaiac-positive stools. Proctoscopic examina-
918
CASE REPORT
Vol. 59, No.6
tion was normal. Following the radiological studies (see below), an operation was performed and demonstrated a carcinoma in the sigmoid colon, with a segment of adherent small bowel. Two metastases, 4 em in diameter, were noted in the left lobe of the liver. A palliative segmental resection was performed and the patient recovered from the operation uneventfully. Radiological studies. February 27, 1969films taken 6 months prior to admission (fig. 1). The gastroduodenal examination was normal. The small bowel showed evidence of hypersecretion with several loops of dilated small bowel in the right lower quadrant. In this region, several loops were separated by edematous thickened walls. The distal ileal mucosal pattern was distorted, manifesting coarse irregularities suggesting a "thumbprint" abnormality. Although these original films were interpreted as suggestive of regional enteritis, the pronounced edema, mucosal irregularity, separation of loops, and "thumbprinting" were compatible with ischemic bowel disease. August 20, 1969-University of Chicago (fig. 2). This second examination of the small bowel indicated striking improvement of the previously abnormal small bowel pattern. The separation of bowel loops was no longer evident and except for minimal mucosal irregularity in the extreme distal ileum, this study was interpreted as normal. A colon examination 3 days later revealed an annular constricting lesion in the sigmoid compatible with a carcinoma (fig. 3). FIG. 3. Colon examination (August 23, 1969) revealing annular constricting lesion in sigmoid compatible with carcinoma .
FIG. 1. Small bowel examination (February 27, 1969) demonstrating edema, mucosal irregularity, separation of loops and thumbprinting (arrows) compatible with ischemic enteritis.
Pathology of operative specimen. The resected sigmoid consisted of a 22-cm segment containing a 7-cm firm, white annular, ulcerated adenocarcinoma penetrating the colon wall and involving 8 to 10 em of the attached ileal mesentery. The ileal segment measured 35 em overall. The adenocarcinoma was composed of irregular papillary and branching glands. It extended through the colon wall into ileal mesentery, but did not penetrate the muscularis propria of the ileum. In the mesentery the adenocarcinoma compressed and occluded small and medium arteries (fig. 4). Ahead of the advancing neoplastic infiltration there was fibrosis, chronic inflammatory cell infiltration, and arteriosclerotic changes in small arteries (fig. 5). The muscularis of the ileum was thin
December 1970
CASE REPORT
919
without flbrosis. The submucosa was of usual thickness with considerable fibrosis and di lated as well as proliferative blood vessels. The mucosa showed a normal villous pattern in the troughs between the circular plicae, but on the apices the villi were short and plump and contained marked lymphocytic infiltrates within the lamina propria (fig. 6).
FIG. 4. Adenocarcinoma (C) compressing and occluding a small artery in the ileal mesentery (Verhoeff-Van Giesen, X 100).
FIG. 5. Adenocarcinoma (C) invading ileal mesentery ahead of which is a band of chronic inflammation and fibrosis (B), a foreign body granuloma (G) and an arteriosclerotic artery (A) (H & E, X 30) .
Discussion The patient's initial symptoms of bloody diarrhea alternating with constipation were a prelude to the series of diffuse abdominal pains necessitating her first hospitalization elsewhere in February 1969. At that time, the small bowel series was interpreted as "suggestive of regional ileitis," for which she was treated with steroids. This acute episode subsided and the increasing obstructive symptoms and recurrent rectal bleeding led to her referral and second hospitalization in August 1969. At this time, the small bowel appeared almost completely normal in radiological appearance and a carcinoma of
FIG. 6. Lymphocyte aggregation and vein dilatation of serosal connective tissue (L), submucosal fibrosis and vessel ectasia (F), mild blunting of villi with lymphocyte infiltration of the lamina propria (H & E, X 30) .
920
CASE REPORT
the colon then was demonstrated on barium enema. Although the findings during the initial hospitalization were compatible with an extensive regional enteritis, it seemed unlikely that complete reversal of this process could take place over a 6-month period, as total healing in this disease is exceedingly rare. 2 For similar reasons, infiltration of the mucosa of the small bowel by tumor is not possible in view of the subsequent recovery of the radiological abnormalities; furthermore, the mucosa was not infiltrated in the operative specimen. This case, therefore, appears to illustrate an ischemic enteritis which had spontaneously recovered over a 6-month period. The initial radiological findings of mucosal wall thickening, due to edema, separation of loops of bowel, and segmental dilation are nonspecific. 2 However, the "thumbprinting," a result of submucosal hemorrhages, is a characteristic mucosal abnormality of ischemic bowel disease. 4 If the ischemic insult is extensive and alternate pathways are inadequate to maintain viability, healing with fibrosis and stricturing may follow. 5 When adequate oxygenation is maintained by these alternate routes preventing extensive necrosis, the hemorrhage and edema may resolve with cdinplete reversibility. 1 ' 2 ' 6 If necrosis affects only the mucosa, the area most vunerable to anoxia, complete regeneration to a normal radiological small bowel pattern usually is the rule. 6 ' 7 Such was the case in our patient, whose small bowel pattern was improved greatly in 6 months. The submucosal fibrosis with relatively intact mucosa are similar to the findings of de Villiers. 7 In his dog experiments, isolated loops of bowel rendered anoxic for 3 hr developed edema, congestion, and ulceration of the mucosa, but over a period of 30 days reverted to normal. The submucosa demonstrated moderate fibrosis, and the muscularis propria and serosa were least affected. The mechanism in the present case presumes slow occlusion of the afferent arteries by tumor while col-
Vol. 59, No. 6
lateral circulation developed simultaneously. The alternate routes prevented long term anoxia; thus most of the changes were reversible. The causes of ischemic enteritis include embolus (e.g., rheumatic heart disease), thrombosis, vasculitis (e.g., HenochSchoenlein purpura), drug-induced (e.g., enteric-coated potassium chloride tablets), bleeding diatheses (e.g., thrombocytopenia or hemophilia), nonocclusive diseases (low flow states), and mechanical problems (e.g., volvulus and incarcerated hernia). In some of these categories, reversibility of abnormal radiological findings also has been reported. 2 ' 3 ' 5 To this list one should add vascular occlusion secondary to carcinomatous infiltration. Even in retrospect, it would have been difficult to differentiate ischemic enteritis from regional enteritis on the initial series of X-rays. The marked reversal to a normal small bowel pattern 6 months later proved to be the first clue that ischemia was operative in this case. This phenomenon of pronounced reversibility of an abnormal mucosal pattern strongly points to ischemic enteritis in a patient with a small bowel pattern originally suggesting regional enteritis. REFERENCES 1. Wang CC, Reeves JD: Mesenteric vascular diseases. Arner J Roentgen 83:895-908, 1960 2. Marshak RH, Lindner AE: Vascular disease of the small bowel and colon, chap 47, Alimentary Tract Roentgenology. Edited by AR Margolis, HJ Burhenne. St Louis, CV Mosby Co, 1968, p 11461170 3. Kodsi BE: Extensive ischemic damage of the small bowel with spontaneous recovery. New Eng J Med 281:309-310, 1969 4. Schwartz S, Boley S, Lash J, et al: Roentgenologic aspects of reversible vascular occlusion of the colon and its relationship to ulcerative colitis. Radiology 80:625-635, 1963 5. Wolf BS, Marshak RH: Segmental infarction of the small bowel. Radiology 66:701-706, 1956 6. Schwartz S, Boley S, Schultz L, et al: A survey of vascular diseases of the small intestine. Sem Roentgen 1:178-218, 1966 7. deVilliers R: Ischemia of the colon: An experimental study. Brit J Surg 53:497-503, 1966