Received for publication, November 20, * Present address: Department of Nursing, College of Medical Sciences, Tohoku

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1 Tohoku J. exp. Med., 1976, 118 (Suppl.), Ischemic Colitis RIKURO SASAKI,* HIKARU WATANABE, SHUICHI IWAI, NOBUYUKI SUGAWARA, HIROTSUGU YAMAGIWA, AKIHIKO ITO, MAKOTO ISHIKAWA j?? and SHOICHI YAMAGATA The Third Department of Internal Medicine, Tohoku University School of Medicine, Sendai SASAIU, R., WATANABE, H., IWAI, S., SUGAWARA, N., YAMAGIWA, H., ITO, A., ISHIKAWA, M. and YAMAGATA, S. Ischemic Colitis. Tohoku J. exp. Med., 1976, 118 (Suppl.), Although several hundred cases of ischemic colitis have been reported from western countries, no case has been reported in our country. Ischemic colitis is a well established entity. Clinicopathological manifestations, diagnosis, treatment and prognosis of the disease are well known. A majority of reported cases were not particularly unusual. Two cases, of which one showed an unusually long lasting acute episode but good prognosis, and the other presented a diagnostic problem and was found to have a fibrous stricture due to ischemic colitis in the sigmoid colon at surgery, were described and discussed in relation to their symptoms, diagnosis and prognosis. ischemic colitis Ischemic colitis presents various clinicopathologic manifestations resulting from failure of the blood supply to the colon. The patients characteristically have symptoms of colitis, including abdominal pain, rectal bleeding and variable diarrhea. Acute vascular insufficiency of the colon after surgical ligation of the inferior mesenteric artery has been well known. Boley et al. (1963), however, have described for the first time the spontaneous occurrence and reversible nature of segmental infarction of the colon. Since then, Marston et al. (1966) presented a clinical classification for all types of vascular insufficiency of the colon and proposed the term "ischemic colitis". Although over 300 cases of ischemic colitis have appeared in the literature (Marston et al. 1966; Kilpatrick et al. 1968; Williams et al. 1969; Balslev et al. 1970; Davis 1970; Boley and Schwartz 1971; Marcuson and Farman 1971; Miller et al. 1971; Moller and Stjernvall 1971; Whitehead 1971; Clark et al. 1972; Ross 1972; Dahria et al. 1973; Kaminski et al. 1973; Thomas and Wellwood 1973), not a single case has been reported in our country. The present paper describes our experience with 2 cases of ischemic colitis. University, Received for publication, November 20, * Present address: Department of Nursing, College of Medical Sciences, Tohoku Sendai. õ Present address: The Second Department of Internal Medicine, Yamagata University School of Medicine, Yamagata. 127

2 123 R. Sasaki et al. CASE REPORT Case 1. A 67-year-old woman complained of the left lower abdominal pain with sudden onset, followed by mucoid bloody stools at the end of November, The patient was admitted to a hospital but continued to have the lower abdominal pain and bloody stools 4-5 times a day. She gradually developed a full sensation of the abdomen, anorexia and nausea, and was transferred to this hospital on February 16, On admission the patient appeared to be chronically ill and pale. The abdomen was distended and tender all over. Blood pressure was 102/60 mm Hg, temperature 37.4 Ž, and pulse rate 110/min. Laboratory studies showed a blood sedimentation rate of 40 mm in 1 hr and 95 mm in 2 hr. The stool contained a large amount of mucous and was strongly positive for occult blood. RBC was 309 mil., Hb g/100ml, WBC 9200, and the differential was almost normal. Total protein was 5.2 g/100ml, albumin 36.6%, and globulin 62.6%. Serum Na was 142 meq/liter, K 3.7 meq/liter and Cl 96 meq/ Fig. 1, a, b. Case 1. Barium enema shows marked thumb -printings in the ascending and transverse colon, and loss of haustral markings with mucosal irregularity in the descending colon (2/6/74).

3 Ischemic Colitis 129 Fig. 2. Case 1. Histology of biopsy specimens from the lesion. a. A picture of strong nonspecific inflammation. b. Intimal thickening in the submucosal artery (2/16/74). liter. The liver function tests were normal. The chest X-ray film and EKG were normal. The upper GI series was also normal. The plain film of abdomen showed remarkable distension of the entire colon but no evidence of intestinal obstruction. Barium enema studies were performed 10 days before the transfer. The films showed characteristic thumb-printings in the ascending and transverse colon and loss of haustral markings with mucosal irregularity in the descending colon (Fig. 1 a, b). The fibercolonoscopic observation revealed that there were many scattered erosions beyond 20 cm from the anus and the mucosa in the rectum was normal. Biopsy specimens from the lesion showed strong inflammatory changes but no granulomatous or malignant changes (Fig. 2a). There was evidence of arteritis (Fig. 2b). Selective angiography was performed but the catheter did

4 130 R. Sasaki et al. Fig. 3. Case 1. a. Aortogram. There were a few shadow defects in the left colic artery just distal to its origin (shown by arrow) (2/21/74). b. Selective angiogram of the inferior mesenteric artery. There were no abnormal findings (7/22/74). not enter the inferior menesteric artery. Aortograms showed a few shadow defects probably due to thrombosis in the left colic artery just distal to its origin but no cessation of the blood flow (Fig. 3a). From the above clinical course and laboratory examinations, the diagnosis of ischemic colitis was made. Because of continuance of bloody diarrhea and abdominal pain for more than 2 months, elective surgical intervention was planned, and conservative treatment was efforted for improvement of general condition. However, she continued to have bloody diarrhea and developed generalized edema. Total protein decreased to 4.3 g/100 ml and serum K to 1.9 meq/liter at that time. Blood transfusion in a total 1800 nil was given, and then she gradually recovered. Bloody diarrhea stopped and serum protein and K increased. The fibercolonoscopic examination 3 weeks after admission showed disappearance of mucosal folds, irregu larity of the surface, loss of extensibility and easy bruisibility (Fig. 4a, b). Repeated barium enema studies showed patterns of polyposis, especially in the descending colon. Typical thumb-printings were no longer present (Fig. 5a). The fibercolono scopic observation 5 months after admission showed complete healing with rough surface of the mucosa (Fig. 4c). Barium enema studies at that time showed typical patterns of polyposis centered in the splenic flexure (Fig. 5b). The shadow defects seen in the left colic artery in the previous angiography have completely

5 Ischemic Colitis 131 Fig. 4. Case 1. Fibercolonoscopic appearance. a. The mucosa in the descending colon appears to be rough or fine granular, and there was blood on the surface of the mucosa. b. Ulcer is seen in the sigmoid colon (3/5/74). c. There is complete healing of erosions and ulcerations, but the rough surface of the mucosa is seen (7/15/74). Fig. 5. Case 1. Barium enema shows patterns of polyposis. a. (3/11/74). b. (7/9/74). disappeared at the selective angiography of the inferior mesenteric artery performed on July 22 (Fig. 3b). The patient was discharged on August 8, 1974 and no symptoms have recurred. Case 2. A 75-year-old woman was well until the end of April, 1975, when she

6 132 R. Sasaki et al. Fig. 6. Case 2. Barium enema shows a sharply demarcated constricted point, short con stricted area with an ulcer in the descending colon. Typical thumb-printings are also seen (6/5/75). developed diarrhea and abdominal pain. The patient was seen at the outpatient clinic on May 1 but refused examinations including barium enema and endoscopic observations. A month later she visited the clinic, and had barium enema studies done on June 5. There were a sharply demarcated constricted point in the sigmoid colon and a short constricted area with an ulcer in the descending colon. There were also thumb-printings in the upper descending colon (Fig. 6). Cancer of the sigmoid colon, ischemic colitis or granulomatous colitis were suspected, but she again refused further examinations. The patient developed constipation, nausea, vomiting and abdominal distension on July 28 and the diagnosis of intestinal obstruction was made. She was admitted to Department of Surgery, Tohoku University Hospital, but strongly refused operations. With subsidence of symptoms, she was transferred for conservative treatment on August 4. At the time of transfer she appeared to be chronically ill. There were no abnormal physical findings. Blood pressure was 116/68 mm Hg, temperature 37.2 C, pulse rate 72 /min. The sedimentation rate was 12 mm in 1 hr and 27 min in 2 hr. Urinalysis and stool were normal. RBC was 408 mil., Hb 11.7 g/100ml, WBC 5200, and the differential was normal. Total protein was 6.3 g/100 ml, albumin 53.2%

7 Ischemic Colitis 133 Fig. 7. (9/ Case 2. 8/75). Selective angiogram of the inferior mesenteric artery sho ws no abnormalities Fig. 8. Case 2. Barium enema shows an complete obliteration in the sigmoid colon (8/18/75).

8 134 R. Sasaki et al. and globulin 46.3%. Serum Na was 137 meq/liter, K 3.lmEq/liter and Cl 98 meq/liter. The liver function tests were normal. The chest X-ray film showed a calcified lesion probably of old tuberculosis in the left hilar area. The plain film of abdomen was essentially normal. Barium enema studies appeared to be about the same as that seen on June 5. The fibercolonoscopic examination failed to observe lesions since the instrument could not be advanced beyond the constricted point in the sigmoid colon. Selective angiography of the inferior mesenteric artery showed no definite occlusion of vessels or cessation of blood stream (Fig. 7). From the clinical course and laboratory findings, no definite diagnosis could be established. The patient developed 2 more episodes of intensified intestinal obstruction with nausea, vomiting and abdominal distension on August 18 and September 10. The plain film of abdomen showed fluid levels and barium enema studies showed a complete obliteration in the sigmoid colon on August 18 (Fig. 8). She finally agreed to operation. At operation she was found to have a fibrous stricture of the sigmoid colon, without evidence of malignancy or inflammation. The patient did well immediately after operation, but developed pneumonia and died 2 weeks after operation. DISCUSSION These two cases will be discusssed in relation to their symptoms, diagnosis, and prognosis. Ischemic colitis usually affects those of middle or older age and is frequently superimposed on a background of arteriosclerotic diseases. Boley and Schwartz (1971) have stated that, of 89 cases of colonic ischemia, 53 percent occurred in females and 47 percent in males. Their ages ranged from one to 87 years and 91 percent were in the seventh decade or older. However, there have been a few reports that younger persons are also affected (Miller et al. 1971; Clark et al. 1972; Dahria et al. 1973; Rickert et al. 1974). Marston et al. (1966) classified the syndrome depending on the degree of is chemia which produced either infarction of the whole bowel wall or severe he morrhagic colitis leading eventually to stricture formation or transient bloody diarrhea with complete recovery. As to incidence of the form of disease, nearly half of the cases are reversible (Marcuson and Farman 1971). Typical clinical symptoms include lower abdominal pain, rectal bleeding and variable diarrhea. The onset is usually abrupt, and the pain is crampy in nature and localized to the left side. Initially, the only abnormal physical finding is abdominal tenderness over the area of the involved colon. Clinical symptoms may, however, be so mild as to be disregarded by the patient. The most common radiological findings in reversible ischemic colitis are thumb printing of the bowel wall and mucosal irregularity. The thumb-printings represent submucosal hemorrhage and are present only in the acute stage. Increasing abdominal signs, fever, leukocytosis, or persistence of diarrhea and bleeding for more than one week indicate development of irreversible changes, and surgical intervention is indicated. Reversible lesions respond to treatment in

9 Ischemic Colitis 135 general within 7 to 10 days. Boley and Schwartz (1971) mentioned that such patients with persistence of diarrhea and bleeding often go on to perforation and peritonitis. Case 1 had apparently an acute episode lasting more than 2 months and the diagnosis of ischemic colitis was made without difficulty. This clinical course, however, must be very unusual. Similar cases with abdominal pain or bloody diarrhea for more than 2 months have not been found in the literature. Such patients might have had surgical intervention very soon. Furthermore, it may well be said that very fortunately she developed no sequential disturbance despite persistence of symptoms. The stricture possibly due to ischemic colitis was retrospectively diagnosed in Case 2. It presents a diagnostic problem. The key for diagnosis of ischemic colitis is early and serial barium enema studies. Any patients with sudden onset of abdominal pain and rectal bleeding or bloody diarrhea should have a barium enema within 48 hr of an acute episode. The disappearance or changes in initial thumb-printings on subsequent studies are the major criterion for radiologic diagnosis. If the initial barium enema is delayed until healing occurs, or the segmental colitis pattern has developed, the ischemic nature of the disease may be missed. Therefore, the diagnosis of ischemic colitis is not so difficult, but it should not be diagnosed on a single evaluation. A definite diagnosis is to be established by following the clinical and radiologic evolution of the patient's course and barium enema findings. It might be an acute episode of the disease that Case 2 developed abdominal pain and diarrhea 3 months prior to admission. There were no ways to make a correct diagnosis at that time. Marston (1971) stated that irreversible lesions such as tubular narrowing occur 3-4 weeks after the onset of the disease. It could be so extensive as to lead to complete obliteration of the lumen. Abrupt loss of the lumen occurring over a few weeks in previously quite healthy bowel is almost always due to infarction. It is presumable that irreparable changes secondary to ischemic colitis occurred in Case 2, though there was no convincing evidence. Marshak et al. (1974) mentioned that late roentogenologic manifestation of ischemic colitis might be confused with that of carcinoma. Indeed, it was very difficult to distinguish ischemic colitis from carcinoma of the sigmoid colon on radiological appearance in Case 2. Petigrow and Ludwig (1971) reported a case in which the prominent features of ischemic colitis masked associated malig nancy and delayed surgical intervention. In Case 2, a correct diagnosis was not made until operation was performed. Endoscopic examination is also helpful for diagnosis when performed soon after the onset of symptoms. Especially, the fibercolonoscopy is valuable since any segment of the involved bowel is within reach of the instrument. It is not yet clear whether inferior mesenteric angiography is of value in the diagnosis of the patients with ischemic colitis. Since most of the reported cases with left colon ischemia have no demonstrable occlusion, normal angiograms do not exclude the disease. Arteriography was once suggested to be a guide to determine whether colon resection should be performed or not (Williams et al.

10 136 R. Sasaki et al. 1969). However, it does not always give correct clues. There have been a few cases reported in which non-occlusive ischemic colitis progressed to irreversible infarction or gangrene (Marston et al. 1966; Williams et al. 1969). On the other hand, there were two cases, which had occlusion of vessels but recovered without surgery (Dunbar 1966; Westcott 1972). The shadow defects observed in the left colic artery in the initial angiography in Case 1 were not found at the follow-up examination 5 months later. It is retrospectively uncertain whether these were truely due to thrombosis. It was believed at that time that there were thrombosis causing incomplete occlusion. Nevertheless, the patient recovered without irreversible changes. Though the angiography was normal in Case 2, irreversible changes had already occurred in the sigmoid colon. Angiographie findings also seemed to be unusual in our cases. The final outcome of ischemic colitis depends on many factors. However, the initial response to ischemia may be the same regardless of its severity. It is, therefore, impossible to predict the progression of the ischemic process from the initial physical, radiologic or endcscopic evaluation (Boley and Schwartz 1971). Marcuson and Farman (1971) collected 122 cases of ischemic colitis and stated that nearly half of the cases will resolve and require no further treatment. The remainder will develop strictures but some of these will dilate with the progress of clinical course. Surgery is indicated for obstruction or to exclude malignancy. The prognosis of patients with ischemic colitis without gangrene seems to be good (Balslev et al. 1970). It requires several months for healing or cicatrization of an involved colon, so that the final fate of the disease cannot be anticipated until complete healing occurs, or a non-reversible lesion is demonstrated which requires excision. It is emphasized that the prognosis of patients with ischemic colitis cannot either be easily predicted from our own experience. References 1) Balslev, I., Jensen, H-E., Norgaard, F. & Poll, P. (1970) Ischemic colitis. Acta chir. scared., 136, ) Boley, S.J. Schwartz, S., Lash, J. & Sternhill, V. (1963) Reversible vascular occlusion of the colon. Surg. Gynec. Obstet. 116, ) Boley, S.J. & Schwartz, S.S., (1971) Colonic ischemia: reversible ischemic lesions. In: Vascular Disorder of the Intestine, edited by S.J. Boley, S.S. Schwartz & L.F. Williams, Jr., Appleton Century Crofts, New York, pp ) Clark, A.W. Lloyd-Mostyn, R.H. & Sadler, M.R. de C. (1972) "Ischaemic" colitis in young adults. Brit. med. J., 4, ) Dahria, K.M., Ngo, N.L., Marino, A.W.M. Jr., Nancini, H.W.N. & Shah, I.C. (1973) Reversible ischemic colitis: report of four cases. Dis. Colon Rect., 16, ) Davis, J.E. (1970) Reversible vascular occlusion of the colon. Ann. Surg., 171, ) Dunbar, J.D. (1966) Reversible cecal infarction. A case report with angiographic follow-up. Amer. J. Surg., 112, ) Kaminski, D.L., Keltner, R.M. & Willman, V.L. (1973) Ischemic colitis. Arch. Surg., 106, ) Kilpatrick, Z.M., Farman, J., Yesner, R. & Spiro, H.M. (1968) Ischemic proctitis. J. Amer. med. Ass., 205,

11 Ischemic Colitis ) Marcuson, R.W. & Farman J.A. (1971) Ischaemic disease of the colon. Proc. roy. Soc. Med., 64, ) Marshak, R.H., Lindner, A.E. & Ruoff, M. (1974) The radiology corner: ischemic colitis. Amer. J. Gastroent., 61, ) Marston, A. (1971) Irreversible vascular lesions of the colon. In: Vasculr Disorder of the Intestine, edited by S.J. Boley, S.S. Schwartz & L.F. Williams, Jr., Appleton -Century Crofts, New York, pp ) Marston, A., Pheils, M.T., Thomas, M.L. & Morson, B.C. (1966) Ischemic colitis. Gut, 7, ) Miller, W.T., De Poto, D.W., Scholl, H.W. & Raffensperger, E.C. (1971) Evanescent colitis in the young adult: a new entity? Radiology, 100, ) Moller, C. & Stjernvall, L. (1971) Ischaemic colitis. Acta chir. Scand., 137, ) Petigrow, N. & Ludwig, W.M. (1971) Ischemic colitis associated with carcinoma of the sigmoid colon. Amer. J. Gastroen.t., 56, ) Rickert, R.R., Johnson, R.G. & Wignarajan, K.R. (1974) Ischemic colitis in a young adult patient: report of a case. Dis. Colon. Rect., 17, ) Ross, S.T. (1972) Ischemic colitis. Postgrad. Med., 51, ) Thomas M.L. & Wellwood, J.M. (1973) Ischaemic colitis and abdomino-perineal excision of the rectum. Gut, 14, ) Westcott J.L. (1972) Angiographic demonstration of arterial occlusion in ischemic colitis. Gastroenterology, 63, ) Whitehead, R. (1971) Ischaemic enterocolitis: an expression of the intravascular coagulation syndrome. Gut, 12, ) Williams, L.F., Bosniak, M.A., Wittenberg, J., Manuel, B., Grimes, E. T. & Byrne, J.J. (1969) Ischemic colitis. Amer. J. Surg., 117,