ANGIOGRAPHIC LOCALIZATION OF GASTROINTESTINAL BLEEDING
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1 GASTROENTEROLOGY Copyright 1968 by The Williams & Wilkins Co. Vol. 54, "0. 5 Print.d;n U.S... I ANGIOGRAPHIC LOCALIZATION OF GASTROINTESTINAL BLEEDING STEWART R. REU1'ER, M.D., AND JOSEPH J. BOOKSTEIN, M.D. Department of Radiology, The University of Michigan, Wayne County General Hospital, Eloise, Michigan, and The University H os pital, Ann Arbor, Michiua n Selective visceral angiography is assuming an important role in the radiological investigation of gastrointestinal bleeding. Nusbaum and Baum 1 were the first to use angiography for the demonstration of active bleeding. In experimental animals they showed accumulation of contrast media at the site of bleeding when blood loss was 0.5 ml per min or more. Subsequent clinical application of the method revealed the site of active bleeding in 18 of 21 patients with bleeding from gastric or duodenal ulcers or Mallory-Weiss esophageal tears.2 Koehler and Salmon 3 have also shown the site of active bleeding in 4 patients. In addition to showing active bleeding, angiography has also been useful in demonstrating lesions which have been the cause of chronic, intermittent bleeding. These lesions have included angioma or arteriovenous malformation,4 tumor,5 and inflammatory disease. 6 We have now demonstrated active bleeding sites in 11 patients and chronic bleeding sites in 9. Our experience in these patients is presented to encourage a more widespread acceptance of this important diagnostic method. This experience is combined with that of others to formulate the role of angiography in the radiological investigation of the bleeding patient. Materials and Methods We have performed angiography in 29 patients with gastrointestinal bleeding. Sixteen were bleeding actively and 13 had chronic, unexplained melena. Three of these patients had been reported previously.7 Patients with hema- R eceived November 14, Accepted December 26, Address requests for reprints to: Stewart R. R euter, M.D. Department of Radiology, Wayne County General Hospital, Eloise, Michigan temesis were examined with celiac and superior mesenteric angiography and those with rectal bleeding, with superior and inferior mesenteric angiography. Patients with recurrent melena had celiac, superior mesenteric, and inferior mesenteric angiographies. Angiography was performed by the percutaneous technique via a femoral artery. For celiac and superior mesenteric angiographies in act iye bleeders 35 to 40 ml and in chronic bleeders 30 ml of 76% Renografin (Squibb, Inc.) were injected at the rate of 12 ml per sec. For inferior mesenteric angiography 20 ml of 60% Renografin were injected at 7 ml per sec. For all studies filming was done at the rate of t.wo films per sec for 5 sec, then one film per sec for 5 ~ e c, and one film every other sec for 10 sec. Results In the 16 patients with active bleeding. the bleeding site was demonstrated in 11. One patient was bleeding from a M allory-weiss tear of the esophagus (fi g. ll. 2 from lesser curvature gastric ulcers, 1 from a previously unsuspected gastric carcinoma, 2 from duodenal ulcers, 1 from hypertrophic gastritis, 1 from a s mall bowel metastasis, 2 from colonic diycl' ticula (fig. 2), and 1 from uremic ulceration of the colon (fig. 3). Failure to demonstrate the bleeding site in 2 patients wa ~ probably due to cessation of bleeding bcfore the a ngiogram. In an additional 2, the left gastric artery did not arise from the celiac axis, and blood supply to the stomach was, therefore, not demonstrated. In the remaining patient, a m a l ed ' l k' ~ obese man, the bleeding area (ascendin g: colon) was not included on the fi lms..-\ II patients in whom active bleeding wa ~ demonstrated angiographically were s u b e ~ quently operated upon and the bleeding site was confirmed at surgery. Opera ti o1 was performed in 3 of the 5 patien ts in whom no bleeding site was demonstrated
2 May 1968 LOCALIZATION OF BLEEDING FIG. 1. Midarterial phase of celiac angiography in an alcoholic, 47-year-old male with hema temesis. Contrast medium leaks into a Mallory-Weiss tea r (--» and runs up the esophagus. 877
3 FIG. 2. Superior mesenteric angiography in a 64-year-old female with rectal bleeding. A, early arterial phase. Atherosclerotic changes are seen in the main SMA (i---». The right colic branch (--» has a tortuous course, and some early leakage of contrast medium is seell in the region of the hepatic flexure. B, venous phase. Two well defined collections of COlltrHRt, mprlillm (--» }1m R,"pn in the ascending colon near the hepatic flexure.
4 FIG. 3. Superior mesenteric angiography in a 15-year-old female with massive rectal bleeding. A, arterial phase. Contrast medium is leaking from branches of the middle colic artery into the lumen of the distal transverse colon (~). B, venous phase. A dense accumulation of contrast medium is seen in the colonic lumen. 879
5 880 REUTER AND BOOKSTEIN Vol. 54, No.5 FIG. 4. Superior mesenteric angiography in a 55-year-old female with recurrent rectal bleeding. A, arterial phase. Early venous drainage (-» is seen from the ascending colon. B, late arterial phase. The dense venous drainage (-» of the A-V fistula is seen. angiographically. In 2 patients, no bleeding site was found at surgery. The 3rd patient was bleeding from a diverticulum in the ascending colon. In the 13 patients examined because of recurrent melena, the probable bleeding site was demonstrated angiographically in 9. Two patients had colonic arteriovenous malformations (fig. 4), 1 had hereditary telangiectasia with a large telangiectasis in the stomach, 1 had an aneurysm of the gastroduodenal artery in the base of an ulcer at a Roux-en-Y anastomosis, 1 had an aneurysm on the marginal artery of the left colon, 1 had a cecal carcinoma which had not been demonstrated at a previous barium enema, 1 had a small sigmoid polyp, and 1 had an infarct due to occlusion of a small branch of an ileal artery. One patient had cirrhotic arterial changes within the liver, and although varices were not demonstrated at arteriography, a follow-up splenoportography revealed a splenic and portal vein occlusion with development of gastric and intestinal varices. The two arteriovenous malformations, the gastroduodenal aneurysm, and the cecal carcinoma were resected. Because of clinical considerations the fell1all1ll1g patients were not explored. In 2 of the 4 patients in whom no lesion was founel at angiography to explain the bleeding, surgery also failed to reveal the cause. In the 3rd, a small bowel lymphangioma was discovered at surgery; the 4th was not explored. Case Reports Two case reports are presented which illustrate the usefulness of angiography in the diagnosis of gastrointestinal bleeding. Case 1: A 55-year-old woman had had intermittent rectal bleeding for 6 months. Repcalt'd upper gastrointestinal series and barium I'm' mas, as well as two prior exploratory laparotomies, had not revealed the cause of bleeding..\ t the second la.parotomy 38 em of normal small bowel were resected empirically in an ;lttelll[jr to remove the bleeding site. The physical examination on admif'sion \\':1." normal. Sigmoidoscopy, barium enema, and upper gastrointestinal examinations were l10rmn I. Superior and inferior mesenteric angiography was performed at a time when the pa tient \ :. VI ~ not actively bleeding. These studies demollstrated a small arteriovenous fistuh in the colon near the hepati c flexure (fig. 4). TIlt' ;11'('"
6 May 1968 LOCALIZATION OF BLEEDING 881 was supplied by a branch of the middle colic artery. Ten days after admission the patient again began to bleed actively, passing large clots of bright red blood per rectum. Abdominal exploration revealed no obvious abnormality of the intestinal surface to inspection. Palpation was also normal except for a minute, questionably polypoid lesion in the ascending colon near the hepatic flexure. The surgeon commented that this lesion could easily have been missed had he not been specifically alerted to the hepatic flexure as a probable bleeding site byangiography. A colotomy revealed a 2- by 3-mm mucosal ulceration near the hepatic flexure with a small clot at its base. Removal of the clot produced arterial bleeding. The area was excised. The histological diagnosis was arteriovenous malformation. In the 6 months since surgery there has been no recurrence of the gastrointestinal bleedmg. Case 2: A 15-year-old girl with chronic glomerulonephritis had been maintained on an artificial kidney for 1 year. Following a routine dialysis, she developed massive rectal bleeding requiring 100 U of blood in 1 week. Barium examinations were normal. Angiography was performed and contrast media collected in the transverse colon near the splenic flexure (fig. 3). A branch of the middle colic artery supplied the bleeding site. A transverse colectomy was performed immediately after the angiography. No bleeding site was seen at the time of the surgery, although several superficial ulcerations were present. Following the colectomy, no further bleeding occurred, but the patient developed a pelvic abscess and septicemia and, after a downhill course for 1 week, expired. Discussion Two radiological approaches are applicable to the investigation of the patient with gastrointestinal bleeding: barium examination and angiography. The two methods are complementary, and best applied under different circumstances. It should be emphasized that, in patients with intermittent, currently inactive, or minimal gastrointestinal bleeding, barium should still be used. Esophagrams, upper gastrointestinal series, and barium enemas will indicate the source of bleeding in the majority of such patients. Angiography should be used when conventional barium studies have failed to explain the gastrointestinal bleeding. It is in this group of patients that arteriovenous malformations, tumors, hereditary telangiectasis, regional enteritis, aneurysms, and bowel infarctions may be identified angiographically. In patients with active bleeding, barium studies frequently do not reveal the site of bleeding. The gastrointestinal series may be difficult to perform because the patient is often in near shock and uncooperative, and intravenous administration of blood and fluids makes the manipulation of the patient awkward. Moreover, the presence of blood and clots in the intestinal tract may mask the lesion and make interpretation difficult. On the other hand, angiography is most accurate in the actively bleeding patient. Not only is it capable of demonstrating the underlying lesion, but the bleeding itself will usually be seen as a localized intraintestinal accumulation of contrast medium. It is important to stress that the more active the bleeding, the more reliable the angiography. Baum et al. perform angiography only on those patients bleeding so actively that the decision to perform surgery has already been made. 8 Bleeding from varices will not be demonstrated directly, but the varices may be seen in the venous phase. 9 Even if varices are not seen, the cirrhotic appearance of the intrahepatic Yessels 10 and the enlarged spleen with development of portosystemic collateral flow, seen in the venous phase, will indicate portal hypertension. If the patient is known to be bleeding actively, we prefer to do angiography first. If the angiography does not provide a diagnosis and if the patient can be stabilized, barium studies may still be performed. On the other hand, the use of barium usually precludes the use of angiography for a few days because of the barium retention. Thus, in an actively bleeding patient requiring an urgent diagnosis, prior use of barium may render angiography ineffective. When bleeding is severe enough to,varrant emergency surgery, the importance of correct preoperative localization of the bleeding site cannot be overemphasized.
7 882 REUTER AND BOOKSTEIN Vol. 54, No. 5 Exploratory laparotomy is largely outmoded as a diagnostic procedure. If bleeding is from varices, laparotomy is contraindicated. The presence of intraabdominal adhesions from prior laparotomy or previous infections may make a thorough examination of the bowel difficult or impossible. When faced with an intestine full of blood at laparotomy the surgeon may find it impossible to localize the bleeding source, especially if the bleeding has ceased. When the bleeding occurs from an extensive diverticulosis, precise identification of the diverticulum responsible for the bleeding is often impossible, and an extensive partial colectomy may be necssary. Small arteriovenous ma lformations are particularly difficult to detect at surgery. Inability to identify the site of bleeding at laparotomy has at times led to a blind bowel resection, which ordinarily proves to be therapeutically ineffective. The cause of active bleeding is often known from the history or from a previous barium examination. These patients do not require angiography, and may be operated upon directly if necessary. All other severely bleeding patients requiring surgery should have angiography, performed on an emergency basis on the way to the operating room. In experienced hands, the procedure will require 30 to 45 min. The films can b e developed and interpreted while the patient is transferred to the operating room, and a knowledge of the bleeding site is in the hands of the surgeon before the knife. The angiographic findings in some of the lesions of the small bowel and colon which cause bleeding have been described. 6 Several tumors, such as leiomyoma, carcinoid, and carcinoma, have typical angiographic appearances. An arteriovenous malformation is identified by the early venous drainage from the lesion in addition to the vessels in the lesion itself. An infarct is identified by the abrupt t ermination of a vessel and collateral filling to the infarcted segment of bowely One complication was encountered in the present group of patients. A 29-yearold woman with upper gastrointestinal bleeding from hypertrophic gastritis was in shock at the t ime of angiography. During the examination the pulse in the left femoral artery disappeared. The examination was quickly completed and tlw catheter was removed. The films showed active bleeding from the stomach. Emergency gastrectomy was required and t h i ~ prevented prompt surgical correction of the femoral occlusion. Several weeks after the gastrectomy, the thrombosis of t lw femora l artery was removed but the pubc did not return to the foo t and subsequent amputation was necessary. H alpern12 ha:, reported an increased number of angiographic complications in patients with decreased cardiac output, and extreme ca re' must be exercised when examining p a t i e n t ~ in shock. It is important to have a clinician in attendance during the angiographic ex amination of bleeding patients to monitor vital signs and p eripheral pulses and to supervise the proper administration of fluids. This patient also demonstrates the importance of immediate surgical correction of angiographic complications.] :: Thrombosis is a rare complication oi angiography, and the benefit of preoperative identification of the site of bleeding far outweighs the risks of the examination. Summary The site of gastrointestinal bleeding ha ~ been shown by angiography in 11 of 16 patients with active bleeding and in 9 of 13 with chronic, intermittent b l e e d i n ~. Our experience in these patients has led U ~ to suggest the following radiological approach. If a patient is bleeding adin'b' ~ i. t e a n g i o g rc ahl l p~ ' l l i from an unknown gastrointestinal angiography should be performed a ~ the initial radiological procedure. If no blec:d ing site is demonstrated and the patient can be :;;tabilized, bariul1j examinations should then be done. III patients with chronic, intermittent blf edillg. barium examinations should be the iuitial radiological procedure. If no lesion is delllonstrated, angiography should thell h ~ l used. R E F E R E ~ C E S 1. Nusbaum, M., and S. Baum R,vliugraphic demonstration of unknown sitl' ':' of
8 May 1968 LOCALIZATION OF BLEEDING 8 8 : ~ gastrointestinal bleeding. Surg. Forum 14: Baum, S., M. Nusbaum, H. R. Clearfield, K. Kuroda, and H. P. Tumen Angiography in the diagnosis of gastrointestinal bleeding. Arch. Intern. Med. 119: Koehler, P. R., and R. B. Salmon Angiographic localization of unknown acute gastrointestinal bleeding. Radiology 89: Wholey, M. H., K. M. Bron, and J. D. Haller Selective angiography of the colon. Surg. Clin. ~ Amer.. 45: Boijsen, E., and S. R. Reuter Angiography in the diagnosis of chronic unexplained melena. Radiology 89: Boijsen, E., and S. R. Reuter Angiography in the evaluation of inflammatory and neoplastic disease of the intestine. Radiology 87: Frey, C. F., E. Colvin, S. M. Lindenauer, H. J. Bartle, and J. J. Bookstein Use of arteriography in the diagnosis of occult gastrointestinal and traumatic intra-abdominal hemorrhage. ArneI'. J. Surg. 113: Baum, S., M. Nusbaum, \V. S. Blakemore, and A. K. Finkelstein The pre-operative radiographic demonstration of intraabdominal bleeding from undetermined sites by percutaneous selective celiac and superior mesenteric arteriography. Sl1l'gery 58: Boijsen, E., C. A. Ekman, and T. Olin Celiac and superior mesenteric angiography in portal hypertension. Acta ChiI'. Scand. 126: Boijsen, E Selective angiography of the celiac axis and superior mesenteric artery in cirrhosis of the liver. Rev. Int. Hepat. 15: Aakhus, T The value of angiography in superior mesenteric artery embolism. Brit. J. Radiol. 39: Halpern, M Percutaneous transfemoral arteriography. ArneI'. J. Roentgen. 92: Lang, E Prevention and treatment of complications followiug arteriography. Radiology 88:
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