Arteriovenous Malformations of the Colon Patrick F. Hagihara, MD, Lexington, Kentucky Vincent P. Chuang, MD,’ Lexington, Kentucky Ward 0. Grlffen, MD, PhD, Lexington, Kentucky
of the colon are increasingly recognized as one of the major causes of massive rectal bleeding of colonic origin. Unfortunately, many of these vascular malformations are small, requiring for detection an experienced angiographer and sophisticated radiologic equipment including serial magnification potential, which is not yet widely available. Thus, detection of arteriovenous malformations of the colon at times must of necessity depend upon a combined approach of conventional visceral angiography, colonoscopy, and operative judgment. However, the ultimate diagnosis and proof of correct surgical extirpation must rest on the histologic demonstration of these vascular malformations on sectioning the suspected lesions from the excised specimen. Four cases of arteriovenous malformations of the colon have been seen at the University of Kentucky Medical Center (UKMC). The fourth ease was detected since the angiography unit was equipped with magnification capabilities. The cases illustrate the diagnosis of arteriovenous malformations of the colon by the combined approach and its confirmation by both gross and histologic examination of the excised specimen. (Arteriographic features of the vascular malformation in case I (DN) have been previously presented [I].)
Arteriovenous
malformations
Case Rqorts Cam I. DN, a sixty-six year old white male was admitted to UKMC on October IS,1973 with rectal bleeding. Four years prior to admission he developed iron-deficiency anemia. He had a thorough work-up which included barium enema followed by air-contrast enema, upper gastrointestinal series, coagulation studies, and proctoscopy. From the Oepertmems of Sugmy end Ftadlofogy’, University of Kentucky, Co@te of hdiche and Veterans Administration Hospital. Lexington, Kentucky. Reprtnt requests should be addressed to Patrick F. Hagitwa. MD, Department of Svgery. University of Kentucky Gobegs of Medicine. Lexln@~n. Kentucky 40506.
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Results of these examinations were all within normal limits. Since then he had repeated episodes of rectal bleeding and received unknown quantities of blood in transfusion. He had a total of five upper gastrointestinal series, five barium enemas, and several repeat coagulation studies-all of these were again within normal limits. On admission, his vital signs were stable and his rectal bleeding was subsiding. Proctoscopy was negative to 15cm except for blood clots in the rectum. Coagulation studies including platelet counts, prothrombin time, and partial thromboplastin time were within normal limits. After adequate blood transfusions, visceral arteriography was obtained. Selective superior mesenteric arteriography demonstrated a large cluster of arteriovenous malformations in the cecum in the distribution of the ileocolic artery. There were no other detectable vascular abnormalities. Ten days after admission he underwent operation. The cecum and right colon were normal on inspection and palpation. The ileocolic vein was somewhat enlarged. Right hemicolectomy with ileotransverse colostomy was performed. The excised specimen was opened and washed of its contents. Several ulcers were easily seen on the mucosal surface of the cecum. (Figure 1.) Histologic sections through one of the ulcers revealed art.eriovenous malformations. (Figure 2.) His postoperative course was uneventful. Since discharge from the hospital, he has remained well without rectal bleeding for two and a half years. Case II. RP, a fifty-four year old white female was admitted to UKMC on January 22,1975 for the second time with rectal bleeding. Her two initial episodes of rectal bleeding, four years prior to her current admission, led to vagotomy-pyloroplasty for duodenal ulcer. Since then she had three episodes of rectal bleeding requiring 5 units of blood in transfusion. She had innumerable upper gastrointestinal series, coagulation studies, proctoscopies, and barium enemas. The only abnormality found was divertitular disease of the colon. During one of the episodes, she was admitted to UKMC for the first time and had an upper gastrointestinal series and gastroscopy, which revealed no abnormalities. Selective superior mesenteric and inferior mesenteric arteriography was performed during the active phase of the rectal bleeding. No abnormality was detected.
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F&we 1. Case I. ht~lt&k cecal ukers ranghg up 2 to mm are easily vlslble wtthout compression maneuver.
Colonoscopy without fluoroscopic control was negative to the left transverse colon. On her current admission she had been bleeding for eight days, requiring transfusion of 4 units of blood. Coagulation studies including platelet counts, prothrombin time, and partial thromboplastin time were within normal limits. Although an upper gastrointestinal series suggested an ulcer in the deformed duodenal bulb, gastroscopy revealed only mild gastritis. Aortogram with selective celiac and superior mesenteric arteriographies performed during her active bleeding revealed no abnormality. The colon was thoroughly irrigated with normal saline, and colonoscopy was performed under fluoroscopic control. A raised bright red vascular malformation was seen in the cecum pulsating with arterial and venous channels feeding the malformation. (Figure 3.)
F@re 2. Case I. Section thmu@ one of the ukers. Cbstefs of vascular ma/formstlons and fibrosis at the base of the ulcer. Large vascular takes in the mucosa. (Hematoxylin and eosin stain; 0rtghal magn/ficathm X 63.5; reduced 30 per cent.)
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After transfusion of 11 units of blood, she underwent a limited resection of the cecum with a portion of the terminal ileum. The resected specimen was immediately opened and washed of its content. Nothing could be seen on simple inspection of the mucosal surface. The mesenteric vessels of the resected specimen were clamped, the resected ends of the specimen were compressed, and the mucosa was effaced. A small depressed defect was visible on the mucosal surface with faint outline of a vessel leading to the mucosal defect. (Figure 4.) Sutures were placed through the mucosa immediately next to the defect for the purpose of identification. On standing for 1 to 2 hours, this
Figure 3. Case II. An endoscopk view of a cecal vascular ma/format/on with a raised hemanglomatous area and its arterial and venous connections.
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FIgwe 4. Case II. The excised specimen. The vascular m8Normatlon seen 8s 8 Ml811 depressed 8re8 under compression maneuver. A faini outllneof8vesselhwdfngthe&pressed 8re8 is also visible.
defect could not be seen on gross inspection even with the compression maneuver. Histologic sections through this identified area revealed arteriovenous malformations. (Figure 5.) Her postoperative course was uneventful. She has had no recurrent rectal bleeding for more than one and a half years since the operation. Case III. EW, a seventy-two year old white female was admitted to UKMC for the second time with rectal bleeding on May 26, 1973. For thirty-one years prior to admission she had been having intermittent rectal bleeding, with increasing frequency in the last eight years. Examinations including sigmoidoscopies, barium enemas, upper gastrointestinal series, and coagulation studies were within normal limits on several occasions except for prominent hemorrhoids. Seven years prior to admission she underwent hetnorrhoidectomy. During one of her bleeding episodes, she had been admitted to UKMC for the first time for one week. Sigmoidoscopy, upper gastrointestinal series with small bowel follow-through, and barium enema were within normal limits except for divert&la in the sigmoid. She received 2 units of blood in transfusion. She was offered a sigmoid resection, which she declined. On her current admission to UKMC proctoscopy was negative to 14 cm except for blood in the rectum. Coagulation studies including platelet counts, prothrombin time, and partial thromboplastin time were within normal limits. While she was actively bleeding, she underwent abdominal aortogram with selective celiac and superior mesenteric arteriographies. &O bleeding point or vascular malformation was detected. She also had colonoscopy to the left. transverse colon during the active phase of the bleeding; no abnorma1it.y was seen. She received 2 units of whole blood in transfusion followed by 5 units of lymphocytepoor blood because of her febrile reaction to the whole blood. She underwent operation eleven days after the admission. The terminal ileum was first opened. No blood was
Volume 133, Juno 1977
seen. Thus, subtotal colectomy was performed including the diverticula-hearing portion of the sigmoid colon. The intestinal continuity was reestablished by ileoprtctostomy. The excised specimen was immediately opened and its content washed out. The vascular pedicles of the specimen were clamped and small segments of the specimen were compressed on both ends at a t.ime until the entire colonic mucosal surface was examined. A pinpoint opening was found in the mucosa of the transverse colon from which blood could be expressed. Moreover. this compression maneuver brought out a vessel feeding the defect. (Figure 6.) A suture was placed near the mucosal defect and the specimen was submitted to pathologic examination. Mutiple sections were taken of the area marked with the suture. The histologic sections revealed arteriovenous malformations. (Figure 7.)
Figure 5. Case Il. L8rge vasculsr lakes in the mucosa. Clusters of anomalous vessels In the submucosa. (Hematoxylln and eosin stain: original magnification X 63.5; reduced 30 per cent.)
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Figure 6. Case iii. Under compression maneuver, blood is expressed from a pinpoini opening in the mucosa of the transverse colon. A small tortuous artery feeding the opening is faintly visible.
Figure 7. Case ill. Clusters of anomalous vessels in the submucosa extending into the mucosa. (ifematoxylin and eosin stain; original magnification X 63.5; reduced 30 per cent.)
Figw? 6A. Case IV. Magnification angiography (2X) of the iieocolic artery; arierial phaSe. The slightly enfeedfng larged artery (cfosed arrows), the vascular lake (the arterioverwus ma/formation itseif, iarge closed arrows), and the ear/y draining vein (open arrows) are seen.
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Her postoperative course was uneventful. After the operation and adequate blood volume replacement, a repeat physical examination revealed a small vascular malformation on her lower lip and tortuous aneurysmal blood vessels under the tongue. She remained free of rectal bleeding for three years. Case IV. RH, a forty-three year old white female was admitted to UKMC on February 24,1976. Two years prior to admission she had her first episode of rectal bleeding. Two months prior to admission she had another episode requiring blood transfusions. Upper gastrointestinal series and sigmoidoscopy were negative. Barium enema was thought to be suspicious of “ulcerative colitis.” Just prior to admission she had her third episode of rectal bleeding. Gastroscopy and colonoscopy to 40 cm during her active bleeding proved negative. Repeat barium enema was noninformative.
Figure 86. Capillary phase of the angiogrem. Persistence of the vascular lake (skrgle closed arrow) and welt opacified prominent early draining vein (open arrows).
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Malformations
Upon her admission to this hospital, sigmoidoscopy, barium enema, and upper gastrointestinal series were performed, all negative. Subsequently, selective celiac, superior mesenteric, and inferior mesenteric arteriography was performed. The superior mesenteric arteriogram with magnification showed an arteriovenous malformation in the cecum with early venous drainage. (Figures 8A and B.) Nine days after the admission she underwent right hemicolectomy. Intraoperative colonoscopy revealed a bleeding point in the cecum. The excised specimen revealed an easily recognized 2 mm ulcerated area in the cecum. Histologic sections of the area showed arteriovenous malformations. Comments
In the 1950s when the concept of diverticular bleeding of the colon had barely been accepted and
Hagihara, Chuang, and Griffen
the concept of bleeding from small vascular malformations of the colon was unknown, the cases of rectal bleeding which eluded all preoperative efforts at diagnosis remained undiagnosed even after laparotomy 30 to SO per cent of the time. In a review by Retzlaff, Hagedorn, and Bartholomew 121,of 100 patients at the Mayo Clinic who had documented gastrointestinal bleeding of various magnitude without hematemesis and had no diagnosis established after appropriate and often repeated laboratory studies, 53 still remained without diagnosis after exploratory laparotomy. Among 47 patients with a clear-cut or indeterminate diagnosis after exploratory laparotomy, only 2 had lesions in the colon-both carcinomas of the colon. One can only suspect that a large majority of those with massive bleeding remaining without diagnosis might have had either diverticular disease or arteriovenous malformations of the colon as the basis of their bleeding. Due to the work of Noer [3,4] and others [5-8] diverticular disease of the colon had been accepted as the major colonic cause of massive rectal bleeding. Mere presence of diverticula in the colon in the absence of other possible causes had constituted presumptive evidence for diverticular bleeding. In a great majority of the colons removed for bleeding, histologic proof of diverticular bleeding could not be established [9]. Sampling errors due to the numerous diverticula encountered in the excised colon might have been one reason for the lack of histologic proof. In some, undetected arteriovenous malformations might have been another reason. Prior to arteriographic demonstration of vascular malformations of the gastrointestinal tract, the malformations had been grouped as either capillary or cavernous hemangiomas. While reporting a case of hemangioma of the colon, Ruis-Moreno (101 surveyed the literature up to 1961 and found only 16 cases of hemangioma of the colon reported; most vascular malformations of the gastrointestinal tract, particularly small ones, are usually invisible on the serosal surface. Moreover, small vascular malformations are undetectable on casual inspection of the mucosal surface of the excised colon. Since the first arteriographic demonstration of a bleeding arteriovenous malformation of the cecum by Margulis, Heinbecker, and Bernard ]1 I] in 1960 and largely through the clinical and experimental studies on angiographic technic in the detection of gastrointestinal bleeding by Raum and Nusbaum (12-14). arteriovenous malformations of the gastrointestinal tract have become recognized as a major cause of gastrointestinal bleeding. Baum and Nusbaum 123,141 were able to define blood vessels as
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small as SOto 90 ~1by serial magnification on visceral angiography, thus considerably increasing the chances of detecting small vascular malformations. Alfidi et al [15] performed visceral angiography on twelve patients whv had recurrent gastrointestinal bleeding and had remained without diagnosis despite repeated and adequate laboratory studies. All patients had arteriovenous malformations of the bowel. Subsequently, Alfidi [16] reported on a total of twenty arteriovenous malformations of the bowel det.ected at the Cleveland Clinic. Angiographically, an arteriovenous malformation consists of a slightly enlarged feeding artery, a vascular lake, and an early draining vein. The feeding artery and the vascular lake (the arteriovenous malformation itself) may vary from very obvious to very subtle, and they may be at times difficult to detect unless magnification angiography is performed. However, the early draining vein is usually very prominent and tends to. parallel the feeding artery. This early draining vein is almost invariably visualized in the late arterial phase when the peripheral branches of the mesenteric arteries and the vasa rectae are still opacified by the contrast medium. Thus, if the lesion is not readily apparent, it is important to search for the early draining, enlarged vein in the venous phase of the mesenteric angiogram and then trace it back to the arterial phase. Using this approach, one of us correctly diagnosed the site of’ vascular malformations in case II and ascertained approximate site in case III in retrospect without clinical history. Thus, selective mesenteric angiography is a reliable method of making the diagnosis if competent angiographic interpretation and technical expertise are available. In a patient with chronic recurrent lower gastrointestinal hemorrhage, in whom conventional examination including proctoscopy and barium enema have been negative, mesenteric angiography is indicated. Arteriovenous malformations of the colon are not ordinarily detected by barium enema. If lower gastrointestinal bleeding is acute and the estimated rate of bleeding is greater than 0.5 cc/min. mesenteric angiography should be performed before barium enema, for the cause of colonic bleeding, whether of diverticular origin or vascular malformations, may be detected as an extravasat ion of the contrast media into the colonic lumen. Colonoscopy has become widely available as a diagnostic tool. IJnfortunately, the examination is difficult when the bleeding is brisk. .4t times. repeated saline enemas may be able to clear the colon and also slow the rate of the bleeding, thus facilitating the colonoscopic examination and diagnosis.
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Even bleeding diverticula of the colon may be occasionally detected by this means. If visceral arteriography and colonctscopy fail to achieve the diagnosis, explorat.ory laparotomy may be the only recourse. The exploration should he done while the patient is actively bleeding and in good condit.ion. If ileotomy shows t.hat the small bowel is free of blood and thus bleeding is limited to the colon, most of the colon may be excised down to the level ot the dist.al sigmoid or upper rectum which had heen determined free of’ disease preoperatively. removing the entire diverticula-bearing colon. Thus. the suriical tnanagement is not different from that which is exercised l’or presumed diverticular bleeding of the colon. The bowel continuity is reestablished with ileoproctostomy. The excised specimen should be opened and washe:] of’ its contents immediately af’ter excision while the \.ascular pedicles of the specimen are either tied or clamped. The mucosal surface should be inspected a small segment at a time hy manually compressing the ends of the selected segment and stretching the mucosa. thus rendering the submucosal vessels prominent. A small mucosal defect tnay become visible. from which the blood may be expressed. The tnucosal defect seen in this manner may or may not he it tnucosal ulcer. It may be the site uf collapsed capillaries and vascular spaces in the tnucosa as in case I I. I;nless the defect and feeding vessels are precisely marked wit.h subures immediately, they may become undet.ect.able over hours on standing. The site of small vascular malformations are completely undetectable after formalin fixation as in cases II and III. Multiple sections of the previously tnarked site will accurately locate the vascular malfortn;~tiotts f’or histologic examination. In some cases. tirrcosal ulcers associated with vascular malf’ormations are large and easily detectable. Alternatively, one of several materials may be used to distend the arteriovenous malformation in the resected specimen and thus facilitate identification of the malformation. Shlesinger gelatin mass, methyl methacrylate (TensolTM cement #7) and Microfil (silicon rubber; Canton biomedical product) are examples [ I6,lRj. Precise s\tr#ical extirpation ol‘ vascular tnalformations in the stnall bowel must of necessity depend upon angiography. Operative visceral angiography may aid in precise localization and resection of the bleedin:: vascular malformations of the small bowel. Hoive\.tlr. sttch ef’f’orts may not be t’ruitful unless surgical operations are performed in a radiology room that is f’ully equipped for ;qiography [ 15).
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Arteriovenous
Malformations
Summary .4rteriovenous malformations have become recognized as a major cause of massive bleeding of the colonic origin. Although an arteriographic unit capable of serial magnification is ideal for detecting arteriovenous malformations in the bowel, t.he diagnosis tnay still he made hy a combined approach of convent.ional arteriography, colonoscopy and operative judgment. The final diagnosis rests on gross and histologic demonstration of’ vascular malformations in the excised specimen. References 1. Hernandez GE. Durnin RE, Hagihara. PI? Arterievenous rnalformation of the colon: case report. J Ky A&d Assoc 72: 488. 1974. 2. Retzlaff JA. Hagedom AB. Bartholomew LG: Abdominal exploration for gastrointestinal bleeding of obscure origin. JAMA 177: 94. 1961. 3. Noer RJ: Hemorrhage as a complication of diverticulitis. Ann Surg 141: 674, 1955. 4. Noer RJ, Hamilton JE, Williams DJ. Broughton DS: Rectal hemorrhage: moderate and severe. Ann Surg 155: 794, 1962. 5. Rives JD, Emmett RO: Melena. A survey of 206 cases. Am Sung 20: 456, 1954. 6. Mobley JE. Dockerty MB. Waugh JM: Bleeding in colonic diverticulitis. Am J Surg 94: 44, 1957. 7. Rosser C: The surgical management of diverticulitis. SouN, &d d32: 1203, 1939. 8. Fansler WA: Diverticulosis and diverticulitis-with particular reference to the large bowel. Trans Am Proctology Sot 4 1: 231. :940. 9. Rigg BM. Ewing MR: Current attitudes on diverticulitis with particular reference to colonic bleeding. Arch Surg 92: 32 1, 1966. 10. Ruiz-Moreno f: Hemangiomatosis of the colon: report of a case. Dis Colon Rectum 5: 453, 1962. 11. Margulis AF, Heinbecker P, Bernard H: Operative mesenteric arieriography in the search for the site of bleeding in unexplained gastrointestinal hemorrhage. Surgery 48: 534. 1960. 12. Baum S, Nusbaum M. Ctearfield HR. Kurcxla K, lumen HJ: Angiography in the diagnosis of gastrointestinal bleeding. Arch Intern h&d 119: 16. 1967. 13. Baum S, Nusbaum M, Kuroda K. BlAkemore WS: Direct serial magnification arteriography as an adjuvant in the diagnosis of surgical lesions of the alimentary tract. Am J Sufg 117: 170. 1969. 14. Nusbaum M, Baum S. Blakemore WS: Clinical experience with the diagnosis and management of gastrointestinal hemorrhage by selective mesenteric catheterization. Ann Surg 170: 506. 1969. 15. Alfidi RJ, Esselstyn CD. Tarar R. Klein KI. Hermann RE. Weakley FL. Turnbull RB: Recognition and angio-surgical detection of arteriovenous malformations of the bowel. Ann Surg 174: 573, 1971. 16. Alfidi RJ: Angiography in identifying the source of intestinal bleeding. Dis Co/on Rectum 17: 442. 1974. 17. Genant HK. Ranniger K: Vascular dysplasia of the ascending colon. Report of two cases and review of the literature. Am J Roentgenol Radium Ther Nucl Med 115: 349. 1972. 18. Baum S: Small vessel angiography of the gut, chapt 34, p 454. Small Vessel Angiography (Hilal SK. ed). St. Louis. CV Mosby. 1973.
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of the colon are increasingly recognized as one of the major causes of massive rectal bleeding of colonic origin. Unfortunately, many of these vascular malformations are small, requiring for detection an experienced angiographer and sophisticated radiologic equipment including serial magnification potential, which is not yet widely available. Thus, detection of arteriovenous malformations of the colon at times must of necessity depend upon a combined approach of conventional visceral angiography, colonoscopy, and operative judgment. However, the ultimate diagnosis and proof of correct surgical extirpation must rest on the histologic demonstration of these vascular malformations on sectioning the suspected lesions from the excised specimen. Four cases of arteriovenous malformations of the colon have been seen at the University of Kentucky Medical Center (UKMC). The fourth ease was detected since the angiography unit was equipped with magnification capabilities. The cases illustrate the diagnosis of arteriovenous malformations of the colon by the combined approach and its confirmation by both gross and histologic examination of the excised specimen. (Arteriographic features of the vascular malformation in case I (DN) have been previously presented [I].)
Arteriovenous
malformations
Case Rqorts Cam I. DN, a sixty-six year old white male was admitted to UKMC on October IS,1973 with rectal bleeding. Four years prior to admission he developed iron-deficiency anemia. He had a thorough work-up which included barium enema followed by air-contrast enema, upper gastrointestinal series, coagulation studies, and proctoscopy. From the Oepertmems of Sugmy end Ftadlofogy’, University of Kentucky, Co@te of hdiche and Veterans Administration Hospital. Lexington, Kentucky. Reprtnt requests should be addressed to Patrick F. Hagitwa. MD, Department of Svgery. University of Kentucky Gobegs of Medicine. Lexln@~n. Kentucky 40506.
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Results of these examinations were all within normal limits. Since then he had repeated episodes of rectal bleeding and received unknown quantities of blood in transfusion. He had a total of five upper gastrointestinal series, five barium enemas, and several repeat coagulation studies-all of these were again within normal limits. On admission, his vital signs were stable and his rectal bleeding was subsiding. Proctoscopy was negative to 15cm except for blood clots in the rectum. Coagulation studies including platelet counts, prothrombin time, and partial thromboplastin time were within normal limits. After adequate blood transfusions, visceral arteriography was obtained. Selective superior mesenteric arteriography demonstrated a large cluster of arteriovenous malformations in the cecum in the distribution of the ileocolic artery. There were no other detectable vascular abnormalities. Ten days after admission he underwent operation. The cecum and right colon were normal on inspection and palpation. The ileocolic vein was somewhat enlarged. Right hemicolectomy with ileotransverse colostomy was performed. The excised specimen was opened and washed of its contents. Several ulcers were easily seen on the mucosal surface of the cecum. (Figure 1.) Histologic sections through one of the ulcers revealed art.eriovenous malformations. (Figure 2.) His postoperative course was uneventful. Since discharge from the hospital, he has remained well without rectal bleeding for two and a half years. Case II. RP, a fifty-four year old white female was admitted to UKMC on January 22,1975 for the second time with rectal bleeding. Her two initial episodes of rectal bleeding, four years prior to her current admission, led to vagotomy-pyloroplasty for duodenal ulcer. Since then she had three episodes of rectal bleeding requiring 5 units of blood in transfusion. She had innumerable upper gastrointestinal series, coagulation studies, proctoscopies, and barium enemas. The only abnormality found was divertitular disease of the colon. During one of the episodes, she was admitted to UKMC for the first time and had an upper gastrointestinal series and gastroscopy, which revealed no abnormalities. Selective superior mesenteric and inferior mesenteric arteriography was performed during the active phase of the rectal bleeding. No abnormality was detected.
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F&we 1. Case I. ht~lt&k cecal ukers ranghg up 2 to mm are easily vlslble wtthout compression maneuver.
Colonoscopy without fluoroscopic control was negative to the left transverse colon. On her current admission she had been bleeding for eight days, requiring transfusion of 4 units of blood. Coagulation studies including platelet counts, prothrombin time, and partial thromboplastin time were within normal limits. Although an upper gastrointestinal series suggested an ulcer in the deformed duodenal bulb, gastroscopy revealed only mild gastritis. Aortogram with selective celiac and superior mesenteric arteriographies performed during her active bleeding revealed no abnormality. The colon was thoroughly irrigated with normal saline, and colonoscopy was performed under fluoroscopic control. A raised bright red vascular malformation was seen in the cecum pulsating with arterial and venous channels feeding the malformation. (Figure 3.)
F@re 2. Case I. Section thmu@ one of the ukers. Cbstefs of vascular ma/formstlons and fibrosis at the base of the ulcer. Large vascular takes in the mucosa. (Hematoxylin and eosin stain; 0rtghal magn/ficathm X 63.5; reduced 30 per cent.)
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After transfusion of 11 units of blood, she underwent a limited resection of the cecum with a portion of the terminal ileum. The resected specimen was immediately opened and washed of its content. Nothing could be seen on simple inspection of the mucosal surface. The mesenteric vessels of the resected specimen were clamped, the resected ends of the specimen were compressed, and the mucosa was effaced. A small depressed defect was visible on the mucosal surface with faint outline of a vessel leading to the mucosal defect. (Figure 4.) Sutures were placed through the mucosa immediately next to the defect for the purpose of identification. On standing for 1 to 2 hours, this
Figure 3. Case II. An endoscopk view of a cecal vascular ma/format/on with a raised hemanglomatous area and its arterial and venous connections.
The American Journal of Surgwy
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FIgwe 4. Case II. The excised specimen. The vascular m8Normatlon seen 8s 8 Ml811 depressed 8re8 under compression maneuver. A faini outllneof8vesselhwdfngthe&pressed 8re8 is also visible.
defect could not be seen on gross inspection even with the compression maneuver. Histologic sections through this identified area revealed arteriovenous malformations. (Figure 5.) Her postoperative course was uneventful. She has had no recurrent rectal bleeding for more than one and a half years since the operation. Case III. EW, a seventy-two year old white female was admitted to UKMC for the second time with rectal bleeding on May 26, 1973. For thirty-one years prior to admission she had been having intermittent rectal bleeding, with increasing frequency in the last eight years. Examinations including sigmoidoscopies, barium enemas, upper gastrointestinal series, and coagulation studies were within normal limits on several occasions except for prominent hemorrhoids. Seven years prior to admission she underwent hetnorrhoidectomy. During one of her bleeding episodes, she had been admitted to UKMC for the first time for one week. Sigmoidoscopy, upper gastrointestinal series with small bowel follow-through, and barium enema were within normal limits except for divert&la in the sigmoid. She received 2 units of blood in transfusion. She was offered a sigmoid resection, which she declined. On her current admission to UKMC proctoscopy was negative to 14 cm except for blood in the rectum. Coagulation studies including platelet counts, prothrombin time, and partial thromboplastin time were within normal limits. While she was actively bleeding, she underwent abdominal aortogram with selective celiac and superior mesenteric arteriographies. &O bleeding point or vascular malformation was detected. She also had colonoscopy to the left. transverse colon during the active phase of the bleeding; no abnorma1it.y was seen. She received 2 units of whole blood in transfusion followed by 5 units of lymphocytepoor blood because of her febrile reaction to the whole blood. She underwent operation eleven days after the admission. The terminal ileum was first opened. No blood was
Volume 133, Juno 1977
seen. Thus, subtotal colectomy was performed including the diverticula-hearing portion of the sigmoid colon. The intestinal continuity was reestablished by ileoprtctostomy. The excised specimen was immediately opened and its content washed out. The vascular pedicles of the specimen were clamped and small segments of the specimen were compressed on both ends at a t.ime until the entire colonic mucosal surface was examined. A pinpoint opening was found in the mucosa of the transverse colon from which blood could be expressed. Moreover. this compression maneuver brought out a vessel feeding the defect. (Figure 6.) A suture was placed near the mucosal defect and the specimen was submitted to pathologic examination. Mutiple sections were taken of the area marked with the suture. The histologic sections revealed arteriovenous malformations. (Figure 7.)
Figure 5. Case Il. L8rge vasculsr lakes in the mucosa. Clusters of anomalous vessels In the submucosa. (Hematoxylln and eosin stain: original magnification X 63.5; reduced 30 per cent.)
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Figure 6. Case iii. Under compression maneuver, blood is expressed from a pinpoini opening in the mucosa of the transverse colon. A small tortuous artery feeding the opening is faintly visible.
Figure 7. Case ill. Clusters of anomalous vessels in the submucosa extending into the mucosa. (ifematoxylin and eosin stain; original magnification X 63.5; reduced 30 per cent.)
Figw? 6A. Case IV. Magnification angiography (2X) of the iieocolic artery; arierial phaSe. The slightly enfeedfng larged artery (cfosed arrows), the vascular lake (the arterioverwus ma/formation itseif, iarge closed arrows), and the ear/y draining vein (open arrows) are seen.
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Her postoperative course was uneventful. After the operation and adequate blood volume replacement, a repeat physical examination revealed a small vascular malformation on her lower lip and tortuous aneurysmal blood vessels under the tongue. She remained free of rectal bleeding for three years. Case IV. RH, a forty-three year old white female was admitted to UKMC on February 24,1976. Two years prior to admission she had her first episode of rectal bleeding. Two months prior to admission she had another episode requiring blood transfusions. Upper gastrointestinal series and sigmoidoscopy were negative. Barium enema was thought to be suspicious of “ulcerative colitis.” Just prior to admission she had her third episode of rectal bleeding. Gastroscopy and colonoscopy to 40 cm during her active bleeding proved negative. Repeat barium enema was noninformative.
Figure 86. Capillary phase of the angiogrem. Persistence of the vascular lake (skrgle closed arrow) and welt opacified prominent early draining vein (open arrows).
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Malformations
Upon her admission to this hospital, sigmoidoscopy, barium enema, and upper gastrointestinal series were performed, all negative. Subsequently, selective celiac, superior mesenteric, and inferior mesenteric arteriography was performed. The superior mesenteric arteriogram with magnification showed an arteriovenous malformation in the cecum with early venous drainage. (Figures 8A and B.) Nine days after the admission she underwent right hemicolectomy. Intraoperative colonoscopy revealed a bleeding point in the cecum. The excised specimen revealed an easily recognized 2 mm ulcerated area in the cecum. Histologic sections of the area showed arteriovenous malformations. Comments
In the 1950s when the concept of diverticular bleeding of the colon had barely been accepted and
Hagihara, Chuang, and Griffen
the concept of bleeding from small vascular malformations of the colon was unknown, the cases of rectal bleeding which eluded all preoperative efforts at diagnosis remained undiagnosed even after laparotomy 30 to SO per cent of the time. In a review by Retzlaff, Hagedorn, and Bartholomew 121,of 100 patients at the Mayo Clinic who had documented gastrointestinal bleeding of various magnitude without hematemesis and had no diagnosis established after appropriate and often repeated laboratory studies, 53 still remained without diagnosis after exploratory laparotomy. Among 47 patients with a clear-cut or indeterminate diagnosis after exploratory laparotomy, only 2 had lesions in the colon-both carcinomas of the colon. One can only suspect that a large majority of those with massive bleeding remaining without diagnosis might have had either diverticular disease or arteriovenous malformations of the colon as the basis of their bleeding. Due to the work of Noer [3,4] and others [5-8] diverticular disease of the colon had been accepted as the major colonic cause of massive rectal bleeding. Mere presence of diverticula in the colon in the absence of other possible causes had constituted presumptive evidence for diverticular bleeding. In a great majority of the colons removed for bleeding, histologic proof of diverticular bleeding could not be established [9]. Sampling errors due to the numerous diverticula encountered in the excised colon might have been one reason for the lack of histologic proof. In some, undetected arteriovenous malformations might have been another reason. Prior to arteriographic demonstration of vascular malformations of the gastrointestinal tract, the malformations had been grouped as either capillary or cavernous hemangiomas. While reporting a case of hemangioma of the colon, Ruis-Moreno (101 surveyed the literature up to 1961 and found only 16 cases of hemangioma of the colon reported; most vascular malformations of the gastrointestinal tract, particularly small ones, are usually invisible on the serosal surface. Moreover, small vascular malformations are undetectable on casual inspection of the mucosal surface of the excised colon. Since the first arteriographic demonstration of a bleeding arteriovenous malformation of the cecum by Margulis, Heinbecker, and Bernard ]1 I] in 1960 and largely through the clinical and experimental studies on angiographic technic in the detection of gastrointestinal bleeding by Raum and Nusbaum (12-14). arteriovenous malformations of the gastrointestinal tract have become recognized as a major cause of gastrointestinal bleeding. Baum and Nusbaum 123,141 were able to define blood vessels as
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small as SOto 90 ~1by serial magnification on visceral angiography, thus considerably increasing the chances of detecting small vascular malformations. Alfidi et al [15] performed visceral angiography on twelve patients whv had recurrent gastrointestinal bleeding and had remained without diagnosis despite repeated and adequate laboratory studies. All patients had arteriovenous malformations of the bowel. Subsequently, Alfidi [16] reported on a total of twenty arteriovenous malformations of the bowel det.ected at the Cleveland Clinic. Angiographically, an arteriovenous malformation consists of a slightly enlarged feeding artery, a vascular lake, and an early draining vein. The feeding artery and the vascular lake (the arteriovenous malformation itself) may vary from very obvious to very subtle, and they may be at times difficult to detect unless magnification angiography is performed. However, the early draining vein is usually very prominent and tends to. parallel the feeding artery. This early draining vein is almost invariably visualized in the late arterial phase when the peripheral branches of the mesenteric arteries and the vasa rectae are still opacified by the contrast medium. Thus, if the lesion is not readily apparent, it is important to search for the early draining, enlarged vein in the venous phase of the mesenteric angiogram and then trace it back to the arterial phase. Using this approach, one of us correctly diagnosed the site of’ vascular malformations in case II and ascertained approximate site in case III in retrospect without clinical history. Thus, selective mesenteric angiography is a reliable method of making the diagnosis if competent angiographic interpretation and technical expertise are available. In a patient with chronic recurrent lower gastrointestinal hemorrhage, in whom conventional examination including proctoscopy and barium enema have been negative, mesenteric angiography is indicated. Arteriovenous malformations of the colon are not ordinarily detected by barium enema. If lower gastrointestinal bleeding is acute and the estimated rate of bleeding is greater than 0.5 cc/min. mesenteric angiography should be performed before barium enema, for the cause of colonic bleeding, whether of diverticular origin or vascular malformations, may be detected as an extravasat ion of the contrast media into the colonic lumen. Colonoscopy has become widely available as a diagnostic tool. IJnfortunately, the examination is difficult when the bleeding is brisk. .4t times. repeated saline enemas may be able to clear the colon and also slow the rate of the bleeding, thus facilitating the colonoscopic examination and diagnosis.
The American
Journal of Surgery
Colonic
Even bleeding diverticula of the colon may be occasionally detected by this means. If visceral arteriography and colonctscopy fail to achieve the diagnosis, explorat.ory laparotomy may be the only recourse. The exploration should he done while the patient is actively bleeding and in good condit.ion. If ileotomy shows t.hat the small bowel is free of blood and thus bleeding is limited to the colon, most of the colon may be excised down to the level ot the dist.al sigmoid or upper rectum which had heen determined free of’ disease preoperatively. removing the entire diverticula-bearing colon. Thus. the suriical tnanagement is not different from that which is exercised l’or presumed diverticular bleeding of the colon. The bowel continuity is reestablished with ileoproctostomy. The excised specimen should be opened and washe:] of’ its contents immediately af’ter excision while the \.ascular pedicles of the specimen are either tied or clamped. The mucosal surface should be inspected a small segment at a time hy manually compressing the ends of the selected segment and stretching the mucosa. thus rendering the submucosal vessels prominent. A small mucosal defect tnay become visible. from which the blood may be expressed. The tnucosal defect seen in this manner may or may not he it tnucosal ulcer. It may be the site uf collapsed capillaries and vascular spaces in the tnucosa as in case I I. I;nless the defect and feeding vessels are precisely marked wit.h subures immediately, they may become undet.ect.able over hours on standing. The site of small vascular malformations are completely undetectable after formalin fixation as in cases II and III. Multiple sections of the previously tnarked site will accurately locate the vascular malfortn;~tiotts f’or histologic examination. In some cases. tirrcosal ulcers associated with vascular malf’ormations are large and easily detectable. Alternatively, one of several materials may be used to distend the arteriovenous malformation in the resected specimen and thus facilitate identification of the malformation. Shlesinger gelatin mass, methyl methacrylate (TensolTM cement #7) and Microfil (silicon rubber; Canton biomedical product) are examples [ I6,lRj. Precise s\tr#ical extirpation ol‘ vascular tnalformations in the stnall bowel must of necessity depend upon angiography. Operative visceral angiography may aid in precise localization and resection of the bleedin:: vascular malformations of the small bowel. Hoive\.tlr. sttch ef’f’orts may not be t’ruitful unless surgical operations are performed in a radiology room that is f’ully equipped for ;qiography [ 15).
Volume 133, June 1977
Arteriovenous
Malformations
Summary .4rteriovenous malformations have become recognized as a major cause of massive bleeding of the colonic origin. Although an arteriographic unit capable of serial magnification is ideal for detecting arteriovenous malformations in the bowel, t.he diagnosis tnay still he made hy a combined approach of convent.ional arteriography, colonoscopy and operative judgment. The final diagnosis rests on gross and histologic demonstration of’ vascular malformations in the excised specimen. References 1. Hernandez GE. Durnin RE, Hagihara. PI? Arterievenous rnalformation of the colon: case report. J Ky A&d Assoc 72: 488. 1974. 2. Retzlaff JA. Hagedom AB. Bartholomew LG: Abdominal exploration for gastrointestinal bleeding of obscure origin. JAMA 177: 94. 1961. 3. Noer RJ: Hemorrhage as a complication of diverticulitis. Ann Surg 141: 674, 1955. 4. Noer RJ, Hamilton JE, Williams DJ. Broughton DS: Rectal hemorrhage: moderate and severe. Ann Surg 155: 794, 1962. 5. Rives JD, Emmett RO: Melena. A survey of 206 cases. Am Sung 20: 456, 1954. 6. Mobley JE. Dockerty MB. Waugh JM: Bleeding in colonic diverticulitis. Am J Surg 94: 44, 1957. 7. Rosser C: The surgical management of diverticulitis. SouN, &d d32: 1203, 1939. 8. Fansler WA: Diverticulosis and diverticulitis-with particular reference to the large bowel. Trans Am Proctology Sot 4 1: 231. :940. 9. Rigg BM. Ewing MR: Current attitudes on diverticulitis with particular reference to colonic bleeding. Arch Surg 92: 32 1, 1966. 10. Ruiz-Moreno f: Hemangiomatosis of the colon: report of a case. Dis Colon Rectum 5: 453, 1962. 11. Margulis AF, Heinbecker P, Bernard H: Operative mesenteric arieriography in the search for the site of bleeding in unexplained gastrointestinal hemorrhage. Surgery 48: 534. 1960. 12. Baum S, Nusbaum M. Ctearfield HR. Kurcxla K, lumen HJ: Angiography in the diagnosis of gastrointestinal bleeding. Arch Intern h&d 119: 16. 1967. 13. Baum S, Nusbaum M, Kuroda K. BlAkemore WS: Direct serial magnification arteriography as an adjuvant in the diagnosis of surgical lesions of the alimentary tract. Am J Sufg 117: 170. 1969. 14. Nusbaum M, Baum S. Blakemore WS: Clinical experience with the diagnosis and management of gastrointestinal hemorrhage by selective mesenteric catheterization. Ann Surg 170: 506. 1969. 15. Alfidi RJ, Esselstyn CD. Tarar R. Klein KI. Hermann RE. Weakley FL. Turnbull RB: Recognition and angio-surgical detection of arteriovenous malformations of the bowel. Ann Surg 174: 573, 1971. 16. Alfidi RJ: Angiography in identifying the source of intestinal bleeding. Dis Co/on Rectum 17: 442. 1974. 17. Genant HK. Ranniger K: Vascular dysplasia of the ascending colon. Report of two cases and review of the literature. Am J Roentgenol Radium Ther Nucl Med 115: 349. 1972. 18. Baum S: Small vessel angiography of the gut, chapt 34, p 454. Small Vessel Angiography (Hilal SK. ed). St. Louis. CV Mosby. 1973.
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