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Provocative angiography for obscure gastrointestinal bleeding
Provocative Angiography for Obscure Gastrointestinal Bleeding Paul V. Suhocki, MD
Patients who present for angiography in 2003 present a challenge not experienced by angiographers 4 decades ago. Patients who have gone through the battery of sophisticated radiologic, scintigraphic, and endoscopic examinations available today and remain without a known source of gastrointestinal hemorrhage rely on the angiographer to critically evaluate the mesenteric vasculature for abnormalities. If the diagnostic angiography shows no vascular abnormality, the angiographer has several pharmocologic agents that can be used to provoke hemorrhage to assist in detecting the source. If the bleeding site is seen, the angiographer may then use embolic agents to occlude the vessel or provide visual cues for assisting the surgeon in resection of the appropriate segment of bowel. © 2003 Elsevier Inc. All rights reserved.
he radiologist has played a role in detection of gastrointestinal bleeding sites since 1965 when Baum et al1,2 showed the utility of selective angiography of the celiac and superior mesenteric arteries for this purpose. Cross-sectional imaging and endoscopy have since replaced this invasive procedure and its attendant risks in most patients with gastrointestinal bleeding. However, selective mesenteric angiography still plays a role in diagnosing those sources of bleeding in the small bowel, which are beyond the reach of the endoscope. The emerging technology of capsule endoscopy may soon augment or replace angiography in this region of the gastrointestinal tract as well. Selective mesenteric angiography of the gastrointestinal tract still plays a pivotal role in patients who have a persistent lowgrade gastrointestinal hemorrhage despite having had multiple negative endoscopies, scintigrams, and cross-sectional imaging studies. Once the site of hemorrhage is shown, the radiologist can embolize small bowel and colonic bleeds using a microcatheter, with a lower incidence of bowel infarction than previously with older technology. Transcatheter diagnostic angiography, without or with provocative maneuvers, and transcatheter intervention in the patient with obscure gastrointestinal bleeding are the focus of this article.
T
From the Department of Radiology, Duke University Medical Center, Durham, NC. Address reprint requests to Paul V. Suhocki, MD, Box 3808, Duke University Medical Center, Erwin Road, Durham, NC 27710. © 2003 Elsevier Inc. All rights reserved. 1096-2883/03/0503-0005$30.00/0 doi:10.1053/S1096-2883(03)00037-8
Diagnostic Mesenteric Angiography in the Patient With Obscure Gastrointestinal Bleeding Preparation for the Diagnostic Arteriogram The radiologist performs a standard diagnostic arteriogram before pharmacologic measures are taken to provoke a gastrointestinal bleed on the angiography table. The radiologist first reviews the chronicity of bleeding, blood transfusion requirements, coagulation profile, anticoagulant use, platelet count, and the results of all previously performed angiograms and endoscopies. Coagulation and platelet abnormalities are corrected to near normal as possible to prevent bleeding after catheter removal and assist in the hemostatic properties of embolic agents, should embolization be performed. Arterial closure devices can be used for hemostasis at the groin entry site at the conclusion of the procedure in those patients in whom coagulopathy cannot be corrected to a desired level. Because iodinated contrast used during angiography is nephrotoxic, patients with renal insufficiency are hydrated for 24 hours before angiography. Allergies to the contrast are treated with a steroid prep for 24 hours before the study. Past medical and surgical history are reviewed to glean information that will assist in the interpretation of the angiogram. A family history of arteriovenous malformations (Osler-Weber-Rendu Syndrome) would prompt the radiologist to observe for abnormal arteriovenous communications on angiography, with large feeding arteries and very early draining veins. Patients with end-stage renal disease may exhibit foci of angiodysplasia (Fig 1) in the bowel wall, characterized by early opacification of the draining vein, persistence of this vein into the venous phase, and the presence of a vascular tuft along the antimesenteric border.3 In a patient who has had a mesenteric artery previously ligated or embolized, (1) large submucosal collaterals can ulcerate and hemorrhage,4, (2) catheterization of the mesenteric arteries may be difficult or impossible, and (3) risk of ischemia to the viscus is increased if the radiologist embolizes all or part of the remaining blood supply. A history of hepatic or pancreatic disorders prompts a close evaluation of the celiac artery distribution. Bleeding from the liver or pancreas may be a result of previous biopsy, tumor, trauma, parasitic, or bacterial infection or stones. Pseudoaneurysms (Fig 2) or arteriovenous fistulae (Fig 3) may be the source of hemorrhage in these settings. Small bowel neoplasms occasionally escape notice on computed tomography (CT) scan or small bowel follow through because of a lack of oral contrast, poor intravenous contrast bolus timing, slice thickness, artifact, or inability of the patient
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Fig 3. Arteriovenous fistula (arrowhead) is present between the anterior pancreaticoduodenal artery and a portal venous tributary. The fistula was created during percutaneous biopsy of the pancreatic head.
Fig 1. Angiodysplasia (arrowhead) involves the inferior mesenteric artery with early opacification of the draining vein, persistence of this vein into the venous phase, and the presence of a vascular tuft along the antimesenteric border.
to cooperate. Angiography may show vascular blush, vascular lakes, aneurysm formation, arteriovenous shunting, parasitization of blood supply, large draining veins, vascular encasement, and abrupt change in the course of a vessel (Fig 4).3 Vascular narrowing or occlusion secondary to subintimal fibrosis may be seen in the patient with a history of radiation to the abdomen or pelvis. Transmural necrosis may occasionally occur.3 Chronic bleeding in the young patient should prompt a close evaluation of the distal ileum looking for the presence of a
Fig 2. A wide-mouthed saccular pseudoaneurysm (arrow) involves the distal portion of the splenic artery in a patient with pancreatitis.
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vitelline artery and possibly a mucosal blush of a Meckel’s diverticulum (Fig 5). A small percentage of these patients may have a negative radionuclide Meckel’s scan. SPECT (single photon emission computed tomography) imaging in the nuclear medicine department may disclose the Meckel’s diverticulum not seen on the planar imaging of a standard Meckel’s scan, obviating the need for mesenteric angiography.5 Patients with a history of polyarteritis nodosa would direct attention to the small branches of the hepatic or mesenteric arteries observing for saccular or fusiform aneurysm of the branches (Fig 6). Such aneurysms can spontaneously rupture into bile ducts, pancreatic ducts, or the wall or lumen of the bowel. Varices are usually seen endoscopically in the patient with portal hypertension or sinistral hypertension secondary to splenic vein occlusion. Small bowel varices are usually visualized on CT. Angiography is not useful for diagnosing variceal bleeds because the iodinated contrast becomes too dilute during the venous phase of superior mesenteric artery (SMA) arteriography. It may show splenic vein or portal vein occlusion,
Fig 4. Tumor vascularity (arrowheads) is seen in this spindle cell tumor of the duodenum supplied by the pancreaticoduodenal artery. PAUL V. SUHOCKI
Fig 5. A tortuous vitelline artery (arrows) supplying a Meckel’s diverticulum extends from the superior mesenteric artery toward the dome of the urinary bladder.
but this is more easily seen on CT, magnetic resonance imaging, or Doppler ultrasound. The interventional radiologist can, however, assist in making the diagnosis of portal hypertension. The radiologist can obtain indirect portal vein pressure measurements by measuring wedged and free hepatic vein pressures through a transjugular venous route. Transjugular liver biopsy may be performed at the same time. This means of obtaining liver tissue by traversing the wall of the middle hepatic vein greatly reduces the risk of hepatic hemorrhage during liver biopsy in the coagulopathic patient. Transjugular intrahepatic portosystemic shunt is a well-established means of treating variceal bleeding and is also done in the interventional radiology suite. In patients with segmental arterial mediolysis, angiography shows areas of arterial dilatation, dissection, and occlusion (Fig 7). The celiac artery is most commonly involved. Abnormalities may less commonly be seen in the superior mesenteric artery, inferior mesenteric artery, and renal arteries (Ryan SM, Suhocki PV, Smith TP: Coil embolization of segmental arterial mediolysis of the hepatic artery. J Vasc Interv Radiol 11:865-868, 2000).
Fig 6. A small aneurysm (arrowhead) involves an early jejunal branch of the superior mesenteric artery in a patient with polyarteritis nodosa. PROVOCATIVE ANGIOGRAPHY
Fig 7. Multiple areas of fusiform dilatation (arrows) are seen in branches of the superior mesenteric artery in a patient with segmental arterial mediolysis.
Patient history of previous aortic aneurysm repair should alert the medical team to the possibility of an aortoenteric fistula being present. Aortic stent grafts have been reported to erode into adjacent bowel.6 Arteriography has no role in making this diagnosis. Patients with this suspected diagnosis should undergo CT scan of the abdomen. The radiologist searches for evidence of an aortoenteric fistula, which usually involves the duodenum, but may involve any portion of the gastrointestinal tract. Barium studies should not be ordered before obtaining a CT scan because the barium will degrade the CT imaging and make diagnosis impossible
Diagnostic Mesenteric Angiography Procedure Diagnostic angiography is performed with the patient under conscious sedation. The radiologist uses micropuncture technique with a 21-gauge needle to place a 5-French vascular sheath into the femoral artery. The left brachial artery is accessed if the femoral arteries are occluded, although this carries a risk of stroke. The radiologist then selectively catheterizes the celiac artery, superior mesenteric artery, and inferior mesenteric artery. The inferior mesenteric artery is often occluded or stenotic in the elderly patient, particularly in those with extensive atherosclerosis. Rapid sequence digital angiography is performed for each vascular distribution, while iodinated contrast is injected through the catheter. The nonprovocative mesenteric angiogram has a high likelihood of showing a vascular abnormality, making it unnecessary to use pharmacologic agents for induction of bleeding. In 1988, Tillotson et al7 published the results of 408 diagnostic mesenteric angiograms performed for gastrointestinal bleeding of obscure origin. Fifty-one percent of the studies were positive. Sixty percent of these showed gross extravasation of contrast. Forty percent of the positive studies showed vascular abnormalities only. In 1991, Rollins et al8 published the results of 36
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TABLE 1. Use of Provocative Angiography for Detecting Source of Obscure Gastrointestinal Bleeding
Koval et al, 1987 Bloomfeld et al, 20009 Mernagh et al, 200110 Ryan et al, 200111
No. of Patients
Pharmacologic Agents
Diagnostic Yield (%)
No. of Complications
10 7 18 17
Heparin, Heparin, Heparin, Heparin,
80 29 67 50
2 (minor) 0 0 0
tolazoline, streptokinase tolazoline, urokinase papaverine tolazoline, tPA
diagnostic mesenteric angiograms performed for obscure gastrointestinal bleeding. Forty-four percent of these studies were positive. Thirty percent of these showed gross extravasation of contrast. Seventy percent showed vascular abnormalities only. The definition of obscure gastrointestinal bleeding has changed since these 2 reports because of improvements in endoscopic and radiologic equipment. However, the findings do warrant a complete investigation of a mesenteric angiographic study for abnormalities before provocative measures are undertaken. Attention is paid to vascular contours and the rate of venous drainage. The radiologist looks for the gross extravasation of contrast into bowel lumen, vasculitis, aneurysms, pseudoaneurysms, arteriovenous fistulae, arterioenteric fistulae, tumor,
and angiodysplasia. Because it is commonly seen on endoscopy, angiodysplasia may be an incidental finding and not the source of hemorrhage. When angiodysplasia is identified, the radiologist must complete angiography of all 3 vessels searching for other sources of hemorrhage before the angiodysplasia is labeled the most likely source.
Provocative Angiography in the Patient With Obscure Gastrointestinal Bleeding If the diagnostic mesenteric arteriogram is normal, the radiologist proceeds to provoke bleeding with the use of pharmacotherapy. Provocative angiography has been proven to be a rel-
Fig 8. Provocative arteriogram and transcatheter embolization. (A) After infusion of tPA and priscoline into the superior mesenteric artery, extravasation of contrast (arrowheads) is seen in the jejunum. (B) The arterial branch supplying the bleeding site (arrowhead) is selectively catheterized with a microcatheter. (C) A metallic microcoil (arrowhead) is deposited in the vascular arcade near the hemorrhage. (D) Repeat arteriography shows absence of bleeding and normal mucosal blush of bowel from adjacent vessels.
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atively safe procedure. The provoked bleed is usually slow and does not cause hemodynamic compromise. However, it is helpful for the radiologist to let the medical and surgical team know when the procedure will be performed so that emergency treatment can be performed by personnel familiar with the patient should they become unstable and unable to be embolized successfully and promptly. Contraindications to provoking hemorrhage with fibrinolytic agents include recent stroke, intracranial tumor, and recent surgery in the tissue bed being infused.
Provocative Angiography Procedure An intravenous bolus of heparin is given, appropriate for the patient’s weight, and a constant intravenous infusion of heparin is begun. The radiologist catheterizes the mesenteric artery that is the most likely source of hemorrhage, usually the superior mesenteric artery. There are many published combinations of fibrinolytic and vasodilator agents used intra-arterially with intravenous heparin to provoke gastrointestinal hemorrhage. The diagnostic yield and complication rate of these published studies are shown in Table 1. The most common fibrinolytic agents used are tissue plasminogen activator and urokinase. The efficacy of streptokinase as a fibrinolytic agent is variable and unpredictable because of antibodies to this agent being present in much of the population. Tolazoline and papaverine are the most commonly used vasodilator agents. Pharmacologic agents have also been used to provoke gastrointestinal bleeding during radiolabeled red blood cell studies. Malden et al12 performed 10 provocative scintigrams in 1998. They administered an intravenous bolus of 10,000 IU of heparin followed by 500 IU/h intravenously for 3 hours. They also gave an intravenous bolus of 250,000 IU of urokinase followed by 250,000 IU/h of urokinase for 3 hours. Four of the bleeding studies became positive within 4 hours, and 3 studies turned positive 8 to 24 hours later, giving a 70% diagnostic yield. They did not experience any hemorrhagic complications. When a provocative arteriogram is positive, the location of the bleed is discussed with the medical and surgical teams (Fig 8). The decision is made to either go to operating room for partial bowel resection or for the patient to remain on the angiography table for embolization of the bleeding vessel. If an operation is planned, the radiologist can first mark the abnormal segment of bowel so that the surgeon can identify it in the operating room. There are 2 ways in which the abnormal site can be marked. The radiologist can simply leave a catheter tip in the abnormal mesenteric artery branch. The patient proceeds to the operating room with the catheter in place. The catheter is injected with methylene blue. The stained segment of bowel is resected. The potential pitfall with this method of tagging is the surgeon dislodging the catheter from the abnor-
Fig 9. Agents used for transcatheter embolization include Gelfoam pledgets (solid arrow), Polyvinyl alcohol particles 250 to 350 microns in diameter (open arrows), and stainless steel coils (arrowhead) with Dacron fibers being deployed through a catheter. Cartridge in which the coil is preloaded is seen below.
mal artery in the operating room by bowel manipulation before the methylene blue is injected. A more favored approach to tagging is for the radiologist to deposit a metallic coil (platinum or stainless steel) in the abnormal artery through the catheter. The catheter is then removed. The patient is transported to the operating room where the surgeon uses fluoroscopy to identify the radiopaque coil lying within the abnormal bowel segment. This segment of bowel is then resected. With this technique, the hemostatic properties of the coil may very well stop the bleeding, making surgery unnecessary. If bleeding does cease after coil embolization, it is prudent to pursue the cause of bleeding. Small bowel bleeding is uncommon and malignancy must be excluded as a source. Various agents have been used for embolizing mesenteric arteries for bleeding (Fig 9). They include stainless steel or platinum coils (Cook Inc, Bloomington, IN), polyvinyl alcohol particles (Contour, Boston Scientific, Natick, MA), gelfoam (Pharmacia Upjon USA, Peapack, NJ), and N-butyl-2-cyanoacrylate glue (Histacryl, Braun, Melsungen, Germany). Several recent reports of embolization for gastrointestinal bleeding are shown in Table 2. Absence of bleeding for 30 days after embolization constituted success. Despite a success rate of 76% to 85%, the major complication rate was surprisingly low (0%7%). Intra-arterial infusion of vasopressin, a potent vasoconstrictor, does not play a role in the treatment of the slow rate of
TABLE 2. Use of Transcatheter Embolization for Gastrointestinal Bleeding
Evangelista et al, 2000 Luchtefeld et al, 200014 Defreyne et al, 200115 Funaki et al, 200116 Patel et al, 200117
13
PROVOCATIVE ANGIOGRAPHY
No. of Patients
Embolic Agents
Success (%)
No. of Complications
17 17 40 27 10
Coils, PVA, Gelfoam Not Available Coils, PVA, Glue Coils Coils, PVA, Gelfoam
76 76 85 81 80
0 1 0 2 0
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bleeding typically seen with gastrointestinal bleeding of obscure origin.
Conclusions Detecting and treating the source of obscure gastrointestinal hemorrhage will continue to be a challenge for all services involved. Improvements in imaging equipment and catheters have made diagnostic and therapeutic radiologic techniques more sensitive and safer over the last 4 decades. The use of capsule endoscopy and other innovative noninvasive techniques will determine what future role the radiologist will play in the management of obscure gastrointestinal bleeding.
References 1. Baum S, Roy R, Finkelstein A, et al: Clinical application of selective celiac and superior mesenteric arteriography. Radiology 84:279-295, 1965 2. Baum S, Nusbaum M, Blakemore W, et al: The preoperative radiographic demonstration of intra-abdominal bleeding from undetermined sites by percutaneous celiac and superior mesenteric arteriography. Surgery 58:797-805, 1965 3. Kadir S: Diagnostic angiography. Philadelphia, PA, Saunders, 1986 4. Baron PW, Sindram D, Suhocki P, et al: Upper gastrointestinal bleeding from gastric submucosal arterial collaterals secondary to splenic artery occlusion: Treatment by splenectomy and partial gastric devascularization. Am J Gastroenterol 95:3003-3004, 2000 5. Connolly LP, Treves ST, Bozorgi F, et al: Meckel’s diverticulum: Demonstration of heterotopic gastric mucosa with technetium-99mpertechnetate SPECT. J Nucl Med 39:1458-1460, 1998
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6. Norgren L, Jernby B, Engellau L: Aortoenteric fistula caused by a ruptured stent-graft: a case report. J Endovasc Surg 5:269-272, 1998 7. Tillotson CL, Geller SC, Kantrowitz L, et al: Small bowel hemorrhage: Angiographic localization and intervention. Gastrointest Radiol 13: 207-211, 1988 8. Rollins ES, Picus D, Hicks ME, et al: Angiography is useful in detecting the source of chronic gastrointestinal bleeding of obscure origin. AJR Am J Roentgenol 156:385-388, 1991 9. Bloomfeld RS, Smith TP, Schneider AM, et al: Provocative angiography in patients with gastrointestinal hemorrhage of obscure origin. Am J Gastroenterology 95:2807-2812, 2000 10. Mernagh JR, O’Donovan N, Somers S, et al: Use of heparin in the investigation of obscure gastrointestinal bleeding. Can Assoc Radiol J 52:232-235, 2001 11. Ryan JM, Key SM, Dumbleton SA, et al: Nonlocalized lower gastrointestinal bleeding: Provocative bleeding studies with intraarterial tPA, Heparin, and Tolazoline. J Vasc Interv Radiol 12:1273-1277, 2001 12. Malden ES, Hicks ME, Royal HD, et al: Recurrent gastrointestinal bleeding: Use of thrombolysis with anticoagulation in diagnosis. Radiology 207:147-151, 1998 13. Evangelista PT, Hallisey MJ: Transcatheter embolization for acute lower gastrointestinal hemorrhage. J Vasc Interv Radiol 2000;11: 601-606, 2000 14. Luchtefeld MA, Senagore AJ, Szomstein M, et al: Evaluation of transarterial embolization for lower gastrointestinal bleeding. Dis Colon Rectum 43:532-534, 2000 15. Defreyne L, Vanlangenhove P, De Vos M, et al: Embolization as a first approach with endoscopically unmanageable acute nonvariceal gastrointestinal hemorrhage. Radiology 218:739-748, 2001 16. Funaki B, Kostelic JK, Lorenz J, et al: Superselective microcoil embolization of colonic hemorrhage. AJR Am J Roentgenol 177:829836, 2001 17. Patel TH, Cordts PR, Abcarian P, et al: Will transcatheter embolotherapy replace surgery in the treatment of gastrointestinal bleeding? Curr Surg 58:323-327, 2001
PAUL V. SUHOCKI
Patients who present for angiography in 2003 present a challenge not experienced by angiographers 4 decades ago. Patients who have gone through the battery of sophisticated radiologic, scintigraphic, and endoscopic examinations available today and remain without a known source of gastrointestinal hemorrhage rely on the angiographer to critically evaluate the mesenteric vasculature for abnormalities. If the diagnostic angiography shows no vascular abnormality, the angiographer has several pharmocologic agents that can be used to provoke hemorrhage to assist in detecting the source. If the bleeding site is seen, the angiographer may then use embolic agents to occlude the vessel or provide visual cues for assisting the surgeon in resection of the appropriate segment of bowel. © 2003 Elsevier Inc. All rights reserved.
he radiologist has played a role in detection of gastrointestinal bleeding sites since 1965 when Baum et al1,2 showed the utility of selective angiography of the celiac and superior mesenteric arteries for this purpose. Cross-sectional imaging and endoscopy have since replaced this invasive procedure and its attendant risks in most patients with gastrointestinal bleeding. However, selective mesenteric angiography still plays a role in diagnosing those sources of bleeding in the small bowel, which are beyond the reach of the endoscope. The emerging technology of capsule endoscopy may soon augment or replace angiography in this region of the gastrointestinal tract as well. Selective mesenteric angiography of the gastrointestinal tract still plays a pivotal role in patients who have a persistent lowgrade gastrointestinal hemorrhage despite having had multiple negative endoscopies, scintigrams, and cross-sectional imaging studies. Once the site of hemorrhage is shown, the radiologist can embolize small bowel and colonic bleeds using a microcatheter, with a lower incidence of bowel infarction than previously with older technology. Transcatheter diagnostic angiography, without or with provocative maneuvers, and transcatheter intervention in the patient with obscure gastrointestinal bleeding are the focus of this article.
T
From the Department of Radiology, Duke University Medical Center, Durham, NC. Address reprint requests to Paul V. Suhocki, MD, Box 3808, Duke University Medical Center, Erwin Road, Durham, NC 27710. © 2003 Elsevier Inc. All rights reserved. 1096-2883/03/0503-0005$30.00/0 doi:10.1053/S1096-2883(03)00037-8
Diagnostic Mesenteric Angiography in the Patient With Obscure Gastrointestinal Bleeding Preparation for the Diagnostic Arteriogram The radiologist performs a standard diagnostic arteriogram before pharmacologic measures are taken to provoke a gastrointestinal bleed on the angiography table. The radiologist first reviews the chronicity of bleeding, blood transfusion requirements, coagulation profile, anticoagulant use, platelet count, and the results of all previously performed angiograms and endoscopies. Coagulation and platelet abnormalities are corrected to near normal as possible to prevent bleeding after catheter removal and assist in the hemostatic properties of embolic agents, should embolization be performed. Arterial closure devices can be used for hemostasis at the groin entry site at the conclusion of the procedure in those patients in whom coagulopathy cannot be corrected to a desired level. Because iodinated contrast used during angiography is nephrotoxic, patients with renal insufficiency are hydrated for 24 hours before angiography. Allergies to the contrast are treated with a steroid prep for 24 hours before the study. Past medical and surgical history are reviewed to glean information that will assist in the interpretation of the angiogram. A family history of arteriovenous malformations (Osler-Weber-Rendu Syndrome) would prompt the radiologist to observe for abnormal arteriovenous communications on angiography, with large feeding arteries and very early draining veins. Patients with end-stage renal disease may exhibit foci of angiodysplasia (Fig 1) in the bowel wall, characterized by early opacification of the draining vein, persistence of this vein into the venous phase, and the presence of a vascular tuft along the antimesenteric border.3 In a patient who has had a mesenteric artery previously ligated or embolized, (1) large submucosal collaterals can ulcerate and hemorrhage,4, (2) catheterization of the mesenteric arteries may be difficult or impossible, and (3) risk of ischemia to the viscus is increased if the radiologist embolizes all or part of the remaining blood supply. A history of hepatic or pancreatic disorders prompts a close evaluation of the celiac artery distribution. Bleeding from the liver or pancreas may be a result of previous biopsy, tumor, trauma, parasitic, or bacterial infection or stones. Pseudoaneurysms (Fig 2) or arteriovenous fistulae (Fig 3) may be the source of hemorrhage in these settings. Small bowel neoplasms occasionally escape notice on computed tomography (CT) scan or small bowel follow through because of a lack of oral contrast, poor intravenous contrast bolus timing, slice thickness, artifact, or inability of the patient
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Fig 3. Arteriovenous fistula (arrowhead) is present between the anterior pancreaticoduodenal artery and a portal venous tributary. The fistula was created during percutaneous biopsy of the pancreatic head.
Fig 1. Angiodysplasia (arrowhead) involves the inferior mesenteric artery with early opacification of the draining vein, persistence of this vein into the venous phase, and the presence of a vascular tuft along the antimesenteric border.
to cooperate. Angiography may show vascular blush, vascular lakes, aneurysm formation, arteriovenous shunting, parasitization of blood supply, large draining veins, vascular encasement, and abrupt change in the course of a vessel (Fig 4).3 Vascular narrowing or occlusion secondary to subintimal fibrosis may be seen in the patient with a history of radiation to the abdomen or pelvis. Transmural necrosis may occasionally occur.3 Chronic bleeding in the young patient should prompt a close evaluation of the distal ileum looking for the presence of a
Fig 2. A wide-mouthed saccular pseudoaneurysm (arrow) involves the distal portion of the splenic artery in a patient with pancreatitis.
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vitelline artery and possibly a mucosal blush of a Meckel’s diverticulum (Fig 5). A small percentage of these patients may have a negative radionuclide Meckel’s scan. SPECT (single photon emission computed tomography) imaging in the nuclear medicine department may disclose the Meckel’s diverticulum not seen on the planar imaging of a standard Meckel’s scan, obviating the need for mesenteric angiography.5 Patients with a history of polyarteritis nodosa would direct attention to the small branches of the hepatic or mesenteric arteries observing for saccular or fusiform aneurysm of the branches (Fig 6). Such aneurysms can spontaneously rupture into bile ducts, pancreatic ducts, or the wall or lumen of the bowel. Varices are usually seen endoscopically in the patient with portal hypertension or sinistral hypertension secondary to splenic vein occlusion. Small bowel varices are usually visualized on CT. Angiography is not useful for diagnosing variceal bleeds because the iodinated contrast becomes too dilute during the venous phase of superior mesenteric artery (SMA) arteriography. It may show splenic vein or portal vein occlusion,
Fig 4. Tumor vascularity (arrowheads) is seen in this spindle cell tumor of the duodenum supplied by the pancreaticoduodenal artery. PAUL V. SUHOCKI
Fig 5. A tortuous vitelline artery (arrows) supplying a Meckel’s diverticulum extends from the superior mesenteric artery toward the dome of the urinary bladder.
but this is more easily seen on CT, magnetic resonance imaging, or Doppler ultrasound. The interventional radiologist can, however, assist in making the diagnosis of portal hypertension. The radiologist can obtain indirect portal vein pressure measurements by measuring wedged and free hepatic vein pressures through a transjugular venous route. Transjugular liver biopsy may be performed at the same time. This means of obtaining liver tissue by traversing the wall of the middle hepatic vein greatly reduces the risk of hepatic hemorrhage during liver biopsy in the coagulopathic patient. Transjugular intrahepatic portosystemic shunt is a well-established means of treating variceal bleeding and is also done in the interventional radiology suite. In patients with segmental arterial mediolysis, angiography shows areas of arterial dilatation, dissection, and occlusion (Fig 7). The celiac artery is most commonly involved. Abnormalities may less commonly be seen in the superior mesenteric artery, inferior mesenteric artery, and renal arteries (Ryan SM, Suhocki PV, Smith TP: Coil embolization of segmental arterial mediolysis of the hepatic artery. J Vasc Interv Radiol 11:865-868, 2000).
Fig 6. A small aneurysm (arrowhead) involves an early jejunal branch of the superior mesenteric artery in a patient with polyarteritis nodosa. PROVOCATIVE ANGIOGRAPHY
Fig 7. Multiple areas of fusiform dilatation (arrows) are seen in branches of the superior mesenteric artery in a patient with segmental arterial mediolysis.
Patient history of previous aortic aneurysm repair should alert the medical team to the possibility of an aortoenteric fistula being present. Aortic stent grafts have been reported to erode into adjacent bowel.6 Arteriography has no role in making this diagnosis. Patients with this suspected diagnosis should undergo CT scan of the abdomen. The radiologist searches for evidence of an aortoenteric fistula, which usually involves the duodenum, but may involve any portion of the gastrointestinal tract. Barium studies should not be ordered before obtaining a CT scan because the barium will degrade the CT imaging and make diagnosis impossible
Diagnostic Mesenteric Angiography Procedure Diagnostic angiography is performed with the patient under conscious sedation. The radiologist uses micropuncture technique with a 21-gauge needle to place a 5-French vascular sheath into the femoral artery. The left brachial artery is accessed if the femoral arteries are occluded, although this carries a risk of stroke. The radiologist then selectively catheterizes the celiac artery, superior mesenteric artery, and inferior mesenteric artery. The inferior mesenteric artery is often occluded or stenotic in the elderly patient, particularly in those with extensive atherosclerosis. Rapid sequence digital angiography is performed for each vascular distribution, while iodinated contrast is injected through the catheter. The nonprovocative mesenteric angiogram has a high likelihood of showing a vascular abnormality, making it unnecessary to use pharmacologic agents for induction of bleeding. In 1988, Tillotson et al7 published the results of 408 diagnostic mesenteric angiograms performed for gastrointestinal bleeding of obscure origin. Fifty-one percent of the studies were positive. Sixty percent of these showed gross extravasation of contrast. Forty percent of the positive studies showed vascular abnormalities only. In 1991, Rollins et al8 published the results of 36
123
TABLE 1. Use of Provocative Angiography for Detecting Source of Obscure Gastrointestinal Bleeding
Koval et al, 1987 Bloomfeld et al, 20009 Mernagh et al, 200110 Ryan et al, 200111
No. of Patients
Pharmacologic Agents
Diagnostic Yield (%)
No. of Complications
10 7 18 17
Heparin, Heparin, Heparin, Heparin,
80 29 67 50
2 (minor) 0 0 0
tolazoline, streptokinase tolazoline, urokinase papaverine tolazoline, tPA
diagnostic mesenteric angiograms performed for obscure gastrointestinal bleeding. Forty-four percent of these studies were positive. Thirty percent of these showed gross extravasation of contrast. Seventy percent showed vascular abnormalities only. The definition of obscure gastrointestinal bleeding has changed since these 2 reports because of improvements in endoscopic and radiologic equipment. However, the findings do warrant a complete investigation of a mesenteric angiographic study for abnormalities before provocative measures are undertaken. Attention is paid to vascular contours and the rate of venous drainage. The radiologist looks for the gross extravasation of contrast into bowel lumen, vasculitis, aneurysms, pseudoaneurysms, arteriovenous fistulae, arterioenteric fistulae, tumor,
and angiodysplasia. Because it is commonly seen on endoscopy, angiodysplasia may be an incidental finding and not the source of hemorrhage. When angiodysplasia is identified, the radiologist must complete angiography of all 3 vessels searching for other sources of hemorrhage before the angiodysplasia is labeled the most likely source.
Provocative Angiography in the Patient With Obscure Gastrointestinal Bleeding If the diagnostic mesenteric arteriogram is normal, the radiologist proceeds to provoke bleeding with the use of pharmacotherapy. Provocative angiography has been proven to be a rel-
Fig 8. Provocative arteriogram and transcatheter embolization. (A) After infusion of tPA and priscoline into the superior mesenteric artery, extravasation of contrast (arrowheads) is seen in the jejunum. (B) The arterial branch supplying the bleeding site (arrowhead) is selectively catheterized with a microcatheter. (C) A metallic microcoil (arrowhead) is deposited in the vascular arcade near the hemorrhage. (D) Repeat arteriography shows absence of bleeding and normal mucosal blush of bowel from adjacent vessels.
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PAUL V. SUHOCKI
atively safe procedure. The provoked bleed is usually slow and does not cause hemodynamic compromise. However, it is helpful for the radiologist to let the medical and surgical team know when the procedure will be performed so that emergency treatment can be performed by personnel familiar with the patient should they become unstable and unable to be embolized successfully and promptly. Contraindications to provoking hemorrhage with fibrinolytic agents include recent stroke, intracranial tumor, and recent surgery in the tissue bed being infused.
Provocative Angiography Procedure An intravenous bolus of heparin is given, appropriate for the patient’s weight, and a constant intravenous infusion of heparin is begun. The radiologist catheterizes the mesenteric artery that is the most likely source of hemorrhage, usually the superior mesenteric artery. There are many published combinations of fibrinolytic and vasodilator agents used intra-arterially with intravenous heparin to provoke gastrointestinal hemorrhage. The diagnostic yield and complication rate of these published studies are shown in Table 1. The most common fibrinolytic agents used are tissue plasminogen activator and urokinase. The efficacy of streptokinase as a fibrinolytic agent is variable and unpredictable because of antibodies to this agent being present in much of the population. Tolazoline and papaverine are the most commonly used vasodilator agents. Pharmacologic agents have also been used to provoke gastrointestinal bleeding during radiolabeled red blood cell studies. Malden et al12 performed 10 provocative scintigrams in 1998. They administered an intravenous bolus of 10,000 IU of heparin followed by 500 IU/h intravenously for 3 hours. They also gave an intravenous bolus of 250,000 IU of urokinase followed by 250,000 IU/h of urokinase for 3 hours. Four of the bleeding studies became positive within 4 hours, and 3 studies turned positive 8 to 24 hours later, giving a 70% diagnostic yield. They did not experience any hemorrhagic complications. When a provocative arteriogram is positive, the location of the bleed is discussed with the medical and surgical teams (Fig 8). The decision is made to either go to operating room for partial bowel resection or for the patient to remain on the angiography table for embolization of the bleeding vessel. If an operation is planned, the radiologist can first mark the abnormal segment of bowel so that the surgeon can identify it in the operating room. There are 2 ways in which the abnormal site can be marked. The radiologist can simply leave a catheter tip in the abnormal mesenteric artery branch. The patient proceeds to the operating room with the catheter in place. The catheter is injected with methylene blue. The stained segment of bowel is resected. The potential pitfall with this method of tagging is the surgeon dislodging the catheter from the abnor-
Fig 9. Agents used for transcatheter embolization include Gelfoam pledgets (solid arrow), Polyvinyl alcohol particles 250 to 350 microns in diameter (open arrows), and stainless steel coils (arrowhead) with Dacron fibers being deployed through a catheter. Cartridge in which the coil is preloaded is seen below.
mal artery in the operating room by bowel manipulation before the methylene blue is injected. A more favored approach to tagging is for the radiologist to deposit a metallic coil (platinum or stainless steel) in the abnormal artery through the catheter. The catheter is then removed. The patient is transported to the operating room where the surgeon uses fluoroscopy to identify the radiopaque coil lying within the abnormal bowel segment. This segment of bowel is then resected. With this technique, the hemostatic properties of the coil may very well stop the bleeding, making surgery unnecessary. If bleeding does cease after coil embolization, it is prudent to pursue the cause of bleeding. Small bowel bleeding is uncommon and malignancy must be excluded as a source. Various agents have been used for embolizing mesenteric arteries for bleeding (Fig 9). They include stainless steel or platinum coils (Cook Inc, Bloomington, IN), polyvinyl alcohol particles (Contour, Boston Scientific, Natick, MA), gelfoam (Pharmacia Upjon USA, Peapack, NJ), and N-butyl-2-cyanoacrylate glue (Histacryl, Braun, Melsungen, Germany). Several recent reports of embolization for gastrointestinal bleeding are shown in Table 2. Absence of bleeding for 30 days after embolization constituted success. Despite a success rate of 76% to 85%, the major complication rate was surprisingly low (0%7%). Intra-arterial infusion of vasopressin, a potent vasoconstrictor, does not play a role in the treatment of the slow rate of
TABLE 2. Use of Transcatheter Embolization for Gastrointestinal Bleeding
Evangelista et al, 2000 Luchtefeld et al, 200014 Defreyne et al, 200115 Funaki et al, 200116 Patel et al, 200117
13
PROVOCATIVE ANGIOGRAPHY
No. of Patients
Embolic Agents
Success (%)
No. of Complications
17 17 40 27 10
Coils, PVA, Gelfoam Not Available Coils, PVA, Glue Coils Coils, PVA, Gelfoam
76 76 85 81 80
0 1 0 2 0
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bleeding typically seen with gastrointestinal bleeding of obscure origin.
Conclusions Detecting and treating the source of obscure gastrointestinal hemorrhage will continue to be a challenge for all services involved. Improvements in imaging equipment and catheters have made diagnostic and therapeutic radiologic techniques more sensitive and safer over the last 4 decades. The use of capsule endoscopy and other innovative noninvasive techniques will determine what future role the radiologist will play in the management of obscure gastrointestinal bleeding.
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6. Norgren L, Jernby B, Engellau L: Aortoenteric fistula caused by a ruptured stent-graft: a case report. J Endovasc Surg 5:269-272, 1998 7. Tillotson CL, Geller SC, Kantrowitz L, et al: Small bowel hemorrhage: Angiographic localization and intervention. Gastrointest Radiol 13: 207-211, 1988 8. Rollins ES, Picus D, Hicks ME, et al: Angiography is useful in detecting the source of chronic gastrointestinal bleeding of obscure origin. AJR Am J Roentgenol 156:385-388, 1991 9. Bloomfeld RS, Smith TP, Schneider AM, et al: Provocative angiography in patients with gastrointestinal hemorrhage of obscure origin. Am J Gastroenterology 95:2807-2812, 2000 10. Mernagh JR, O’Donovan N, Somers S, et al: Use of heparin in the investigation of obscure gastrointestinal bleeding. Can Assoc Radiol J 52:232-235, 2001 11. Ryan JM, Key SM, Dumbleton SA, et al: Nonlocalized lower gastrointestinal bleeding: Provocative bleeding studies with intraarterial tPA, Heparin, and Tolazoline. J Vasc Interv Radiol 12:1273-1277, 2001 12. Malden ES, Hicks ME, Royal HD, et al: Recurrent gastrointestinal bleeding: Use of thrombolysis with anticoagulation in diagnosis. Radiology 207:147-151, 1998 13. Evangelista PT, Hallisey MJ: Transcatheter embolization for acute lower gastrointestinal hemorrhage. J Vasc Interv Radiol 2000;11: 601-606, 2000 14. Luchtefeld MA, Senagore AJ, Szomstein M, et al: Evaluation of transarterial embolization for lower gastrointestinal bleeding. Dis Colon Rectum 43:532-534, 2000 15. Defreyne L, Vanlangenhove P, De Vos M, et al: Embolization as a first approach with endoscopically unmanageable acute nonvariceal gastrointestinal hemorrhage. Radiology 218:739-748, 2001 16. Funaki B, Kostelic JK, Lorenz J, et al: Superselective microcoil embolization of colonic hemorrhage. AJR Am J Roentgenol 177:829836, 2001 17. Patel TH, Cordts PR, Abcarian P, et al: Will transcatheter embolotherapy replace surgery in the treatment of gastrointestinal bleeding? Curr Surg 58:323-327, 2001
PAUL V. SUHOCKI