Radiologic diagnosis and treatment of gastrointestinal hemorrhage and ischemia

Med Clin N Am 86 (2002) 1357–1399

Radiologic diagnosis and treatment of gastrointestinal hemorrhage and ischemia Zvi Lefkovitz, MDa,b,*, Mitchell S. Cappell, MD, PhDc,d, Robert Lookstein, MDa,b, Harold A. Mitty, MDa,b, Perry S. Gerard, MDd,e a

Department of Radiology, Mount Sinai Medical Center, New York, NY 11206, USA b Department of Radiology, Box 1234, Mount Sinai School of Medicine, One Gustav Levy Place, New York, NY 10029-6574, USA c Division of Gastroenterology, Department of Medicine, Woodhull Medical Center, 760 Broadway Avenue, Brooklyn, NY 10029, USA d Department of Medicine, State University of New York, SUNY Downstate Medical School, 450 Clarkson Avenue, Brooklyn, NY 11203, USA e Division of Nuclear Medicine, Department of Radiology, Maimonides Medical Center, 4802 Tenth Avenue, Brooklyn, NY 11219, USA

Dramatic technical advances during the past 25 years have revolutionized the diagnosis and treatment of gastrointestinal (GI) hemorrhage and ischemia. Although advances in GI endoscopy are well known and widely disseminated, important advances in GI radiology are inadequately represented outside the radiologic and gastroenterologic literature. The radiologist has a broad armamentarium to diagnose GI hemorrhage and ischemia including spiral and multislice computerized tomography (CT), magnetic resonance (MR) angiography, radionuclide scanning, and digital subtraction angiography, in addition to traditional abdominal radiographs and barium studies. The radiologist can, moreover, treat GI hemorrhage by vasopressin infusion or embolization with superselective catheterization; treat acute intestinal ischemia with intra-arterial papaverine; and treat chronic intestinal ischemia with percutaneous transluminal angioplasty (PTA) with stenting. This article reviews the role of diagnostic and therapeutic radiologic procedures in acute or chronic GI bleeding and intestinal ischemia, with a focus on recent advances. * Corresponding author. Department of Radiology, Box 1234, Mount Sinai Medical Center, One Gustav Levy Place, New York, NY 10029-6574. 0025-7125/02/$ - see front matter Ó 2002, Elsevier Science (USA). All rights reserved. PII: S 0 0 2 5 - 7 1 2 5 ( 0 2 ) 0 0 0 8 0 - 9

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GI hemorrhage Initial management Initially GI bleeding acuity, activity, and severity are assessed. Severe bleeding with hemodynamic compromise is suggested by symptoms, such as lightheadedness, diaphoresis, syncope, and angina; signs, such as tachycardia, hypotension, orthostatic changes in blood pressure or pulse, and cold distal extremities; laboratory findings, such as a low or declining hematocrit and prerenal azotemia; and observation of hematemesis, a bloody nasogastric aspirate, or profuse hematochezia [1]. The hematocrit can be deceptively normal soon after the onset of hemorrhage before hemodilution has occurred [2]. The initial assessment also includes differentiating upper (above the ligament of Treitz) from lower GI bleeding, and variceal from nonvariceal upper GI bleeding. Acute upper GI hemorrhage generally manifests as hematemesis or melena, whereas acute lower GI hemorrhage generally manifests as hematochezia [3]. Profuse upper GI hemorrhage can occasionally produce hematochezia [4]. Prerenal azotemia, with a serum blood urea nitrogen-to-creatinine level ratio greater than 20:1, suggests an upper GI bleed [5]. Aside from routine blood chemistries and a complete blood count, serum biochemical parameters of liver function should be determined to help exclude cirrhosis and portal hypertension, which are major risk factors for variceal bleeding. A coagulation profile should also be determined to exclude coagulopathy. Nasogastric tube aspiration helps localize the bleeding site, assess the bleeding activity, and clear blood and clots from the stomach for endoscopy. The initial assessment helps guide decisions concerning blood transfusion, the timing of endoscopy, and triage to an ICU. Patient resuscitation begins during the initial evaluation to restore blood volume, by intravascular fluid administration or blood transfusion, to ensure adequate tissue perfusion and oxygenation. Patients with acute upper GI bleeding are traditionally treated, even before the cause is determined, with acid suppressive therapy, with either a histamine-2 (H2) receptor antagonist or proton pump inhibitor [6]. Endotracheal intubation should be considered to protect the airway in patients with massive hematemesis, altered mental status, or respiratory compromise [7]. Acute upper GI hemorrhage Causes of acute upper GI hemorrhage include: Relatively common causes Peptic ulcers: duodenal or gastric Esophageal and gastric varices Hemorrhagic gastritis Esophagitis Duodenitis

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Mallory-Weiss tear Marginal (anastomotic) ulcer Dieulafoy’s lesion Esophageal, gastric, duodenal, and pancreatic neoplasms Portal gastropathy Uncommon causes Angiodysplasia Gastric antral vascular ectasia Endoscopic sphincterotomy Hemobilia Aortoenteric fistula Pseudoaneurysm Gastric polypectomy Endoscopy Panendoscopy (EGD) is the first and primary procedure to evaluate and localize upper GI hemorrhage. Plain abdominal roentgenograms help to exclude associated pathology, such as GI perforation and mechanical obstruction. Barium radiography may hinder the diagnosis and treatment of acute bleeding because retained intraluminal barium may preclude angiography and hinder endoscopy [8]. Abdominal ultrasound, CT, or MRI can be useful after endoscopy to evaluate a specific underlying cause, such as a mass or malignancy. Panendoscopy is diagnostic in 90% or more of cases [5]. Likewise, EGD is therapeutic, or the bleeding spontaneously stops, in 90% or more of upper GI bleeders [9,10]. When endoscopy fails to elucidate the diagnosis or establish hemostasis, angiography should be considered to localize or control the bleeding, particularly for massive bleeding that causes hemodynamic instability or requires transfusion of 4 or more units of packed erythrocytes during a 24-hour period [11,12]. Endoscopic localization of the bleeding site, even without determining the etiology, helps guide which artery to cannulate first at angiography [13]. Negative endoscopic information, such as excluding esophageal bleeding, is also valuable for angiography. Diagnostic angiography History of angiography Nusbaum and Baum [14] applied angiography to determine the cause of GI bleeding in a landmark study in 1963. In 1965, they identified the site of GI bleeding by selective celiac and superior mesenteric artery (SMA) catheterization [15]. In 1968, Nusbaum et al [16] selectively infused vasopressin in the SMA to treat bleeding esophageal varices, and in 1970, Baum et al [17] applied this same therapy for other bleeding GI lesions. In 1971, Rosch et al [18,19] angiographically infused epinephrine or vasopressin to arrest

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acute GI bleeding. In 1972, Rosch et al [20] embolized the right gastroepiploic artery with autologous clot to control bleeding uncontrolled by selective intra-arterial epinephrine infusion. Since the introduction of angiography, the radiographic equipment, catheters, and guidewires have dramatically improved. Technical advances in digital subtraction have produced markedly improved image resolution and immediate image availability. Peripheral visceral arterial branches as small as 2 mm in diameter are routinely superselectively catheterized with 2.2F coaxial catheters [21]. Patient preparation Routine serum electrolyte values, serum parameters of renal function, and a coagulation profile are determined before angiography. Patients are resuscitated and laboratory abnormalities are corrected, when feasible, before angiography. Azotemia and hypovolemia increase the risk of nephrotoxicity from injected contrast. Severe coagulopathy should be corrected before angiography. Patients with pulmonary compromise may require endotracheal intubation and mechanically assisted ventilation before angiography. Relative contraindications to angiography include severe coagulopathy, congestive heart failure, recent myocardial infarction, renal insufficiency, pregnancy, and allergy to contrast. There are, however, no known absolute contraindications. The angiographer should briefly describe to the patient the procedure technique, risks, benefits, and alternatives, and obtain written, signed, and witnessed informed consent. Technique Angiographers should be notified early about contemplated angiography to provide time for team mobilization and patient preparation. An angiography team needs to be available on short notice at all hours for emergencies. Angiography requires local anesthesia and may require intravenous sedation. Cardiopulmonary status is monitored during angiography by continuous pulse oximetry, continuous electrocardiography, and intermittent sphygmomanometry. The pedal pulse is also monitored. Using the Seldinger technique, the angiographic catheter is inserted percutaneously into the common femoral, or axillary, artery by a guidewire and then deployed into the abdominal aorta. A standard 5F catheter is then selectively catheterized, under fluoroscopic guidance, into the celiac artery and SMA. Nonionic iodinated contrast is administered using an automatic power injector for digital subtraction angiography. If no extravasation is evident, the left gastric, gastroduodenal, pancreaticoduodenal, and splenic arteries may be sequentially selectively catheterized [22]. Diagnosis The minimal bleeding rate for angiographic detection, using state-of-theart equipment, is approximately 0.5 mL/min. The optimal bleeding rate for angiographic detection is at least 1 mL/min, which corresponds to approx-

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imately 3 units of blood per day [13]. The angiographic technique, quality of radiologic equipment, degree of vessel selectivity, and volume of injected contrast all affect test sensitivity [22]. Bleeding must occur during injection to detect extravasation because injected contrast lasts only about 30 seconds in the circulation. Intermittent bleeding that has stopped generally results in a negative angiographic study and angiography should be canceled if bleeding has ceased. When bleeding is severe and associated with shock, angiography is often bypassed in favor of emergency surgery. Bleeding is initially detected as a localized intraluminal collection of contrast material between folds on the dependant surface of bowel that first intensifies and then persists after washout of intravascular contrast media [23]. When the angiographic findings are equivocal, the catheter, when technically feasible, is advanced more distally and selectively for contrast reinjection. Normal parenchymal blushes sometimes resemble extravasation [24]. For example, a densely opacified left adrenal gland superimposed on the gastric fundus must be distinguished from extravasation [23]. When bleeding localization is uncertain in the anteroposterior projection the angiogram is repeated in another projection for precise localization. Angiography can also diagnose lesions that are not actively bleeding, such as angiodysplasia or cancer. Peptic ulcers are the most common cause of upper GI bleeding. They produce no distinctive angiographic abnormality, but their bleeding produces contrast extravasation during the arterial phase of the angiogram that persists during and beyond the venous phase and may outline GI mucosa. Hemorrhagic gastritis is an important cause of bleeding secondary to physiologic stress, particularly in the ICU. Although the incidence of stress gastritis has been reduced by prophylactic therapy of critically ill patients, this lesion is still a clinically important cause of bleeding. The bleeding typically appears at angiography as multiple small foci of extravasation in a diffusely hypervascular gastric mucosa. Although a Dieulafoy’s lesion is recognized anatomically as a caliber persistent (untapered) artery in the mucosa, this lesion is too small to be detected by angiography. The lesion is suspected when contrast extravasates from a point source, supplied by the left gastric artery or short gastric arteries, in the proximal gastric body or fundus along the lesser curvature [25–27]. The watermelon stomach (gastric antral vascular ectasia) is diagnosed by the characteristic endoscopic and histologic findings, with little diagnostic role for angiography. Angiography may reveal a diffusely hypervascular antrum [28], or no appreciable abnormalities [29,30]. The most common causes of nonvariceal esophageal hemorrhage are Mallory-Weiss tears and hemorrhagic esophagitis, both of which typically occur at the gastroesophageal junction or distal esophagus. These esophageal regions are usually supplied by the left gastric artery, and bleeding from the left gastric artery is easily detected at angiography. Bleeding lesions in the middle and proximal esophagus are generally not supplied by the left gastric artery and are difficult to detect at angiography.

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Selective angiography is limited in demonstrating venous bleeding. Bleeding esophageal varices are diagnosed only indirectly by angiographic findings of hepatofugal flow, consistent with portal hypertension, and large esophageal varices. Transjugular intrahepatic portosystemic shunt (TIPS), rather than selective angiography, is recommended for the radiologic diagnosis and therapy of bleeding esophageal varices. Complications The risks of angiography are small, especially in experienced hands [31]. Complications can occur at the puncture site or during cannulation. Local puncture site complications include thrombosis; hematoma; and, rarely, infection. Bleeding after catheter removal can be reduced or stopped by manual compression of the femoral artery. Iodinated contrast material may induce a rash; asthmatic attack; or, rarely, generalized anaphylaxis in allergic patients. Iodinated contrast material may cause nephrotoxicity. Risk factors for nephrotoxicity include renal insufficiency, hypovolemia, and prior contrast reactions. Distal embolization of an aortic or visceral vascular plaque or thrombus is a serious, but uncommon, complication that is minimized by proper training and scrupulous technique. Vascular dissection or perforation rarely occurs. Therapeutic angiography Therapeutic angiography is most strongly indicated in a frail or severely ill patient who is a poor surgical candidate, but can be considered in all patients with acute GI bleeding refractory to endoscopic therapy, particularly when contrast extravasation is demonstrated at angiography. Although selective intra-arterial vasopressin was the standard angiographic therapy [32], embolotherapy has become popular since microvascular technology has become available. Vasopressin Technique. Once bleeding is identified by contrast extravasation, the angiographic catheter is secured and 0.2 units of vasopressin per minute are infused. Vasopressin causes constriction of smooth muscle in vascular endothelium and in the bowel wall mediated by the V-1 receptor in smooth muscle. Both effects help decrease bowel wall perfusion and bleeding. The angiogram is repeated 20 minutes later to assess for hemostasis, as evidenced by cessation of contrast extravasation. If hemostasis is not achieved, the infusion rate is increased to 0.4 units per minute and then, if necessary, to 0.6 units per minute. Faster infusion is not recommended because of the risks of intestinal or myocardial ischemia. On establishing hemostasis, the patient is transferred to an ICU where the vasopressin is infused at the same rate for 12 to 24 hours, then gradually tapered during the next 24 hours, and then changed to a 5% dextrose or saline infusion for an additional 24 hours

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to maintain catheter access. If bleeding recurs during tapering, resumption of the previously effective dose usually restores hemostasis. If rebleeding recurs after catheter removal, however, repeat therapeutic angiography has a much lower efficacy [33]. Efficacy. The reported efficacy ranges from 60% to 90% [20,33–35]. Despite the postulated pathogenetic role of ischemia in stress gastritis [36], selective vasopressin infusion in the left gastric artery achieves hemostasis in 80% of cases [23]. Bleeding from an anastomotic ulcer after upper GI surgery should be treated by vasopressin, not embolization, because prior surgical ligation of collateral vessels may result in ischemia after embolization [37]. Intravenous infusion of vasopressin reduces portal pressure and stops variceal bleeding as effectively as intra-arterial infusion with fewer side effects and is the recommended route of administration for variceal bleeding [38]. Therapeutic angiography is sometimes only a temporizing measure for bleeding peptic ulcers, and when this bleeding is difficult to control angiographically, the patient, if a good surgical candidate, should be referred for surgery without prolonged attempts at angiographic therapy. Vasopressin often fails to control bleeding from cancer because cancerous blood vessels may lose vasoconstrictive responsiveness [22]. GI bleeding from cancer is best treated endoscopically for paliation or surgically for cure. Toxicity. The patient is carefully monitored for complications in an ICU during infusion. Abdominal cramps on instituting the infusion are usually caused by hyperperistalsis from vasopressin-induced muscular contraction, and are self-limited and transient. About 20% of patients experience significant side effects [39]. Vasopressin can cause bowel ischemia or infarction and is absolutely contraindicated in patients with GI bleeding from bowel ischemia. It can cause myocardial ischemia and congestive heart failure and is relatively contraindicated in patients with coronary artery disease or congestive heart failure. Simultaneous administration of sublingual nitroglycerin with vasopressin, particularly in patients who are elderly or have mild coronary artery disease, can mitigate the coronary vasoconstriction produced by vasopressin. Vasopressin can also cause ischemia of the brain, kidneys, or other end organs. Vasopressin can cause fluid retention and hyponatremia because of a weak antidiuretic effect. Other side effects include sinus bradycardia, other cardiac arrhythmias, and systemic hypertension [40]. Prolonged catheterization may cause groin hematomas at the puncture site, and thrombosis or dissection of the femoral or mesenteric arteries. Embolotherapy Technique. Selective transcatheter embolization can be used instead of, or after failure of, vasopressin therapy. Under fluoroscopic guidance the catheter is positioned as close as possible to the site of extravasation. The embolization is tailored according to the arterial supply, as determined

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by the antecedent diagnostic angiography. A precarious collateral supply from prior surgery increases the risk of gastroduodenal ischemia after embolotherapy. A rich collateral supply increases the risk of residual bleeding after embolizing one feeding vessel and may require embolizing additional vessels for hemostasis. Embolic materials. In 1975, Gianturco et al [41] introduced coils and Tadavarthy et al [42] introduced polyvinyl alcohol (Ivalon) for embolization. In 1976, other embolic materials, such as isobutyl 2-cyanoacrylate [43], and gelatin sponge pledgets [44] were introduced. Absolute alcohol or absorbable gelatin sponge powder have been largely abandoned for embolotherapy because these agents are associated with an increased risk of bowel necrosis. Autologous blood clots are not recommended because clot lysis after 12 to 24 hours may cause recurrent bleeding [45]. Currently, microcoils, either alone or with gelatin sponge pledgets or polyvinyl alcohol particles (diameter of 355 to 500 lm), are the preferred embolic materials [22,46,47]. Efficacy and complications. Several small series have demonstrated the efficacy of embolization [47–49]. Aside from demonstrated efficacy for common causes of acute upper GI bleeding, embolization has been used successfully to treat uncommon causes, including bleeding resulting from percutaneous endoscopic gastrostomy [50], pseudoaneurysms complicating pancreatitis [51], endoscopic sphincterotomy [52], and hemobilia from various causes [53]. Embolization of the left gastric artery has even been performed safely and successfully in patients after endoscopy showed active bleeding, but the angiogram failed to show extravasation presumably because of intermittent bleeding [54,55]. Arterial embolization is generally safe in the upper GI tract because it has a rich collateral arterial supply. The stomach has numerous submucosal plexuses supplied by the left gastric, splenic, gastroduodenal, and gastroepiploic arteries. The duodenum has a dual blood supply, arising from the gastroduodenal or inferior pancreaticoduodenal arteries. Nonetheless, the main complication is GI ischemia: the area at risk for ischemia is that normally perfused by the embolized vessel. Reported ischemic complications include gastric necrosis [56,57], duodenal stricture [58], splenic abscess [33], gangrenous cholecystitis, pancreatitis [59], pancreatic necrosis [60], and hepatic necrosis [53]. Minor complications include abdominal pain and fever. During the past 15 years, embolization has become safer because of greater technical expertise; improved catheter and guidewire design, including the introduction of small (2.2F catheter), radiopaque coaxial catheter systems [21,61] and open-ended guidewires [62,63]; improved radiologic equipment including digital subtraction technology; and improved embolic materials. Embolization is becoming the standard angiographic treatment for massive upper GI hemorrhage, particularly when experienced interventional

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radiologists and state-of-the-art equipment are available (Fig. 1). It has greater efficacy than vasopressin. For example, Gomes et al [64] reported 88% hemostasis with embolization, as compared with 52% hemostasis with vasopressin. Embolization is particularly favored when vasopressin is relatively contraindicated or has failed. Successful embolotherapy produces immediate hemostasis, permits prompt catheter removal, avoids the systemic toxicity of vasopressin, and facilitates early ICU discharge. Patients undergoing embolization required significantly fewer blood transfusions than patients receiving vasopressin. In one study, however, 12.5% of patients treated with embolization had major complications, as compared with 8.7% of patients treated with vasopressin [64]. Embolization can be used at most sites and for most causes of upper GI bleeding. Portal coronary vein embolization, however, has been largely supplanted by peripheral vasopressin infusion or transjugular intrahepatic portosystemic shunt for esophageal variceal hemorrhage. Embolization is effective at controlling bleeding induced by a hepatoma [65]. Acute lower GI bleeding Causes of acute lower GI bleeding include the following: Common causes Diverticulosis Hemorrhoids Colon cancer and other neoplasms Inflammatory bowel disease Angiodysplasia Bowel ischemia Adenomatous colonic polyps Uncommon causes Radiation colitis AIDS-related lesions Meckel’s diverticulum Aortoenteric fistula Postpolypectomy and other postendoscopic bleeding Acute infectious bloody diarrhea Colonic Dieulafoy’s lesion Colonic varices Colonic hemangiomas Initial diagnostic evaluation Nonhemorrhoidal lower GI bleeding is about one quarter as common a cause of hospitalization as upper GI bleeding [66]. Lower GI bleeding is more difficult to evaluate clinically than upper GI bleeding because of imprecise assessment of the bleeding rate caused by variable intestinal transit time and

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Fig. 1. Embolization of duodenal bleeding from pancreatic carcinoma. (A) Selective superior mesenteric arteriogram. The celiac artery is occluded at its origin. Retrograde flow from the inferior pancreaticodoudenal artery fills the gastroduodenal artery (arrowheads) and the hepatic branches (open arrow). There is extravasation (solid arrow) at the bleeding site. (B) Coils placed in the inferior pancreaticoduodenal artery (large arrow) by a microcatheter (small arrows). (C) Embolized vessel has thrombosed, as evidenced by no contrast visualized beyond the coils (solid arrow) and no further extravasation. Superior mesenteric artery identified by an open arrow.

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poorer endoscopic visualization of the unprepared colon than the upper GI tract. Acute ongoing lower GI bleeding can be evaluated by emergency colonoscopy on an unprepared colon, or by a bleeding scan and angiography [67]. Colonic lesions may be concealed and missed at colonoscopy because of poor colonic preparation or active bleeding [68]. When bleeding cannot be localized to the upper or lower GI tract by clinical criteria, EGD may be performed before colonoscopy to exclude an upper GI lesion. Bleeding scans Nuclear bleeding scans can localize the site of lower GI bleeding and confirm active bleeding before angiography, when colonoscopy was nondiagnostic or could not be performed because of active bleeding. Bleeding scans are rarely indicated for upper GI bleeding because EGD is so sensitive. When a bleeding scan fails to show active GI bleeding, angiography is generally not recommended because it is less sensitive, requiring a higher bleeding rate for detection. When a bleeding scan is positive, angiography or endoscopy is generally recommended to confirm the bleeding location, to diagnose the specific cause, and possibly to apply endoscopic or angiographic therapy. A positive bleeding scan, moreover, helps guide the angiographic approach: the presumed bleeding site at the bleeding scan determines which mesenteric vessel to catheterize first at angiography. Angiographers often require a positive bleeding scan as a prerequisite for emergency angiography. In comparison with angiography, nuclear scans are easy to perform, require minimal patient preparation, are noninvasive, are well tolerated, and are very safe (Table 1) [69,70]. Bleeding scans use either 99m Tc sulfur colloid or 99m Tc–labeled erythrocytes. Significantly higher doses of radioactive tracer are used in either technique, as compared with that used in a liver-spleen scan, because only a small fraction of the injected radioactive tracer extravasates. Yet, the radiation exposure is still negligible during the scan. Radioactivity is detected by a gamma camera, analyzed by a computer, and recorded on photographic film. GI bleeding is identified as local tracer extravasation into the bowel lumen. Active hemorrhage is conclusively diagnosed when a radioactive focus is identified outside the normal vascular pool; increases in intensity over time; conforms to small or large bowel anatomy in shape, location, and orientation; and exhibits antegrade or retrograde peristalsis (see Fig. 2). A static radioactive focus usually represents a vascular abnormality, such as an aneurysm, collateral vessel, or arteriovenous shunt rather than a bleeding lesion. The bleeding site is inferred from the location, shape, and orientation of the radioactive focus. Bleeding localization is particularly unreliable with delayed imaging caused by peristaltic movements with time. When a radioactive focus is identified, earlier scan images should be analyzed carefully to find the radioactive location on the first image at which the bleeding is detected and then to image radionuclide progression sequentially within bowel [71]. Yet, localization

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Table 1 Comparison of nuclear bleeding scan versus angiography in the management of acute gastrointestinal bleeding Advantages of bleeding scan

Advantages of angiography

Cheaper Less radiation exposure Less invasive Better tolerated Safer Requires fewer trained personnel Higher sensitivity at detecting bleeding Better for intermittent bleeding (can rescan for 24 h)

More precise bleeding localization May identify cause and site of bleeding Therapeutic and diagnostic

is still imprecise because of peristaltic movements of the radioactive tracer, and difficulty in determining bowel anatomy by intraperitoneal location, shape, and orientation. For example, small intestinal bleeding may be misidentified as colonic, and vice versa [72]. Small bowel bleeding is suggested by rapid sequential filling and emptying of loops. The 99m Tc sulfur colloid is extremely sensitive. It can detect bleeding as slow as 0.05 to 0.1 mL/min [69,70]. This agent is inexpensive and easy to prepare. Images are typically obtained every 1 to 2 minutes for 10 minutes. Hemorrhage can be detected only if active bleeding occurs within 10 minutes of injection because of rapid agent uptake by the reticuloendothelial system and disappearance from the bloodstream. This technique is not indicated for intermittent bleeding because the test duration is so brief. Nonbleeding structures that take up the tracer (including the liver, spleen, and bone marrow of the vertebrae and pelvic girdle) are imaged by the scan. Prominent

Fig. 2. Small bowel bleeding demonstrated by technetium 99m–labeled erythrocyte scan. (A) A focus of increased radioactive uptake is identified in the left midabdomen (arrow). (B) Antegrade and retrograde peristalsis with time results in spread of the radioactivity.

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hepatic and splenic radioactive uptake may obscure or mimic bleeding at the hepatic or splenic colonic flexures. Tracer extravasation from bleeding, however, typically travels distally in the colon because of peristalsis, whereas radioactivity from hepatic and splenic uptake remains fixed. Other tissues that can take up the colloid and produce a falsely positive scan include accessory spleens, transplanted kidneys undergoing rejection, and male genitalia. If the initial study is negative, tracer can be reinjected and the patient rescanned. The 99m Tc–labeled erythrocytes are very sensitive, detecting bleeding as slow as 0.1 mL/min, but are slightly less sensitive than 99m Tc sulfur colloid because of the persistent presence of tracer in the vascular background. The best results are obtained by labeling the patient’s own erythrocytes in vitro. This labeling requires only about 10 mL of the patient’s blood and takes only about one half hour to prepare. The major abdominal vessels including the aorta, inferior vena cava, and iliac vessels are visualized because of the presence of intravascular tracer. The liver, spleen, kidneys, and bladder uptake some radioactivity but they generally do not obscure the bleeding point. Confusion between bladder radioactivity and rectosigmoid bleeding is resolved by postvoid or lateral pelvic images [71]. Patients are often imaged for 1 to 2 hours initially. After tracer injection abdominopelvic images are taken every 3 seconds for the first minute, then every 5 minutes for the next 45 minutes, followed by every 15 to 60 minutes depending on the clinical setting. Prolonged imaging increases the likelihood of detecting intermittent bleeding, a common pattern of lower GI bleeding. Customized imaging, with computerized data storage, increases test sensitivity, as does cine imaging to follow peristaltic movements [73–76]. If the initial scan is negative, the patient can be rescanned without reinjection for up to 24 hours because the tracer remains radioactive and in the bloodstream for this duration [77]. Bleeding is, however, imprecisely localized with delayed imaging due to tracer movement with time. Falsely positive scans may be caused by pelvic or ectopic kidneys, hepatic hemangiomas, variceal veins, and venous or arterial aneurysms. The 99m Tc–labeled erythrocyte technique has a reported 93% sensitivity and 95% specificity and is generally the radioactive tracer of choice (Table 2) [78,79]. For example, in one comparative study the bleeding site was detected by labeled erythrocytes in 38 patients, but by labeled sulfur colloid in only 5 patients [78]. The 99m Tc sulfur colloid technique is generally used only for active bleeding when labeled erythrocytes are unavailable. Diagnostic angiography Rationale. Surgery, without preoperative bleeding localization, results in more extensive bowel resection, longer intraoperative time, greater patient morbidity, and higher intraoperative and postoperative mortality [12]. Bleeding localization by a bleeding scan is insufficiently precise to permit segmental colonic resection, so localization by this technique should be

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Table 2 Comparison of nuclear bleeding scan techniques: technetium-labeled erythrocytes versus technetium-labeled sulfur colloid Characteristic Minimal bleeding detection rate Type of bleeding detected Tracer circulation time within bloodstream Retesting Preparation Applicability

Technetium-labeled erythrocytes

Technetium-labeled sulfur colloid

0.1 mL/min Active or intermittent 24 h

0.05 mL/min Active only 10 min

Retest without reinjection for 24 h 10 mL of patient’s blood and 30 min to prepare General

Retesting requires reinjection No patient blood necessary and no preparation time Rarely used

confirmed by angiography before surgery. Moreover, angiographic control of the bleeding, with either vasopressin or embolotherapy, can permit elective, rather than emergent, surgical resection in good surgical candidates and can be the definitive treatment for benign bleeding lesions in poor surgical candidates. Angiography is compared with colonoscopy in Table 3. Technique. The SMA is usually cannulated initially because most lower GI bleeding arises from the right colon, which is supplied by this artery. If this study is nondiagnostic, the inferior mesenteric artery (IMA) is cannulated. Before this cannulation, the bladder should be emptied, by insertion of a Foley catheter, so that a bleeding site is not missed behind a contrast-filled Table 3 Comparison of colonoscopy versus angiography to manage lower gastrointestinal bleeding Advantages of colonoscopy Easier to perform More widely available Cheaper Less invasive Lower mortality Ability to biopsy colonic tissue for pathologic diagnosis Provides simple and effective colonoscopic therapy for bleeding Can be done when angiography is relatively contraindicated (eg, allergy to contrast) Advantages of angiography Can detect small bowel lesions during examination Can be performed on unprepared colon (intestinal blood or stool less of a problem) May be diagnostic when colonoscopy is nondiagnostic (eg, tiny bleeding lesions, such as angiodysplasia) Provides another nonoperative therapeutic modality if colonoscopic therapy is unsuccessful Can be done when colonoscopy is not technically feasible (eg, strictures or adhesions) Can treat intestinal ischemia with papaverine or PTA with stents Abbreviation: PTA, percutaneous transluminal angioplasty.

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bladder. If this study is also nondiagnostic, the celiac artery is cannulated because this artery sometimes supplies the middle colic artery and usually supplies the distal duodenum, which may be the source of obscure GI bleeding [80]. Superselective catheterization is performed as necessary. Intra-arterial digital subtraction helps decrease the volume of injected contrast [81]. Diagnosis. The accuracy of angiography for lower GI bleeding varies from 40% to 92% [82–85]. Angiodysplasia are an important cause of lower GI bleeding, particularly in the elderly. Angiodysplasia are found in approximately 2% of autopsies [86], but account for about 3% to 5% of lower GI bleeding [87–89]. They typically occur in the right colon, particularly the cecum [90]. Angiodysplasia may be missed at colonoscopy because they can be very small; located in the small intestine; obscured by overlying stool; misdiagnosed as mucosal trauma by an inexperienced endoscopist; and diminished in size or intensity by systemic hypotension, hypovolemia, and administration of meperidine during endoscopy [91]. The angiographic hallmarks of angiodysplasia include a vascular tuft or tangle resulting from the local mass of irregular vessels, best visualized in the arterial phase [92]; an early and intensely filling draining vein (early filling vein) resulting from a direct arteriovenous communication without intervening capillaries [69]; and persistent opacification beyond the normal venous phase (slowly emptying vein) possibly resulting from venous tortuosity (Fig. 3) [93,94]. About 60% to 90% of patients have each of these angiographic signs [94,95]. Angiodysplasia bleed only intermittently and extravasation of contrast material is detected in only about 10% of angiograms [96]. When nonbleeding angiodysplasia are detected in the right colon at angiography, other lesions should be excluded by colonoscopy before attributing the bleeding to the angiodysplasia and before performing right colectomy for the angiodysplasia [4]. Angiodysplasia are treated by embolotherapy; surgical resection; or endoscopic therapy, such as electrocoagulation [97–99]. Even though most diverticula are in the left colon [100], most diverticular bleeding arises from the right colon [101,102]. Diverticular bleeding appears as contrast extravasation initially enclosed within a small pocket representing the diverticulum and then overflowing into adjacent bowel (Fig. 4A). Small intestinal leiomyomas, which are uncommon, are usually hypervascular with abundant vessels. The tumor usually has a well-circumscribed margin at pathologic examination, which is reflected in a well-circumscribed hypervascular tumor blush at angiography. Intestinal carcinoids are also hypervascular, with abundant vessels within the tumor. They are most commonly located in the ileum. Angiographic findings suggestive of carcinoids include retraction, kinking, and occlusion of adjacent mesenteric vessels because of marked desmoplasia of surrounding mesentery. Colonic hemangiomas are a rare cause of lower GI bleeding. They are diagnosed better by

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Fig. 3. Angiodysplasia of cecum. (A) Superior mesenteric artery arteriogram shows a hypervascular area in the cecum containing a dense tangle of vessels (arrow). (B) Cone-down radiograph demonstrates an early draining vein (arrows), a characteristic finding of angiodysplasia.

colonoscopy than angiography. A typical angiographic finding is a focal vascular mass with associated phleboliths [103,104]. Although colon cancer, inflammatory bowel disease, and radiation colitis are usually diagnosed by colonoscopy or barium enema rather than angiography, occasionally these diseases are first recognized at angiography performed for GI bleeding or suspected intestinal ischemia. Colon cancer typically produces randomly distributed, tortuous, and irregular arteries; a hypervascular tumor blush; and early and intensely filling veins. In advanced Crohn’s disease the long vasa recta are irregularly stenosed or occluded because of vascular degeneration. Vessels may be tortuous or stretched because of intramural distortion from inflammation and fibrosis. Collateral vessels may occur. Typically the terminal ileum is most affected. In active ulcerative colitis the vasa recta are increased in caliber; they taper less than normal toward the periphery; and the draining veins are enlarged, perhaps in response to increased mucosal perfusion [105]. Typically, the distal colon is most affected. Radiation enteritis and colitis typically produce irregular stenoses of major branches of the SMA or IMA, tortuous and crowded vasa recta, and a hypovascular bowel wall. Therapeutic angiography Once bleeding is detected at angiography either angiographic therapy or surgery can ensue. Vasopressin has been effectively used since 1973 [34]. It is

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Fig. 4. Vasopressin treatment of diverticular bleeding of the ascending colon. (A) Pretreatment superior mesenteric artery arteriogram shows extravasation in the right colon (arrow). (B) Twenty minutes following infusion of vasopressin, 0.2 units/min, extravasation has ceased.

infused as aforementioned for upper GI bleeding. Efficacy varies from 47% to 92% [64,106,107]. After initial hemostasis, up to 40% experience rebleeding [107]. Vasopressin therapy is particularly effective for diverticular bleeding (see Fig. 4), and particularly ineffective for bleeding from neoplasia because of the loss of a vasoconstrictive response in blood vessels within neoplastic tissue. Diverticular bleeding sometimes recurs after hemostasis with vasopressin and then requires definitive therapy. The lower GI tract has a more sparse collateral blood supply than the upper GI tract. Embolization was initially considered a salvage therapy for patients who were poor surgical candidates and had failed vasopressin therapy because of a reported 20% rate of intestinal infarction after embolotherapy [108–114]. Initially, relatively proximal vessels were embolized, however, without superselective catheterization, so that collateral vessels were often occluded with the bleeding vessel. Recent advances in catheter and guidewire design have rendered superselective catheterization of vasa recta technically feasible to embolize the bleeding vessel without affecting collateral vessels. Several investigators have recently reported successful embolization without intestinal infarction: combining the results of four small clinical studies, embolization produced hemostasis in 34 of 37 patients with lower GI bleeding [46,115,116]. In experienced hands, superselective embolization has become a safe and primary angiographic therapy.

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Chronic (obscure) GI bleeding The causes of chronic GI bleeding include the following: Angiodysplasia or arteriovenous malformation Neoplasm Polyps Leiomyoma Meckel’s diverticulum Inflammatory bowel disease Intestinal ulcer Clinical presentation Approximately 5% of cases of GI bleeding are chronic in that it lasts from months to years [117]. Chronic bleeding presents as gross blood per rectum or occult blood detected by rectal examination. Occult bleeding is often intermittent so that testing for fecal occult blood at three different occasions is recommended to increase test sensitivity. Chronic GI bleeding is usually asymptomatic because of physiologic compensation for gradual blood loss, but patients occasionally present with lightheadedness, dizziness, or headache from inadequate cerebral perfusion; angina or congestive heart failure from compromised myocardial perfusion; and weakness or fatigue from the constitutional effects of severe anemia. Physical examination may reveal pallor; a hyperdynamic (high output) physiologic cardiac murmur; and tachycardia or orthostatic hypotension with inadequate volume repletion. Patients often have iron deficiency anemia. Although proved by pathologic examination of a bone marrow biopsy, iron deficiency anemia is usually clinically inferred from a low serum iron saturation rate and a low serum ferritin level. Initial evaluation Chronic GI bleeding is usually initially evaluated by upper and lower GI endoscopy. The order of endoscopic examination depends on the symptomatology and other clinical findings [118]. For example, a young patient with epigastric pain or prior ulcer disease should initially undergo EGD, whereas an elderly patient with a change of bowel habits should initially undergo colonoscopy. Bleeding localization by symptomatology is, however, unreliable. In the absence of symptoms, iron deficiency anemia or fecal occult blood is first evaluated by colonoscopy in the elderly. When upper and lower GI endoscopy are nondiagnostic, the bleeding is labeled obscure. It is so labeled even when a lesion is identified provided the lesion cannot account for the bleeding severity (eg, moderate gastritis in a patient with iron deficiency anemia). Further evaluation is indicated when obscure bleeding is severe; recurrent; or associated with warning signs of severe disease, such as weight loss. The evaluation should focus on the small bowel and right colon, where most obscure bleeding occurs.

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Endoscopic evaluation of small bowel Although conventional EGD includes examination up to and including the descending duodenum, the endoscopic examination is extended into the jejunum by push enteroscopy, and into the ileum by sonde enteroscopy. Push endoscopy has recently become widely available and can be mastered easily by experienced endoscopists without retraining [119]. Sonde enteroscopy is expensive, cumbersome, and available only at selected tertiary academic facilities [120,121]. A wireless videocapsule swallowed by the patient is an exciting new technique to examine the entire small bowel. The capsule is swallowed and moves passively by intestinal peristalsis. It transmits televised images by battery power using an ultrahigh frequency for about 5 hours. During the examination the patient can ambulate normally and work. In small preliminary studies, about 70% of small intestinal bleeding was localized by this videocapsule [122,123]. This technique has recently received Food and Drug Administration approval, and may become essential to evaluate small intestinal bleeding beyond the ligament of Treitz. Radiologic techniques Barium radiography of the small bowel can identify inflammatory bowel disease or small bowel neoplasms but fails to detect macular, mucosal lesions, particularly angiodysplasia. An enteroclysis study provides better radiographic imaging of the small bowel than a small bowel follow through, but requires nasoenteral intubation. The diagnostic yield of enteroclysis ranged from 10% to 25% in three large studies [124–126]; the findings included Meckel’s diverticulum, Crohn’s disease, adenocarcinoma, metastatic melanoma, leiomyosarcoma, other cancers, leiomyoma, mural hematoma, radiation enteritis, celiac disease, and intestinal ulcer. Barium enema is rarely diagnostic and rarely indicated after a nondiagnostic colonoscopy. It is useful when the colonoscopy was technically unsatisfactory or incomplete because of colonic spasm, patient uncooperation, extrinsic colonic compression, or colonic stricture. Barium enema also helps to localize lesions precisely before surgery, to evaluate extrinsic compression, and to define the anatomy of submucosal masses. Abdominal CT is useful to evaluate the extramural extent, metastasis, and potential resectability of intestinal neoplasms. Nuclear scans Conventional bleeding scans are rarely diagnostic for chronic low-volume GI bleeding because the bleeding is too slow to be detected [71], but a specialized Meckel’s scan may be useful in the appropriate clinical setting. About 2% of the population has a Meckel’s diverticulum. This is the most common congenital GI anomaly, and represents persistence of the omphalomesenteric duct [127]. The lesion is usually asymptomatic and uncommonly causes bleeding. When bleeding occurs, it is usually recurrent and

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painless. Bleeding typically occurs in children 2 years old or younger. Bleeding is from ulceration of ectopic oxyntic (gastric type) mucosa lining the diverticulum [128]. The diverticulum is diagnosed using 99m Tc pertechnetate, regardless of the presence or absence of bleeding. The 99m Tc pertechnetate is actively absorbed and excreted by normal oxyntic mucosa, and ectopic oxyntic mucosa present in a Meckel’s diverticulum is recognized in a Meckel’s scan by the absorption and excretion of this radiotracer [129]. A positive scan is detected as focal radioactivity in the right lower quadrant or midabdomen, which is anterior on a lateral view. The radioactive focus increases and decreases in parallel with oxyntic gastric mucosa and remains fixed despite intestinal peristalsis. Cimetidine increases scan sensitivity by blocking pertechnetate excretion after normal uptake by oxyntic mucosa. This scan is approximately 90% accurate [130]. A Meckel’s diverticulum that lacks oxyntic mucosa occasionally produces a falsely negative scan, and other bowel lesions occasionally produce a falsely positive scan [131]. Meckel’s diverticulum is usually treated by surgical excision. Angiography Angiography is reserved for patients with ongoing chronic bleeding who have undergone a comprehensive but fruitless diagnostic evaluation. The primary test utility is to detect angiodysplasia [132]. As aforementioned, angiodysplasia may be missed by colonoscopy. Although small bowel enteroscopy and the videocapsule can help diagnose small bowel angiodysplasia, these technologies are not readily available. Angiography permits identification of angiodysplasia located in either the small or large bowel at a single examination by the aforementioned angiographic criteria. Small intestinal angiodysplasia, however, are sometimes missed at angiography because of misidentification as normal vascular arcades [120]. Surgery Exploratory laparotomy is occasionally considered for significant, ongoing, and life-threatening obscure bleeding after a thorough, but fruitless, diagnostic evaluation. Intraoperative enteroscopy increases the diagnostic yield. The surgeon helps the endoscopist push the enteroscope through pleated bowel for enteroscopic intubation. Exploratory laparoscopy is a less invasive alternative to laparotomy [133]. The new wireless videocapsule may supplant diagnostic laparotomy for obscure GI bleeding. Surgery permits prompt therapy after diagnosis during the same procedure. New radiologic techniques Promising new diagnostic techniques for GI bleeding include helical CT after intra-arterial injection of contrast media [134], and MRI with intravascular contrast injection [135,136]. Further study of these exciting techniques is warranted.

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Mesenteric ischemia Mesenteric ischemia is classified as acute or chronic in duration and as arterial or venous in origin. In the acute form, bowel ischemia can rapidly progress to infarction if left untreated. Early diagnosis and aggressive therapy are critical because the mortality becomes very high if bowel ischemia progresses to necrosis. In the chronic form, which is uncommon, the blood supply is inadequate to meet the demand but bowel viability is not acutely compromised. Angiography is very important for the diagnosis and treatment of both forms of mesenteric ischemia. Acute mesenteric ischemia: arterial disease Causes of acute mesenteric ischemia are as follows: Intrinsic vascular disease (mesenteric vasculopathy) Thromboembolic arterial disease Nonocclusive mesenteric ischemia Vasculitis Extrinsic vascular compression Dissecting aneurysm Bowel obstruction Neoplasm Trauma Radiation The SMA emboli cause about 50% of cases and nonocclusive (vasospastic) disease about 25% of cases of acute mesenteric ischemia. The term mesenteric vasculopathy is useful to denote mesenteric ischemia caused by intrinsic vascular disease as opposed to extrinsic vascular compression [137]. Clinical presentation Acute mesenteric ischemia is responsible for about 1 per 1000 (0.1%) of hospitalizations [138]. Patients are usually more than 50 years old. Risk factors include congestive heart failure; cardiac arrhythmias, particularly atrial fibrillation; valvular heart disease; recent myocardial infarction; prior arterial emboli; recent open heart surgery; and aortic dissection [139,140]. Patients are often taking digitalis, diuretics, or beta adrenergic receptor antagonists [141]. They may have diabetes mellitus or renal insufficiency. Patients present with abdominal pain, sometimes associated with diarrhea and abdominal distention [142]. The pain is characteristically markedly disproportionate to the physical findings in early mesenteric ischemia [143]. As the ischemia progresses to infarction, however, rebound tenderness and muscle guarding inevitably ensue. Late findings include metabolic acidosis, sepsis, and shock. Leukocytosis commonly occurs.

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Diagnosis: preliminary evaluation by abdominal roentgenogram Plain abdominal roentgenography is performed in the emergency setting because it is a quick and simple test that can help exclude other causes of severe abdominal pain, such as perforated peptic ulcer. It usually shows nonspecific or no abnormalities during the early phase of intestinal ischemia. In one series of 23 patients, 74% had abnormal findings [144]. Most abnormalities, such as thickened mucosal folds, thickened bowel wall, focal gasfilled bowel loops, luminal dilatation, and multiple air-fluid levels, are nonspecific and commonly arise from other causes, such as an adynamic ileus from acute pancreatitis [141]. Thumbprinting is a specific finding of advanced disease. It appears as multiple, round, smooth, soft tissue densities projecting into the air-filled intestinal lumen because of submucosal hemorrhage and edema [145]. Ominous roentgenographic findings include pneumoperitoneum from bowel perforation, intestinal pneumatosis from intramural gas-forming bacteria, and portal vein pneumatosis from vascular invasion by gas-forming microorganisms [146]. Diagnosis: alternatives to angiography Barium studies. Barium studies are generally not indicated because barium could spill into the peritoneum if necrosis produces perforation, residual intraluminal barium precludes angiography, and more sensitive and specific tests are available. Abnormalities identified by barium studies include bowel wall and mucosal fold thickening from mural congestion and edema; separation of bowel loops by thickened mesentery; luminal dilatation from intraluminal gas or luminal narrowing from mural thickening; and rounded intraluminal defects, which correspond to the thumbprints detected on plain abdominal roentgenograms [147]. Barium studies are used to follow-up chronic complications, such as intestinal ulceration or stenosis, and are sometimes used to evaluate abdominal symptoms when mesenteric ischemia is unlikely. CT scan. When acute intestinal ischemia is in the differential diagnosis but clinically unlikely, CT is the initial diagnostic imaging modality because of excellent cross-sectional imaging of abdominal viscera, minimal invasiveness, and high safety. CT is a valuable test to evaluate abdominal pain. CT evaluates the bowel wall and adjacent mesentery, and intraperitoneal vascular structures when intravenous contrast is administered [148]. It is superior to plain abdominal roentgenograms in the diagnosis of mesenteric ischemia [149]. The most common CT abnormality is nodular or uniform mural thickening of bowel [146,148,150]. Venous thrombosis produces more frequent and more severe mural thickening than arterial obstruction because of vascular engorgement from obstructed drainage. Luminal dilatation frequently occurs. Other abnormalities include engorged mesenteric veins from disrupted drainage; increased attenuation of (streaky) mesenteric fat from mesenteric inflammation and edema; and ascites from fluid exudation

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[151–153]. Highly specific, but uncommon, findings include attenuated bowel wall enhancement from decreased perfusion, and direct identification of a mesenteric arterial or venous thrombus [146]. Pneumoperitoneum, intestinal pneumatosis, and mesenteric or portal vein pneumatosis are ominous findings [154]. Differentiation between portal vein and choledochal pneumatosis may be difficult on plain abdominal roentgenogram but is relatively straightforward on CT [145]. When CT findings suggest acute mesenteric ischemia, angiography is indicated. An MRI and ultrasound can demonstrate proximal arterial and venous thrombosis but provide less comprehensive cross-sectional abdominal imaging than CT. For example, in one study ultrasound suggested the diagnosis in only 28% of cases [146]. MRI is increasingly used to help in the diagnosis. Colonoscopy is usually the initial diagnostic test when patients present with lower GI bleeding. Diagnosis: angiography Patient preparation. Angiography is the primary diagnostic modality and is performed emergently when the signs and symptoms strongly suggest the diagnosis [143]. If angiography is performed early, acute mesenteric ischemia can be diagnosed and treated before bowel infarction develops. Angiography should be performed emergently even if surgery is contemplated to guide the surgical approach. Persistent hypotension or hypovolemia, however, are contraindications to angiography because of the decreased specificity of angiography due to hypotension-induced mesenteric vasoconstriction and the resultant delay in surgery caused by the angiography. Before angiography, the renal, electrolyte, and coagulation status of the patient are evaluated. Technique. Using the Seldinger technique, a 5F catheter is placed into the abdominal aorta rostral to the celiac artery under fluoroscopic guidance. An aortogram is then performed using an automatic power injector to inject nonionic iodinated contrast media. A biplane technique is preferred to obtain both anteroposterior and lateral projections for proper localization. The lateral projection is essential to evaluate the proximal SMA and celiac artery. Selective catheterization is tailored according to the results of the aortogram. Diagnosis. Angiography can diagnose mesenteric vasculopathy; determine the site of occlusion; define the collateral circulation; and distinguish between arterial embolus, arterial thrombus, venous thrombus, and nonocclusive ischemia (Table 4). Regardless of etiology, angiography rarely demonstrates contrast extravasation from active bleeding. Nonocclusive mesenteric ischemia (NOMI) results from mesenteric vasospasm. The vasospasm manifests as orificial narrowing of multiple SMA branches; diffuse narrowing of the SMA and its branches that produces a pruned arterial tree; alternating dilatation and narrowing of SMA branches

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Table 4 Angiographic findings with acute superior mesenteric artery obstruction Type of obstruction Embolus

Thrombus

Nonocclusive

Location

Appearance

Other findings

50% middle colic artery, 25% ileocolic artery, 15% SMA origin, 10% distal to ileocolic artery or distal SMA branches Characteristically at SMA orifice

Sharp, rounded filling defect (meniscus sign)

Poor contrast flow beyond obstruction, collaterals uncommon, minimal atherosclerosis, multiple lesions Collaterals common, extramesenteric atherosclerosis

Diffuse involvement at multiple sites of SMA and SMA branches

Extensive, irregular mesenteric arterial obstruction, planar vascular defect Alternating spasm and dilation (string-ofsausages sign), pruned arterial tree, spasm of mesenteric arcades, no embolus or thrombus

Slowed mesenteric flow, aortic reflux of contrast during injection, impaired intramural filling

Abbreviation: SMA, superior mesenteric artery. From Cappell MS. Intestinal (mesenteric) vasculopathy: I. Acute superior mesenteric arteriopathy and venopathy. Gastroenterol Clin North Am 1998;27:783–825; with permission.

that produces the string-of-sausages sign; spasm of mesenteric arcades; delayed and impaired intramural vascular filling; and reflux of contrast into the aorta caused by increased intravascular resistance. The constellation of angiographic findings is diagnostic in the presence of compatible clinical findings and in the absence of shock or vasopressor therapy. The diagnosis of NOMI is favored over the diagnosis of arterial thrombosis by an absence of extramesenteric atherosclerosis and by vasodilation after vasodilator therapy [155]. Emboli typically present as sharp, rounded filling defects (meniscus sign) in the contrast column with high-grade or totally obstructed flow [141]. When angiography is performed more than 24 hours after embolization, the embolic filling defect becomes less sharp and less round because of clot propagation. Emboli typically lodge at major bifurcations or branchings of the SMA: at the origin of the middle colic artery in 50% of cases, at the origin of the right colic and ileocolic arteries in 25%, and at the origin of the SMA in 15% (see Table 4). At the origin of the SMA distinction from a thrombus is difficult [155]. Almost half of patients have extramesenteric emboli and many have multiple emboli in SMA branches. Atherosclerotic lesions are typically minimal; this finding strongly favors the angiographic diagnosis of embolus over thrombus. Collateral vessels usually are not present because embolic obstruction occurs abruptly, without enough time to develop collaterals. Vasospasm, manifested by reduction in the caliber of the SMA or its branches, can occur.

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A thrombus typically occurs within 3 cm of the origin of the SMA from the aorta and typically produces an irregular but extensive arterial cutoff. It is associated with atherosclerosis in mesenteric and other vessels, particularly the aorta. Vasospasm commonly occurs. A thrombus usually occludes the jejunal branches of the SMA and causes ischemia beginning at the ligament of Treitz, whereas an SMA embolus typically lodges more distally and causes more distal ischemia [141]. Thrombotic obstruction usually progresses slowly so that collaterals develop to reconstitute vascular flow. When large collateral vessels from the celiac or IMA supply the SMA distal to the occlusion, the thrombosis may be chronic and not responsible for acute symptoms. The angiography is usually well tolerated. For example, in a series of 50 consecutive angiographies, complications included acute tubular necrosis in 3, local hematomas in 3, and lower extremity arterial occlusion in 1 [156]. Treatment General measures. The patient is resuscitated. Fluids are aggressively administered to replace intravascular fluid lost into the interstitium as edema, into the peritoneum as ascites, or into the lumen from fluid exudation and hemorrhage. Rehydration and optimization of cardiac function help reverse the hypotension and hypovolemia, which can exacerbate the vasospasm. Systemic disorders, such as congestive heart failure or cardiac arrhythmias, are treated aggressively. Critically ill patients may need a Swan-Ganz catheter to monitor fluid status and cardiac hemodynamics. Medications that promote vasoconstriction, such as digitalis or norepinephrine, should be discontinued or avoided. Broad-spectrum antibiotics are administered intravenously to prevent intramural bacterial proliferation and sepsis. GI decompression by a nasogastric tube may promote mucosal perfusion by decreasing intraluminal pressure. A Foley catheter should be inserted to monitor urine output. Supplemental oxygen administration may help improve intestinal oxygenation. Angiographic therapy: papaverine. Selective transcatheter papaverine infusion is recommended to reverse the vasoconstriction in both occlusive and nonocclusive acute mesenteric ischemia and to prevent or reduce the extent of bowel infarction [155,157,158]. The vasodilation is mostly limited to the SMA because papaverine is almost completely cleared during the first hepatic pass [157]. Nonetheless, papaverine is contraindicated in hypotensive patients because it may exacerbate hypotension. The treatment of acute mesenteric ischemia is based on the etiology [142]. A NOMI is definitively treated with papaverine. A 60-mg bolus is administered selectively into the SMA by the indwelling angiographic catheter immediately after angiographic diagnosis followed by continuous infusion, by an infusion pump, at 30 to 60 mg/h [142]. The papaverine is diluted in saline to a concentration of 1 mg/mL but can be concentrated further if fluid

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restriction is necessary. The catheter is sutured to the skin near the entry site to prevent dislodgement. The patient is closely monitored in an ICU. The papaverine is infused for 24 hours after which the infusion is changed to normal saline for 30 minutes before repeat angiography to determine papaverine efficacy. Angiographic evidence of papaverine efficacy includes mesenteric arterial dilation, enhanced arterial filling with contrast, and faster transit of contrast material into mesenteric veins. Clinical evidence of papaverine efficacy includes resolution of abdominal pain, stabilization of vital signs, improvement in abdominal signs, and reversal of serum laboratory abnormalities. Most patients respond within the first 24 hours. If, however, vasoconstriction persists, papaverine is infused for another 24 hours, after which the infusion is again changed to normal saline for 30 minutes before repeat angiography, and so forth up to a maximum of 5 days of papaverine infusion. Laparotomy is indicated to resect overtly necrotic bowel if patients develop persistent peritoneal signs refractory to papaverine therapy. If a second-look laparotomy is performed, papaverine infusion is continued through the second laparotomy until a follow-up angiogram demonstrates no residual vasoconstriction. Papaverine therapy improves survival to a 60% rate [141,159,160]. Patients with a large SMA embolus with persistent peritoneal signs require preoperative papaverine infusion followed by embolectomy to restore intestinal perfusion. Intestinal viability is then assessed after embolectomy and during vasodilator therapy to minimize the extent of bowel resected because borderline bowel may recover after reperfusion. Viability is assessed by inspection of intestinal color, presence of pulsations, and peristalsis; and by palpation of bowel texture and arterial pulsations [161]. When extensive bowel segments are questionably viable at laparotomy, only definitely nonviable bowel is resected. Papaverine is infused postoperatively to prevent vasospasm. A second-look operation is performed 12 to 24 hours later to resect any bowel that has become nonviable. As for NOMI, papaverine infusion is continued during the second laparotomy until follow-up angiography demonstrates no residual vasoconstriction. Approximately 10% of patients undergo second-look laparotomies, of which about 25% undergo bowel resection [162]. Boley et al [160] have achieved 55% survival with this aggressive treatment protocol. Patients with small or minor emboli of SMA branches, with pain relief by papaverine therapy, and without peritoneal signs can be treated expectantly without surgery [142]. Patients with major emboli without peritoneal signs who have strong contraindications to surgery can be treated nonoperatively if the angiogram demonstrates adequate reperfusion to the vascular bed distal to the embolus following papaverine administration. The treatment for thrombus depends on disease stage and severity. Laparotomy is performed if the patient has peritoneal signs. During angiography papaverine is generally infused even if laparotomy is needed if a catheter can be advanced into the SMA. Revascularization, by thrombec-

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tomy or vascular bypass, is performed to restore intestinal flow. Bowel viability is assessed after revascularization to minimize bowel resection. Ambiguously viable bowel is resected as aforementioned for an embolus. If the patient is stable without peritoneal signs, the patient is treated nonsurgically, with anticoagulation; hydration; and, if necessary, nasogastric decompression [109]. This therapeutic algorithm can result in 87% survival [92,163]. Papaverine infusion is generally well tolerated. The complications are similar to those aforementioned for diagnostic angiography. The catheter may become dislodged from its position in the SMA, which may suddenly cause hypotension or increased abdominal pain. The catheter position should then be checked angiographically and the catheter promptly redeployed, as necessary, into the SMA under fluoroscopic guidance. Thrombolytic therapy. Acute mesenteric ischemia occasionally has been treated successfully by thrombolytic therapy with urokinase, streptokinase, or recombinant tissue plasminogen activator [93,164–166]. For example, thrombolytic therapy was successful in 7 of 10 patients with an SMA embolus in one study [167]. Thrombolytic therapy is currently experimental and limited to medical centers with the technical expertise and limited to patients who are poor surgical candidates, who lack peritoneal signs, and who have a short duration of ischemia. Patients undergoing thrombolytic therapy require close surgical monitoring to rapidly detect progression to infarction. Acute mesenteric ischemia: venous thrombosis Clinical presentation Superior mesenteric vein (SMV) thrombosis causes 5% to 10% of acute mesenteric ischemia [165]. It is frequently associated with hypercoagulable states [165]. Patients often have prior deep venous thrombosis caused by an underlying hypercoagulopathy [168]. The clinical presentation is often subtle early in the disease and becomes characteristic only when advanced and severe, when ischemia progresses to necrosis. Symptoms include abdominal pain in 85%, anorexia in 50%, GI bleeding in 50%, diarrhea in 45%, and nausea and vomiting in 45% [137,169]. The abdominal pain is typically severe and disproportionate to the physical findings. Physical signs depend on the severity and stage of intestinal injury. Peritoneal signs are late manifestations that indicate bowel infarction. Laboratory abnormalities include leukocytosis, neutrophilia, elevated serum lactate, and hyperamylasemia. Metabolic acidosis and hypoxia suggest severe intestinal insult. Abdominal roentgenogram The diagnosis is usually made by CT or angiography. Plain abdominal roentgenograms are usually either normal or demonstrate nonspecific abnormalities, such as an ileus. Mucosal thumbprinting is a late roentgenographic

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finding. Significant roentgenographic abnormalities, such as pneumoperitoneum or pneumatosis intestinalis, usually reflect bowel infarction but rarely differentiate between arterial and venous occlusion. CT scan The CT scan is diagnostic in about 80% of cases [165]. Abdominal ultrasound is less sensitive because overlying bowel gas often limits SMV visualization. CT demonstrates a thrombus in the mesenteric, portal, or splenic vein as a central area of low density surrounded by an enhanced peripheral vascular rim [170]. An early thrombus has a higher attenuation value than a late thrombus because of gradual degradation of blood within the thrombus. Other CT abnormalities include a dilated SMV, collateral mesenteric vessels, intestinal mural thickening, vascular engorgement, persistent mural contrast enhancement, dilated bowel, thickened and streaky mesentery, and polypoid intraluminal projections corresponding to the thumbprints present on abdominal roentgenogram [171]. MRI shows promise as a diagnostic test [172]. Angiography Angiography is essential when arterial occlusion, particularly NOMI, is in the differential because of the high diagnostic sensitivity and therapeutic efficacy of angiography for this condition. Angiographic findings include slow or absent filling of the SMV, a persistent filling defect in the SMV from the thrombus, a prolonged arterial phase, a prolonged intramural vascular blush, and arterial spasm [173,174]. When the obstruction has a chronic component, angiography may demonstrate reconstitution of flow around the thrombus by collateral vessels. Angiography is, however, less sensitive at detecting superior mesenteric venopathy than arteriopathy. The SMV may fail to opacify because of technical factors, and when the diagnosis is in doubt selective injections with higher contrast volumes or during papaverine infusion may be necessary to improve SMV opacification. Therapy Intravenous anticoagulation with heparin is indicated to prevent thrombus propagation or recurrence. After acute heparinization, prolonged anticoagulation with warfarin is generally recommended [175]. Surgery is performed to resect nonviable bowel if signs of intestinal infarction develop. Thrombolytic therapy has been rarely used [137]. The mortality of SMV thrombosis is about 25% [169,176]. Ischemic colitis Clinical presentation and etiology Ischemic colitis accounts for about 1 per 2000 hospitalizations [177]. The term ischemic colitis is useful to describe the phenomenology of colonic ischemic injury, especially as observed on colonoscopy, but fails to specify

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the obstructed vessel, mechanism, and cause. The physician should assiduously analyze ischemic colitis to determine the occluded vessel (among colonic branches of the SMA, SMV, IMA, and inferior mesenteric vein); to determine the mechanism of occlusion (among embolus, thrombus, or vasospasm); and to determine the underlying etiology (among atherosclerosis, vasculitis, low-flow states, and hypercoagulopathy) [178]. Ischemic colitis is most commonly caused by atherosclerosis with thrombosis of the IMA or colonic branches of the SMA. IMA emboli are uncommon because most emboli are too large to enter this narrow vessel. Aortic surgery can produce colonic ischemia from iatrogenic IMA ligation, intraoperative hypotension, or rarely atheroemboli [179]. The clinical presentation varies with the underlying cause, extent of vascular obstruction, rapidity of ischemic insult, and degree of collateral circulation. About 75% have abdominal pain. The pain is typically abrupt in onset, crampy, mild, and localized to the left lower quadrant. Other common symptoms include lower GI bleeding, abdominal distention, diarrhea, and nausea or vomiting [180]. The bleeding is typically mild. Signs include mild tenderness over the involved intestinal segment, abdominal distention, low-grade pyrexia, tachycardia, and fecal occult blood. Severe ischemia manifests with leukocytosis, neutrophilia, and a shift to immature leukocyte forms on the leukocyte differential. Plain abdominal roentgenogram Abdominal roentgenogram usually shows only nonspecific findings, such as bowel dilation, air-filled bowel loops, colonic aperistalsis, mural thickening, and ahaustral bowel, but is valuable to exclude other abdominal disorders. Specific findings occur in about 20% of cases [181]. The most characteristic finding is thumbprinting. Pneumoperitoneum, pneumatosis coli, and portal vein pneumatosis indicate impending colonic infarction [146]. Barium enema and CT The sensitivity of barium enema approaches 80% [182]. The most common specific finding is thumbprinting. Other findings include longitudinal ulcers in 60%, eccentric mural deformity in 50%, sacculation in 30%, and transverse ridging from symmetric circumferential contractions in 13% [182]. Abnormalities are typically segmental because the ischemia is segmental and are typically transient because the mucosa rapidly heals. The CT is not routinely performed but may be indicated to exclude other diseases. CT findings include mural thickening, luminal narrowing, and polypoid filling defects that correspond to the thumbprinting [183]. Colonoscopy Colonoscopy is generally the diagnostic test of choice. Colonoscopy is preferred because of a higher sensitivity than barium enema; a higher specificity because of the ability to biopsy mucosa for pathologic analysis; and the

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ability subsequently to perform angiography. With frank necrosis, colonoscopy reveals cyanotic, dusky, gray, or black mucosa. Hemorrhagic nodules at colonoscopy correspond to the thumbprints present at barium enema. Nonspecific colonoscopic findings include mucosal friability, mucosal edema, mucosal erythema, mural spasm, superficial ulceration, and luminal narrowing [184]. Ischemic injury localized to the ascending colon suggests SMA occlusion, which usually requires angiography for further evaluation and therapy. Therapy Patients who have physical signs or laboratory evidence of peritonitis require surgery. Patients are otherwise treated expectantly with medical therapy, including parenteral fluid administration with nothing per os, hyperalimentation, broad-spectrum antibiotics, and colonic decompression with a rectal tube [178]. Most patients rapidly improve with medical therapy. Chronic mesenteric ischemia Etiology and pathophysiology include the following: Atherosclerosis Arteritis and vasculitis Hypercoagulable states Fibromuscular hyperplasia Mesenteric artery dissection Aortic aneurysm Median arcuate ligament compression More than 95% are caused by mesenteric atherosclerosis [185]. Clinical presentation The disease is uncommon but not rare. The disease usually develops after the age of 60, and is threefold more common in women than men. Patients commonly have prior vascular disease, affecting the lower extremities, coronary arteries, renal arteries, or cerebral arteries [186]. Risk factors for atherosclerosis, including cigarette smoking, hypertension, and diabetes mellitus, are common. The classic symptomatic triad is postprandial pain; fear of eating (sitophobia); and involuntary weight loss. This triad typically occurs with advanced disease. The pain typically is chronic and dull, begins 15 to 30 minutes postcibum, and persists for 1 to 4 hours [187]. As the disease progresses, the pain becomes progressively more severe and longer lasting, and occurs after eating smaller amounts of food. Physical examination often reveals an abdominal bruit [188]. Signs of weight loss and malnutrition, such as temporal wasting, are common. Many patients have evidence of peripheral vascular disease, such as absent distal

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pulses and trophic changes in the feet, and of coronary artery disease, such as electrocardiographic abnormalities [189]. Pathophysiology The abdominal viscera are supplied by the celiac axis, SMA, and IMA. Vessels occlude slowly in chronic mesenteric ischemia permitting collaterals to develop to prevent bowel infarction. The celiac artery and SMA communicate by anastomoses between the superior pancreaticoduodenal branch of the gastroduodenal artery, which arises from the hepatic artery, and the inferior pancreaticoduodenal artery, which arises from the first part of the SMA. When the celiac artery is stenosed or occluded, blood flows from the SMA to branches of the celiac artery, and when the proximal SMA is occluded or stenosed blood flows in the reverse direction. An anastomosis may also occur between the ascending division of the left colic branch of the IMA and the left division of the middle colic branch of the SMA in response to stenosis or occlusion of either the IMA or proximal SMA. This anastomosis is called the meandering artery or arc of Riolan [190]. Occasionally, the IMA, which is usually small, may become huge and supply the entire abdominal viscera [191,192]. Because of this rich collateral network, generally at least two of the three major mesenteric vessels must be diseased before symptoms of chronic mesenteric ischemia occur [185]. Diagnosis Upper GI series, CT, and MRI. An upper GI series with small bowel follow through, performed to evaluate abdominal pain or involuntary weight loss, may demonstrate nonspecific findings of contrast segmentation, flocculation, and dilution; of bowel dilatation and hypoperistalsis; and of mural thickening [147]. An abdominal CT may help identify other causes of abdominal pain or help guide the surgical approach by defining the collateral circulation or demonstrating other abdominal diseases that affect the surgical approach [193]. Multislice CT is being used to evaluate chronic mesenteric ischemia. MR angiography is a promising noninvasive test that can accurately demonstrate proximal stenosis of the celiac axis and SMA [194,195]. Doppler ultrasonography. Mesenteric duplex ultrasonography is a promising noninvasive test available at tertiary medical centers. The SMA is visualized in about 95% of cases, whereas the celiac axis is visualized in 80%, and the IMA in less than 50% [196,197]. The degree of vascular stenosis is quantified from flow velocity. Stenosis increases flow velocity. Other findings suggestive of significant stenosis include poststenotic flow turbulence and collateral vessels [198]. The test is fairly accurate provided the vessels are identified and the technical expertise is available. Angiography. Angiography is indicated to confirm the diagnosis, to assess the need for surgery, and to plan the surgical approach. The angiography

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should be biplanar and should include selective catheterization to evaluate distal mesenteric vessels. The anteroposterior view best visualizes the aforementioned collateral pathways and the renal arteries, whereas the lateral view best visualizes proximal visceral vessels, particularly the SMA and celiac arteries. Both views visualize the abdominal aorta. Aortography typically reveals high-grade stenosis (less than one-third normal flow) of both the celiac axis and SMA (Fig. 5). This finding is diagnostic in symptomatic patients, but nonspecific in asymptomatic patients [155]. Patients with two-vessel disease are often asymptomatic because of adequate collateral perfusion [199]. Most patients also have significant IMA stenosis [189]. Approximately one-third of patients demonstrate stenosis of one or both renal arteries, and approximately one-quarter demonstrate atherosclerosis of the infrarenal abdominal aorta [185,200]. The presence of collateral vessels suggests that the ischemia is chronic and that the vascular obstruction is hemodynamically significant. Arteritis and fibromuscular dysplasia produce a characteristic angiographic pattern of patency of the origin of the major mesenteric arteries and stenoses of small mesenteric branches [201,202]. Median arcuate ligament compression is diagnosed at aortography as compression of the proximal celiac artery on a lateral projection [203,204]. Treatment The goal of therapy is to restore mesenteric blood flow to maintain bowel viability and relieve the symptoms. The choice of therapy depends on the pattern of vascular stenoses, the presence of associated arterial lesions, the etiology, and patient comorbidity. Surgery. Surgery is the primary treatment. Nutritional deficiencies and electrolyte abnormalities should be corrected preoperatively, usually parenterally. Generally, both the celiac axis and SMA are reconstructed. Surgical options include thromboendarterectomy, bypass grafting, and reimplantation [190]. Transaortic visceral endarterectomy and antegrade prosthetic aortovisceral bypass grafting are particularly effective, with long-term patency rates of 70% to 93% [205]. The operative mortality, however, ranges from 3% to 20% [206]. Percutaneous transluminal angioplasty. After catheterizing the celiac artery or SMA, the stenosis is crossed by a guidewire under fluoroscopic guidance and the catheter advanced beyond the stenosis. An exchange guidewire is inserted to facilitate advancement of the balloon catheter. The balloon diameter corresponds to the diameter of the vessel just proximal to the stenosis. Usually a 6- or 8-mm diameter balloon is used [94]. The pressure gradient across the stenosis is measured before and after angioplasty. Residual stenosis after angioplasty is assessed by reinjecting contrast. Angioplasty can be repeated safely, if necessary, to optimize the results.

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Fig. 5. Chronic mesenteric ischemia in an 80-year-old woman presenting with the classic symptomatic triad of weight loss; postprandial pain; and sitophobia (fear of eating). (A) Early phase aortogram does not demonstrate any definite abnormality. (B) Late-phase aortogram demonstrates retrograde flow from the hypogastric to the superior hemorrhoidal arteries (small arrows) and retrograde flow up the inferior mesenteric artery to its point of occlusion (large arrow). Flow then continues in a retrograde fashion by the marginal artery (open arrows), which then joins the superior mesenteric artery (curved arrow) to provide additional blood flow to the bowel. This appearance suggests inadequate blood flow in the superior mesenteric artery. (C) Lateral aortogram demonstrates proximal celiac artery (open arrow) and proximal superior mesenteric artery (solid arrow) stenosis. (D) Lateral aortogram demonstrates the superior mesenteric artery becomes markedly increased in caliber (arrow) after angioplasty and stenting of this artery. The patient’s symptoms disappeared following the procedure.

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The PTA has been used to treat focal atherosclerotic stenoses of the visceral vessels since 1980 [207]. PTA avoids general anesthesia, and results in a shorter hospitalization and lower cost than surgery [178]. PTA is safe and effective. Long-term success rates range from 63% to 100%, with a mortality of 0% to 13% [208,209]. Risks include vessel dissection, atheromatous embolization with bowel infarction, vessel thrombosis, or early restenosis [210,211]. PTA is favored in poor surgical candidates, such as patients with severe coronary artery disease. PTA is not recommended for numerous or long stenoses, for stenoses caused by extrinsic compression, and for suspected bowel necrosis [193,212]. Percutaneous stent placement. The recent development of intravascular stents provides another nonsurgical treatment option for use in conjunction with angioplasty. After SMA or celiac artery catheterization with a 5F catheter, a guidewire is inserted under fluoroscopic guidance across the stenosis and a catheter containing a stent at its tip is advanced across the lesion under fluoroscopic guidance. Recent studies have shown stent safety and efficacy (see Fig. 5). Sheeran et al [213] recently reported a 92% success rate, and Nyman et al [214] reported a 100% success rate in small clinical series, with rare complications. Stenting may improve long-term patency with angioplasty. Stenting is particularly recommended when balloon angioplasty is technically difficult, when vascular flow is inadequate after balloon angioplasty, and when angioplasty causes vessel dissection [193]. Although surgery is currently preferred because of a higher long-term patency rate, intravascular stents with angioplasty show great promise because of a lower complication rate and shorter patient hospitalization. Further progress in guidewire, catheter, stent, and angiographic equipment should render angioplasty and stents even more attractive.

Summary Major breakthroughs in catheter, guidewire, and other angiographic equipment currently allow interventional radiologists to diagnose massive life-threatening upper and lower GI hemorrhage and to stop the bleeding safely and effectively using superselective catheterization and microcoil embolization. Similarly, the interventional radiologist can treat acute intestinal ischemia safely and effectively with selective catheterization and papaverine administration and treat chronic mesenteric ischemia by percutaneous angioplasty and stent placement. A multidisciplinary approach, including the gastroenterologist, radiologist, and surgeon, is critical in managing GI bleeding and intestinal ischemia, particularly in patients at high risk or presenting as diagnostic dilemmas.

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