Radiological imaging of mesenteric ischemia.

Dr/ ABD ALLAH NAZEER. MD.

Introduction:Mesenteric ischemia is a rare disease associated with a high mortality rate, especially in the acute setting. This disease is responsible for fewer than one in 1,000 hospital admissions, but its mortality rate ranges between 30%-90% . It is more prevalent in the elderly population, with comorbidities largely influencing the mortality rate.Another factor associated with the high mortality rate is the clinical presentation with nonspecific symptoms and relatively benign physical examination, which leads to a low index of suspicion and therefore delays in the diagnosis. Most of the data in the incidence of this disease is based on autopsy studies. Most cases of mesenteric ischemia are due to an acute event leading to decreased blood supply to the splanchnic vasculature. Chronic mesenteric ischemia is uncommon, accounting for <5% of cases of mesenteric ischemia, and is almost always associated with diffuse atherosclerotic disease.

PathophysiologyAcute mesenteric ischemia is most commonly secondary to acute embolism to the superior mesenteric artery (SMA), which accounts for approximately 40%-50% of all episodes. Acute mesenteric artery thrombosis is the second most common cause of acute mesenteric ischemia (20%-30%) followed by nonocclusive mesenteric ischemia (25%) and less commonly mesenteric and portal venous thrombosis (5%-15%). In the chronic setting, mesenteric ischemia is almost always caused by severe atherosclerotic disease, with rare causes including fibromuscular dysplasia, median arcuate ligament syndrome, and vasculitis Chronic mesenteric ischemia occurs due to occlusive or stenotic atherosclerotic disease and most commonly involves at least two or three main vessels. It is more prevalent in the elderly population and in patients with major risk factors for atherosclerosis such as hypertension, hyperlipidemia, and smoking history.

Clinical PresentationPatients with acute mesenteric ischemia present with abdominal pain out of proportion to the physical examination. A high index of suspicion is necessary to achieve early diagnosis. The main challenge is to differentiate acute mesenteric ischemia from other more common causes of acute abdominal pain such as appendicitis, diverticulitis, peptic ulcer disease, acute pancreatitis, gastroenterocolitis, nephrolithiasis, cholelithiasis, and cholecystitis. Early in the course of disease, laboratory findings are of little value in differentiating among these causes, with the results usually demonstrating leukocytosis, hemoconcentration, elevated amylase levels, abnormal liver enzymes, and/or metabolic acidosis.In the setting of chronic mesenteric ischemia, patients classically present with the clinical triad of postprandial abdominal pain, weight loss, and food avoidance. Nausea and vomiting, postprandial diarrhea, and signs of malabsorption may also be present.

Imaging of Mesenteric Ischemia.

Acute Mesenteric IschemiaRadiographsRadiography is usually the first imaging modality ordered for patients with acute abdominal pain but has a limited role in demonstrating primary and secondary signs of acute mesenteric ischemia. A normal radiograph does not exclude the diagnosis of acute mesenteric ischemia. Radiography findings in patients with acute mesenteric ischemia are usually nonspecific, late, and associated with a high mortality rate, as they often first appear when bowel infarction has already occurred. A radiograph typically shows bowel dilatation in the elderly patients and a gasless abdomen in younger patients with acute mesenteric ischemia . Hepatic portal venous gas is a rare but important radiographic finding associated with several pathological processes, including bowel necrosis secondary to acute mesenteric ischemia. Hepatic portal venous gas can occur alone or in association with pneumatosis intestinalis. When associated with pneumatosis intestinalis, it usually indicates the presence of advanced mesenteric ischemia. Abdominal CT appears to be superior to radiographs for detecting pneumatosis intestinalis and hepatic portal venous gas, and their underlying cause. Therefore, CT should be used as the primary diagnostic tool rather than radiography.

UltrasoundThe efficacy of US in diagnosing acute mesenteric ischemia has been evaluated in many studies. US can demonstrate proximal mesenteric vessel thrombosis via Doppler mode. It was shown that US is highly specific for identifying vascular occlusions (92%-100%) but has a lower sensitivity (70%-89%). Unfortunately, thepresence of extensive gas within the loops of bowel limits the accuracy of this imaging modality. Moreover, duplex US has a limited role in detecting distal arterial emboli or in diagnosing nonocclusive mesenteric ischemia.US might be helpful in excluding other causes of acute abdominal pain such as cholelithiasis, cholecystitis, nephrolithiasis, acute pancreatitis, or even appendicitis, but it is not recommended for initial evaluation of patients with suspected acute mesenteric ischemia because timing of the diagnosis is very critical.

Computed Tomography AngiographyCTA is a fast and noninvasive diagnostic tool for evaluating bowel and assessing intestinal vasculature. Recently the application of CTA as the ideal first-step imaging approach in patients with acute bowel ischemia has been advocated. CTA can also be helpful in stratifying patients to identify those who would benefit from angiography as opposed to the ones who should undergo emergent surgery. Vascular CT findings include arterial stenosis, embolism, thrombosis, arterial dissection, and mesenteric vein thrombosis; nonvascular CT findings include bowel wall thickening, hypoperfusion and hypoattenuation, bowel dilatation, bowel wall hemorrhage, mesenteric fat stranding, pneumatosis intestinalis, and portal venous gas. Overall, combining vascular findings with the appearance of the bowel wall resulted in a specificity of 94% with a sensitivity of 96%.

Magnetic Resonance Angiography.MRA has high sensitivity and specificity for diagnosing severe stenosis or occlusion at the origins of the celiac axis and SMA. However, it has a limited role in diagnosing distal stenosis as well as nonocclusive mesenteric ischemia, and its use may delay therapeutic options in acute settings because it is a long examination that is notreadily available in most practices. MR without contrast has lower sensitivity and specificity but may be used in cases where both iodinated and gadolinium contrast are contra-indicated.

Angiography.Angiography has been the gold standard to aid in diagnosis and preoperative planning in acute mesenteric ischemia, with sensitivity in the range of 74%-100% and specificity of 100%. Early angiography has shown to be associated with increased survival in patients with mesenteric ischemia and allows for initiation of therapeutic maneuvers. Whether angiography should precede surgical intervention in the presence of peritoneal signs is controversial. Some would favor immediate surgery in this setting, as signs of peritonitis usually indicate infarcted bowel. However, others advocate early angiography because of the importance of determining the etiology of bowel ischemia and providing a “roadmap” for revascularization procedures. Nonetheless, angiography should not be considered in patients with significant hypovolemia or hypotension.

Chronic Mesenteric IschemiaRadiographsRadiography has little to no role in the diagnosis of chronic mesenteric ischemia since these patients have not yet developed bowel necrosis, and therefore the radiograph will likely be normal or demonstrate nonspecific findings. A negative radiograph also does not exclude the diagnosis of chronic mesenteric ischemia.

UltrasoundUS with B-mode and Doppler waveform analysis is a useful initial screening tool for chronic mesenteric ischemia. Visualizing the mesenteric vessels with duplex US can be technically challenging. The SMA and celiac arteries are visualized in approximately >90% and 80%, respectively. On the other hand, the inferior mesenteric artery can hardly be visualized on transabdominal US studies due to its anatomical location and course. Peak systolic velocity has been widely used for diagnosing stenosis, with a cutoff value of 275 cm/s for the SMA and 200 cm/s for the celiac artery. US can also help in excluding other causes of chronic abdominal pain such as cholelithiasis, nephrolithiasis, and chronic pancreatitis.

Computed Tomography Angiography.CTA with 3D volume reformatting has sensitivity and specificity of 96% and 94%, respectively, for detecting chronic mesenteric ischemia. Therefore, it should be considered as a first-line alternative to angiography for diagnostic purposes . Moreover, CTAis an accurate diagnosing tool for detecting SMA syndrome. CT can also accurately exclude other causes of chronic abdominal pain.

Magnetic Resonance Angiography.MRA is a noninvasive test that has become increasingly accurate in recent years for diagnosing chronic mesenteric ischemia, with sensitivity and specificity of 100% and 95%, respectively. Nonetheless, obtaining high-resolution angiograms is still limited to the inferior mesenteric arteries, where it depicts only 25% of this vessel due to its anatomical course. MR without contrast has lower sensitivity and specificity but may be used in cases where both iodinated and gadolinium contrast are contraindicated.

Conventional angiography. of the mesenteric arteries remains the gold standard for diagnosing chronic bowel ischemia, with its therapeutic role allowing physicians performing endovascular procedures at timeof diagnosis.The success rate of angiography is reported to be as high as 88%-100%, with initial relief of symptoms in 82%-100% of cases. Nevertheless, traditional angiography is an invasive test that exposes patients to radiation and is associated with complications related to the procedure itself.

Anatomy of the mesenteric vessels.

Anatomy of the mesenteric vessels.

Drawing shows the main collateral vessels in occlusion of the CA or SMA. The pancreaticoduodenal arteries (arrow) connect the CA and the proximal SMA. The marginal artery of Drummond and the paracolic arcade (arrowhead) run between the SMA and IMA. When the IMA is also occluded, the systemic vessels (mainly the internal iliac artery) can feed the IMA (reverse flow) and the other vessels via previously described anastomosis (*).

Mesenteric ischemia. Plain abdominal radiograph in a 49-year-old woman with acute bloody bowel movements shows thumbprinting of the transverse colon.

Mesenteric ischemia. Plain abdominal radiograph in a 17-year-old male patient with encephalitis reveals pneumatosis of the colon dissecting the bowel wall.

Thumbprinting ina patient with

ischemic colitis.

Mesenteric ischemia. Ultrasonographic evaluation in an 83-year-old woman with abdominal pain reveals multiple echogenic foci within the liver, which are suggestive of portal venous air

Mesenteric ischemia. Ultrasonographic evaluation with spectral analysis and color Doppler imaging.

Duplex US findings in isolated stenosis ofthe CA. (a) Lateral US image obtained in color mode shows color aliasing. (b) Lateral US image obtained in Doppler mode shows signs of moderate stenosis with increases in systolic and diastolic velocities, as well asmild turbulence. (c) Lateral US image obtained in Doppler mode shows major poststenoticturbulence and Doppler aliasing, which indicate a stenosis of greater than 75%.

Median arcuate ligament syndrome. (a) Lateral US image obtained with energy and pulsed mode imaging during inspiration shows that the CA and SMA course downward. The velocities in the CA are slightly increased. (b) Lateral US image obtained with energy and pulsed mode imaging during expiration shows that the proximal part of the CA is lowered and impinged on by the median arcuate ligament (arrow). The velocities are markedly increased, and aliasing associated with turbulence is seen.

Duplex ultrasound of the superior mesenteric artery demonstrates a peak systolic velocity (PSV) >275 cm/second correlating with a stenosis of at least 70%.

Superior mesenteric artery stenosis Maximum peak systolic velocity of 304 cm/s and spectral broadening in the proximal SMA. This velocity exceeds the accepted PSV of 275 cm/s for the grading of a >70% stenosis.

Mesenteric ischemia. CT scan shows thickening of the transverse colon suggest a distribution in the superior mesenteric artery territory.

Mesenteric ischemia. CT scan shows wall thickening of the ascending colon. This finding also can be seen with infectious colitis.

Mesenteric ischemia. CT scan shows thickening of the ascending colon and hepatic flexure. The differential diagnoses included conditions with an infectious etiology versus ischemia.

Mesenteric ischemia. CT scan shows inflammatory changes and thickening of the hepatic flexure. Colonoscopy with biopsy showed focal mucosal necrosis with ulceration consistent with ischemic colitis

Mesenteric ischemia. CT scan obtained by using lung window parameters in a 17-year-old male patient with encephalitis reveals free retroperitoneal air.

Old man with mesenteric infarction. Contrast-enhanced CT images of upper (A), mid (B), and lower (C) abdomen show gas in portal venous branches (A), gas in mesenteric veins (circle, B), and gas in bowel wall (arrowheads, C).

Mesenteric ischemia. CT scan in a 76-year-old woman with a 4-day history of abdominal pain and leukocytosis shows congested, edematous, central small bowel loops. Thrombosis was found in the superior mesenteric vein.

Contrast-enhanced CT image in patient with embolism of superior mesenteric artery shows defect (arrowhead) in superior mesenteric artery.

Contrast-enhanced CT image with superior mesenteric vein thrombosis shows defect in superior mesenteric vein (arrowhead). Distal branches of vein are engorged.

Contrast-enhanced CT image of abdomen in with superior mesenteric vein and portal vein thrombosis. Wall thickening of ascending and transverse colon (arrowheads) is shown. Engorgement of mesenteric veins is also visible.

Contrast-enhanced CT image of abdomen with embolism of superior mesenteric artery. Bowel loops are distended with air and their wall is “paper-thin.”

Superior mesenteric artery embolism. Contrast-enhanced CT image shows that mural enhancement is absent at most intestinal loops.

Superior mesenteric artery embolism after reperfusion. Mural thickening of intestine (circle) is visible, showing target appearance.

Superior mesenteric artery embolism shows defect (arrowhead) in superior mesenteric artery. In addition, contrast enhancement of right kidney (arrow) is absent, which indicates embolism of right renal artery.

Superior mesenteric vein thrombosis. Contrast-enhanced CT image obtained cephalad to B shows thrombi in superior mesenteric vein (arrowhead) and splenic vein (arrow).

engorgement of mesenteric veins (arrowhead) and mural thickening of intestine.

Mesenteric ischemia. CT scan in a 59-year-old man with pancreatic adenocarcinoma shows a large mass encasing the superior mesenteric artery. The patient did not have abdominal symptoms of ischemia because the superior mesenteric artery remained patent. Tumor encasement is a rare cause of mesenteric ischemia.

Bowel infarct due to mesenteric arterial occlusion of the ileocolic branch.

Shock bowel after cesarean section with diffuse bowel wall thickening in the ileum(arrows) with large intra-peritoneal fluid collection due to hemoperitoneum.

Venous mesenteric ischemia

Aneurysmal dissection of the CA in a 59-year-old patient who had severe epigastricpain for several years. (a) Color Doppler US image shows an aneurysm of the celiac trunk (arrow). (b) Contrast-enhanced CT scan also shows the aneurysm (arrow). The very thin aspect of the splenic artery and the hypoattenuating crescent anterior to the splenic artery (arrowhead) are suggestive of an associated splenic artery dissection.

Contrast-enhanced CT image shows closed-loop obstruction at right lower abdomen. Distended loops are seen filled with fluid and mesentery is converging toward site of obstruction (circle). Bowel wall is slightly thickened and density of mesentery is increased.

Contrast-enhanced coronal CT image shows closed-loop obstruction at lower abdomen. Distended loops are seen around their mesentery. Contrast enhancement is absent at bowel loops on right-hand side (arrowheads) and attached mesentery shows increased density, which indicates mesenteric ischemia.

Nonocclusive mesenteric ischemia. Contrast enhancement is prominently diminished or absent at distal ileal loops (arrowheads). Bowel wall thickening is not present. After reperfusion, bowel loops show prominent wall thickening with appearance of target sign (B).

Top CT image shows gas in portal venous system (blue circle); center image shows absence of contrast in superior mesenteric artery due to thrombosis of this vessel (blue arrow) [The patient also has a markedly dilated common duct, not related to mesenteric ischemia]; lower image shows extensive pneumatosis intestinalis (red arrows).

Coronal venous-phase maximum intensity projection (MIP) image from contrast-enhanced CT shows that the caliber of the superior mesenteric vein is diminutive (large white arrows) relative to that of the inferior mesenteric vein (black arrowheads) and that there is a further size discrepancy to the superior mesenteric vein (SMV) at the junction (large black arrows) of the splenic vein (small white arrow) with the portal vein (small black arrow), representing partialSMV thrombosis. Note the resulting engorgement of the venous arcades (white arrowheads).

Noncontrast computed tomography (CT) image shows characteristic abnormalities that may be present in the later stages of acute mesenteric ischemia: pneumatosis intestinalis (small white arrows), intravascular air within the main portal vein (large white arrow) as well as within intrahepatic branches and small foci of free air (small black arrows) representing Pneumoperitoneum.

Closed-loop obstruction. Axial MR image in 52-year-old woman shows site of obstruction (arrowhead), closed loop (C), proximal loop (P), and distal loop (D) with bowel loop ischemia.

Acute mesenteric ischemia in a 43-year-old man with acute abdominal pain but no peritoneal signs. (a, b) CT scans obtained in the emergency department. (a) CT scan shows a thrombus in the SMA (arrow) and nonspecific jejunal wall thickening (arrowhead), which produces the target sign. (b) CT scan obtained 2 cm lower shows enhancement of the distal SMA (arrow), which is fed by collateral vessels, and thinningof the mesenteric wall of a jejunal loop (arrowhead), which is a more specific sign of acute ischemia. (c) Image from selective angiography of the SMA shows a thrombus in the trunk of the artery (arrow). (d) Image from selective angiography of the IMAshows that the distal SMA (arrow) is fed by a prominent marginal artery of Drummond (arrowhead). Acute thrombosis complicating preexistent distal stenosis of the SMA was suspected, and urokinase was given as an intraarterial injection of 600,000 U in 6 hours. (e) Control angiogram shows an irregular persistent stenotic lesion (arrow). (f) Angiogram shows a balloon-expandable stent, which was placed to prevent reocclusion and distal migration. Surface irregularities (arrowheads) are visible proximal and distal to the stent and may represent sites of restenosis. The patient returned home on day 5 and was asymptomatic 8 months later.

Acute SMA Thrombosis.

Acute SMV Thrombosis.

Collateral vessels in a 79-year-old patient with thrombosis of the two main visceral arteries but no abdominal symptoms. (a) Global lateral angiogram shows thrombosis of the SMA (arrowhead) and CA (arrow). (b) Image from selective angiography of the IMA shows a prominent marginal artery of Drummond connected to the paracolic arcade. (c) Angiogram shows that the paracolic arcade is connected to the SMA (arrowhead) downstream from the occlusion and feeds the jejunal arteries (). Note that the paracolic arcade is located low in the abdomen due to ptosis of the transverse colon, which is common in elderly patients.

Collateral vessels in a 66-year-old patient with abdominal angina. (a) Lateral angiogram shows thrombosis of the SMA (arrowhead) and severe stenosis of the CA (arrow). (b) Angiogram obtained with selective injection of contrast material into the IMA shows unusual serpentine collateral vessels emerging from the marginal artery of Drummond, which is not connected to the paracolic arcade. (c) Late-phase angiogram shows the SMA (arrow) and CA (arrowhead).

CMI in a 75-year-old woman with arterial dysplasia of the renal and mesenteric arteries. (a) Global angiogram. (b) Angiogram obtained with selective catheterization of the SMA by using a 5-F sidewinder catheter shows an ostial stenosis (arrow). (c) Post-angioplasty completion arteriograms obtained by using a long and armed 6-F sheath, which is pushed to the level of the mesenteric ostium (arrow).

CMI in a 45-year-old man with occlusion of both the CA and the SMA. (a) Lateral angiogram clearly shows a notch at the SMA (arrow). (b) Angiogram shows the occlusion being crossed by using a hydrophilic wire (arrow). (c) Control angiogram obtained after angioplasty shows good circulation in the SMA (arrowhead), but persistent recoil necessitated use of a stent (arrow). (d) Final angiogram shows a good result after stent placement.

Superior mesenteric artery arteriogram shows a large embolus that appears as a central filling defect (large black arrow) and has occluded the distal portion of the arterial trunk (small black arrow). A very small portion of the jejunum remains perfused (small white arrow). Note the abnormally dilated bowel loops (large white arrows) in this patient with acute mesenteric ischemia.

Digital subtraction angiography (DSA) image shows thrombosis (small black arrows) of the superior mesenteric artery that occurred distal to a high-grade stenosis (large white arrow). There is very little perfusion distal to the thrombosis. Note the previously placed stent in the celiac trunk (large black arrow), which is also occluded.

A small embolus (white arrow) has lodged distally in the superior mesenteric artery and this location allows for continued perfusion of most of the bowel in this arterial territory. This contrasts with the severe bowel ischemia that occurs with proximal embolic or thrombotic occlusion.

An acute embolus within the superior mesenteric artery appears as a filling defect (large black arrow) partially obstructing the artery. Smaller filling defects distally (small black arrows) represent fragmentation of the embolus. Note the so-called tram-track appearance in which the filling defects are partially outlined by contrast that courses between the emboli and the arterial wall.

Three-dimensional computed tomography angiography shows an extremely severe superior mesenteric artery stenosis (small white arrow), an occluded celiac trunk (large white arrow), and an enlarged and patent inferior mesenteric artery (black arrow) in a patient with symptoms of intestinal angina. The initial imaging evaluation of suspected chronic mesenteric ischemia should involve a noninvasive modality such as this.

SummaryLiterature supports conventional angiography as the gold standard test for patients with acute and chronic mesenteric ischemia except for hemodynamically unstable patients with acute mesenteric ischemia.CTA is an emerging diagnostic test with high sensitivity and specificity in the setting of both acute and chronic mesenteric ischemia and should be considered the first-line imaging test. CT can also accurately assess for other causes of acute and chronic abdominal pain, and it provides excellent anatomic mapping of the mesenteric vasculature, which is essential in the preoperative planning.MRA is an evolving technique with high sensitivity and specificity for severe stenosis or occlusions at the origin of the celiac axis and SMA, but it has a limited role in the in the evaluation of distal embolism and nonocclusive mesenteric ischemia and is only able to depict 25% of the inferior mesenteric artery. This is also a long test that is not readily available in most centers, making its use even more limited in the acute setting.US of the abdomen with Doppler waveform analysis can depict proximal mesenteric thrombosis and secondary signs of bowel compromise, but it is limited in the diagnosis of distal occlusions/stenosis and nonocclusive mesenteric ischemia and therefore is not recommended as the initial examination in evaluating patients with suspected acute mesenteric ischemia.Radiographs remain of limited value, being able to diagnosis only late stages of acute mesenteric ischemia when bowel necrosis is already present.

Thank You.