Computed Tomography Angiography and Magnetic Resonance Angiography Imaging of the Mesenteric Vasculature Klaus D. Hagspiel, MD, Lucia Flors, MD, Michael Hanley, MD, and Patrick T. Norton, MD Computed tomography angiography (CTA) and magnetic resonance angiography (MRA) are highly accurate cross-sectional vascular imaging modalities that have almost completely replaced diagnostic catheter angiography for the evaluation of the mesenteric vasculature. CTA is the technique of choice when evaluating patients with suspected mesenteric ischemia; it permits to differentiate between occlusive and nonocclusive etiologies, to evaluate indirect signs of bowel ischemia, and in some instances, to provide alternative diagnoses. MRA has the advantage of not using ionizing radiation and iodinated contrast agents and can be appropriate in the nonacute setting. Both CTA and MRA are suitable for the assessment of patients with suspected chronic mesenteric ischemia, allowing to evaluate the degree of atherosclerotic steno-occlusive disease and the existence of collateral circulation, as well as other nonatherosclerotic vascular pathologies such as fibromuscular dysplasia and median arcuate ligament syndrome. CTA provides excellent depiction of visceral aneurysms and has an important role to plan therapy for both occlusive and aneurysmal diseases and in the follow-up of patients after open or endovascular mesenteric revascularization procedures. This article provides an introduction to the CTA and MRA imaging protocol to study the mesenteric vasculature, the imaging findings in patients presenting with acute and chronic mesenteric ischemia and visceral aneurysms, and the value of these imaging techniques for therapy planning and follow-up. Tech Vasc Interventional Rad ]:]]]-]]] C 2014 Elsevier Inc. All rights reserved. KEYWORDS Mesenteric Ischemia, CT Angiography, MR Angiography
Introduction The blood supply to the intestinal tract is derived from the 3 major anterior branches of the abdominal aorta: the celiac artery (CA), the superior mesenteric artery (SMA), and the inferior mesenteric artery (IMA). Examination of patients with suspected mesenteric ischemia or mesenteric aneurysms requires detailed evaluation of these 3 arterial systems and their branches. Computed tomography angiography (CTA) and magnetic resonance angiography (MRA) are highly accurate cross-sectional vascular imaging modalities that have almost completely replaced diagnostic catheter angiography for the Department of Radiology and Medical Imaging, University of Virginia Health System, Charlottesville, VA. Address reprint requests to Klaus D. Hagspiel, MD, Department of Radiology and Medical Imaging, University of Virginia Health System, Charlottesville, VA 22908. E-mail: [email protected] 1089-2516/14/$ - see front matter & 2014 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1053/j.tvir.2014.12.002
evaluation of the mesenteric vasculature.1-4 Catheter-based angiography is nowadays reserved for endovascular therapy or when noninvasive studies are equivocal. The objective of this article is (1) to review the CT and MR imaging (MRI) technique to study the mesenteric vasculature, (2) to review the role of these techniques and the imaging findings in patients presenting with acute and chronic mesenteric ischemia and visceral aneurysms, and (3) to summarize their value for therapy planning and follow-up.
Imaging Technique Multidetector CTA (MDCTA) allows the acquisition of a 3-dimensional (3D)volume during the peak enhancement phase of the vessels of interest following intravenous injection of iodinated contrast material.5,6 State-of-the-art CT systems have gantry rotation times under 300 ms and can cover the entire abdomen and pelvis during a breath 1
2 hold with 0.6-mm isotropic collimation.7,8 Accurate scan timing is achieved by using automated bolus timing techniques. For the initial assessment of patients referred with symptoms of mesenteric ischemia, we perform a biphasic scan consisting of arterial and portal venous phases, the latter with a fixed scan delay of 70 seconds after the start of the contrast agent injection. To minimize the radiation dose, we do not perform an unenhanced CT scan as part of our mesenteric ischemia protocol.9 For the assessment of mesenteric aneurysms, we perform only an arterial phase scan. In patients who underwent treatment of an aneurysm with a covered stent, we perform a triphasic scan (unenhanced, arterial and portal venous phase) similar to that in patients after aortic aneurysm endografts.10 The unenhanced acquisition is helpful for detecting endoleaks. We do not use oral contrast or water before the scans. We review the maximum intensity projection images for delineation of stenoses and use axial source images and multiplanar reformation for evaluation of stent patency or vessels with calcification. Volume-rendering techniques can be helpful for the evaluation of complex visceral aneurysms. Radiation exposure is an ongoing concern with CT. All vendors actively pursue ways to reduce radiation dose while maintaining image quality. We incorporate iterative reconstruction techniques in all our scan protocols with significant dose reduction.11 Dualenergy CT (DECT) is another evolving CT technique using 2 simultaneous acquisitions at different energy levels, allowing differentiation of material based on quantifiable differences in X-ray attenuation.12 DECT characterizes iodine, calcium, and other materials within tissues by their different absorptiometric properties. In particular, DECTbased automated bone removal and calcified plaque removal are useful for mesenteric CTA. By creating monochromatic data sets, dual-energy CTA has the potential to minimize blooming and beam hardening artifacts that simulate or conceal vascular stenosis.13 Recent concerns about nephrogenic systemic fibrosis have led to increased interest in noncontrast-enhanced MRA, and a number of different techniques have been used to assess the mesenteric vasculature. Time-of-flight MRA, phase-contrast MRA, and MR oximetry have been used in the past but ultimately have been abandoned with the advent of newer, more reliable scan techniques.14-18 Steady-state free precession MRI is a newer noncontrast MRI technique that is useful for the assessment of the aorta, but less so for the smaller mesenteric arteries.19 More recently, cardiac-triggered 3D steady-state free precession sequences were developed for renal and mesenteric noncontrast MRA using respiratory gating.20,21 This allows scanning without breath holding; however, the sequence is not as robust as the contrast-enhanced MRA (ceMRA) techniques and is mainly useful for evaluation of the proximal celiac and mesenteric arteries. The use of 3D ceMRA forms the backbone of MR examinations of the mesenteric vasculature.22-24 A highresolution 3D T1-weighted gradient-echo pulse sequence is used in conjunction with intravenous injection of
K.D. Hagspiel et al gadolinium contrast material. With this technique, images of the aorta and its branches can be acquired during a breath hold. We repeat the sequence 3 times to obtain portal venous and systemic venous information in addition to the arterial phase. With the use of modern 1.5- or 3-T MR systems, phased-array coils and parallel imaging techniques, high-image quality, and depiction of small and distal branches can be achieved.25 Spatial resolution and slab thickness of the 3D imaging volume can be adjusted to tailor the acquisition time to the breath-hold interval. Typically, 60-88 sections of 1-2 mm in thickness constitute a 3D slab. Repetition time and echo time for the 3D gradient-echosequence are chosen as short as possible,22 with modern MR scanners allowing a repetition time of 3 ms or less, resulting in acquisition times between 10 and 20 seconds. The echo time is typically in the order of 1.0-1.5 ms, short enough to avoid the effects of spin dephasing that can cause signal loss in areas of turbulence and result in overestimation of stenosis. High-quality mesenteric ceMRA achieves sub 1-mm uninterpolated isotropic voxels; however, its resolution is still inferior to CTA. Arterial signal in ceMRA is based solely on the T1 shortening effect of the gadolinium bolus during its first pass through the vascular territory of interest. Therefore, correct timing and dosing of the gadolinium bolus is critical to achieve high arterial contrast and image quality. An extracellular paramagnetic MR contrast agent is infused via a peripheral venous access using an automated injector at a dose of 0.1 mmol/kg, which we find to be sufficient for high-quality abdominal MRA.24 The center of k-space is primarily responsible for image contrast, and peak arterial enhancement is timed to coincide with its acquisition. It is therefore important to adjust the acquisition timing to the type of k-space mapping, for example, sequential vs centric. The peripheral k-space lines determine image detail, and it is not necessary to maximize arterial contrast during this phase of data acquisition. For this reason, the gadolinium bolus needs only last for part of the scan duration, which allows for reduced contrast dose. The injection rate is adjusted to produce a contrast bolus lasting approximately one-half to two-thirds of the scan duration, and we use an automatic triggering technique. Typical injection rates range from 1-2 mL/ s.24,26 Several groups have investigated the influence of caloric stimulation on image quality with conflicting results and thus we do not use this technique.27,28 The use of anticholinergic agents has not been proven to affect positively on image quality.29 Compared with catheter angiography, state-of-the-art ceMRA has favorable interobserver variability in the common and proper hepatic arteries, the splenic artery, the SMA, as well as the portal, superior mesenteric, and splenic veins.30 However, agreement is poor, and catheter angiography is still necessary for the evaluation of the intrahepatic arteries, the SMA branches as well as the IMA.31 Despite continually improved technology, mesenteric ceMRA is clearly inferior to MDCTA. One of the advantages of performing ceMRA on 3-T system is the ability to reduce the contrast dose owing to the inherently higher signal of
CTA and MRA imaging of the mesenteric vasculature gadolinium at higher field strengths. However, to date, there is no convincing evidence for the diagnostic superiority of ceMRA at 3 T over 1.5 T for the abdominal vasculature. Time-resolved MR techniques have led to a significant reduction in acquisition times.32,33 They provide morphologic and hemodynamic flow information, similar to conventional digital subtraction angiography (DSA). Time-resolved MRA uses view-sharing techniques that undersample the periphery of k-space to increase temporal resolution as compared with traditional ceMRA. We use a sequence providing a voxel size of 1.0 1.0 4.0 mm with a temporal resolution of 2.2 seconds for a 3D data set. As its main advantage is the ability to assess flow dynamics, it can
3 be helpful to diagnose shunts owing to arteriovenous fistulas or delayed portomesenteric venous filling in patients with nonocclusive mesenteric ischemia. A study involving 22 patients undergoing low-contrast-dose time-resolved MRA of the abdominal aorta and its major branches at 3-T magnet concluded that the technique provides rapid and important anatomical and functional information in the evaluation of the abdominal vasculature, but owing to its limited spatial resolution, it is inferior to standard ceMRA in demonstrating fine vascular details.33 Enhanced T1-weighted breath-held gradient-echo fat-saturated sequences are an important component of our mesenteric MRA protocol. They are particularly beneficial for the assessment of arterial and venous thrombi and emboli.34
Figure 1 A 87-year-old man with a history of atrial fibrillation presents with sudden onset of severe abdominal pain. He developed abdominal distention and underwent CTA. Sagittal MPR shows abrupt occlusion of the SMA approximately 3 cm distal to its origin (arrow) (A). A coronal MPR shows the length of the embolus (B). A 2-chamber long-axis reconstruction of the heart demonstrates residual thrombus (arrow) in the left atrial appendage, the source of the embolus (C). MPR, multiplanar reformation.
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Acute Mesenteric Ischemia Acute interruption of the blood supply to the small bowel or colon or both is a catastrophic event, with a morbidity and mortality exceeding 60%.35 The 4 major causes of
acute mesenteric ischemia are SMA embolus, SMA thrombosis, mesenteric venous thrombosis, and nonocclusive mesenteric ischemia (NOMI).35 Aortic dissections have also been reported to cause acute mesenteric ischemia (AMI) on rare occasions.4
Figure 2 A 76-year-old woman develops acute abdominal pain following surgical repair of a juxtrarenal abdominal aortic aneurysm with a tube graft complicated by occlusion of the inferior mesenteric artery. CTA was performed emergently. A volume-rendered image shows the aortic tube graft as well as patent celiac trunk and superior mesenteric arteries (A). A coronal arterial phase CTA MPR shows an occluded inferior mesenteric artery (arrow) as well as lack of enhancement and stranding surrounding the descending colon (arrowheads) (B). An oblique portal venous phase MPR demonstrates the transition between normally enhancing large bowel and the nonenhancing necrotic bowel (arrowheads) (C). Lung windows show pneumatosis of the left colon (arrowheads) (D). MPR, multiplanar reformation. (Color version of figure is available online.)
CTA and MRA imaging of the mesenteric vasculature
Figure 3 A 75-year-old woman with CMI undergoes CTA. Sagittal thin-slab MIP of the arterial phase shows severe tandem ostial stenosis of the celiac trunk (arrowheads) and an occlusion of the SMA (arrow) (A). Coronal MIP shows the enlarged arc of Riolan that provides collateral flow from the IMA to the SMA territory (B). A volumerendered image shows the enlarged IMA (arrow), as well as the arc of Riolan (arrowheads) (C). MIP, maximum intensity projection. (Color version of figure is available online.)
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6 Acute emboli to the SMA account for approximately 40%-50% of all episodes of AMI,35 with the typical patient having a history of cardiovascular disease (Fig. 1). Most emboli in the SMA lodge just beyond the origin of the middle colic artery. Acute mesenteric arterial thrombosis is usually associated with a pre-existing atherosclerotic lesion and consequently a history of intestinal angina is present in up to 50% of cases.35 In contrast to the abrupt catastrophic onset of symptoms associated with an embolus to the SMA, the abdominal pain and symptoms associated with acute mesenteric arterial thrombosis may be more insidious owing to the development of collateral circulation. Thrombotic occlusion of the SMA occurs typically near the ostium, unlike embolic occlusion.35,36 CTA demonstrates calcified and noncalcified ostial plaques, thrombus, as well as collateral vessel.4 Occasionally, acute thrombosis complicates abdominal vascular surgical procedures (Fig. 2). Mesenteric venous thrombosis is rare and can be related to hypercoagulation, infection, portal hypertension, trauma, or malignancy among other causes. It does not typically cause severe bowel ischemia. Nonocclusive mesenteric ischemia (NOMI) is thought to be responsible for approximately 25% of cases of AMI, with a mortality rate as high as 70%.4 NOMI usually develops during an episode of cardiogenic shock or a state of hypoperfusion in which excessive sympathetic activity results in secondary splanchnic vasoconstriction. The response to intraarterial papaverine during DSA is both diagnostic and therapeutic, but the diagnosis can occasionally be made with CTA if there is lack of mesenteric venous enhancement on the portal phase scan in conjunction attenuated SMA branches.37 Approximately 5% of patients with aortic dissection develop mesenteric ischemia as a complication
of the dissection process.35 Isolated dissections of the SMA, either in association with cystic degeneration or as a complication of catheter angiography, are extremely rare but readily diagnosed on CTA. In acute cases, perivascular stranding is typical in isolated SMA dissections.4 Besides assessment of the mesenteric vessels, MDCTA permits the evaluation of secondary signs of bowel ischemia such as bowel dilatation, bowel wall thickening or thinning, edema, submucosal hemorrhage, abnormal wall contrast enhancement (either absent or decreased enhancement, or hyperenhancement), and pneumatosis intestinalis, as well as portomesenteric venous gas, mesenteric fat stranding, ascites, and pneumoperitoneum. In addition, it can provide alternative diagnoses in these patients. A recent study of 91 patients with suspected AMI resulted in the diagnosis of mesenteric ischemia in 18 patients, 14 of whom were of the thromboembolic type and 4 of the nonocclusive type. Positive CTA findings were confirmed by surgery in 13 patients and by clinical followup in 3 cases. Other etiologies for abdominal pain in this cohort were diagnosed by CT in 38 patients out of the remaining 74. There were 2 false-positive and 2 falsenegative CT results, with an overall accuracy of 95.6%. The authors concluded that MDCTA is a fast and accurate investigation for the diagnosis of acute mesenteric ischemia and in most cases can be used as the sole diagnostic procedure.38 The American College of Radiology recently published Appropriateness Criteria for Imaging of Mesenteric Ischemia,39 a document evaluating and rating the appropriateness of imaging to evaluate patients with clinically suspected mesenteric ischemia. The document stated
Figure 4 A 66-year-old man with typical symptoms for CMI. Sagittal thin-slab MIP of a ceMRA demonstrates highgrade ostial stenoses of the celiac trunk, SMA, and IMA (arrows) (A). An axial T1-weighted fat-suppressed 3D breath-hold image using the VIBE sequence demonstrates normal thickness and enhancement of both small and large bowel (B). MIP, maximum intensity projection; VIBE, volumetric interpolated breath-hold examination.
CTA and MRA imaging of the mesenteric vasculature “while catheter-based angiography has been considered the reference standard and enables diagnosis and treatment, advances in computed tomography have made it a first-line test in many patients because it is a fast, widely available, and noninvasive study.” MRA received a less favorable review because although providing “high sensitivity and
7 specificity for diagnosing severe stenosis or occlusion at the origins of the celiac axis and SMA, 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 not readily available in most practices.”39
Figure 5 A 76-year-old woman with chronic abdominal pain undergoes ceMRA for surveillance for an infrarenal abdominal aortic aneurysm. Sagittal MIP demonstrated a moderate to severe stenosis of the celiac trunk and a patent SMA (A). A coronal MIP showed the AAA (asterisk) as well as the main collateral pathway via the pancreaticoduodenal arcades (arrows) with several aneurysms (arrowheads) (B). A CTA performed a few weeks later for planning of an endovascular aneurysm repair shows a severe ostial stenosis of the celiac trunk (arrow) (C) as well as the aneurysms (D). Note the significantly higher spatial resolution of the CTA scan. AAA, abdominal aortic aneurysm; MIP, maximum intensity projection. (Color version of figure is available online.)
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Chronic Mesenteric Ischemia Chronic mesenteric ischemia (CMI) is almost always caused by severe atherosclerotic disease and characterized by a classical clinical triad of postprandial abdominal pain, weight loss, and food avoidance.35 Both CTA and MRA are suitable for the assessment of patients with suspected CMI4 (Figs. 3-5). Although atherosclerosis of the mesenteric circulation is frequent in the elderly, CMI is relatively uncommon, primarily owing to abundant mesenteric collateral circulation (Fig. 3). Knowledge of collateral pathways between the mesenteric arteries is of utmost importance for the correct interpretation of the imaging studies. More than 50 collateral pathways in the large and small bowel have been described.40 The marginal artery of Drummond is situated along the mesenteric border of the colon and formed by the anastomotic continuation between the right, middle, and left colic arteries. The arc of Riolan is situated more centrally within the mesentery and is an inconstant anastomosis between the middle and left colonic arteries (Fig. 3). The meandering artery is also situated within the mesentery and is a very large tortuous vessel communicating between the SMA and IMA. It potentially represents an enlarged arc of Riolan. The dominant collateral pathway between the CA and the SMA is via the gastroduodenal artery and the pancreaticoduodenal arcades (Fig. 5). The arc of Buhler is a persistent embryonic artery and a direct
communication between the CA and SMA. The arc of Barkow (greater omental arcade) consists of arteries and veins within the greater omentum that anastomose between the left and right gastroepiploic arteries.41-43 This mesenteric collateral network can make it difficult to estimate the degree of mesenteric vascular stenosis necessary to cause intestinal angina. It is generally accepted that at least 2 of the 3 main vessels have to be affected by stenoocclusive disease to produce clinical symptoms.35 CTA has been used in the evaluation of CMI with an accuracy approaching 95%-100%.1 However, extensive calcification may limit the diagnostic value of CTA. Drawbacks to CTA include the use of iodine-based contrast agents and radiation. ceMRA is an alternative to CTA in the evaluation of patients suspected of having CMI. The sensitivity and specificity of 3D contrast MRA is approximately 95%100%. A limitation of MRI are the current inability to scan patients with pacemakers, the issue of claustrophobia, availability, lengthy examination time, and the inability to assess patients with mesenteric stents. A recent prospective study comparing stenosis grading of the celiac trunk and the SMA using duplex sonography, CTA, and MRA at 1.5 T in 52 patients with DSA as the reference found that CTA provided the best image quality, reached the highest level of agreement and significance in correlation in stenosis grading, and offered the best diagnostic accuracy44 (Fig. 5). A number of nonatherosclerotic vascular pathologies can cause CMI.4 Fibromuscular dysplasia is a rare but
Figure 6 A 80-year-old woman with chronic abdominal pain undergoes CTA. Finding of sagittal MIP in inspiration was read as normal. Note high-grade ostial stenosis of the IMA (arrow) (A). Owing to suspicion for median arcuate ligament syndrome, the patient returned for repeat scan in expiration. This demonstrated moderate narrowing of the SMA (arrowhead) as well as the IMA stenosis (arrow) (B). MIP, maximum intensity projection.
CTA and MRA imaging of the mesenteric vasculature well-recognized cause of CMI. Median arcuate ligament syndrome is caused by extrinsic compression of the celiac trunk or the celiac neural plexus or both by the central tendon of the crura of the diaphragm. The classic finding on a lateral view of the aorta consists of a smooth indentation of the superior aspect of the proximal CA, which is more marked on expiration than on inspiration4 (Fig. 6). Median arcuate ligament compression can occasionally involve the proximal SMA and even renal arteries. CTA or MRA scans should be done in expiration if this entity is suspected. Aortic dissections can cause both acute and chronic mesenteric ischemia.4 Chronic mesenteric ischemia has also been described as one of the many manifestations of vasculitides, especially Takayasu arteritis.4
Visceral Artery Aneurysms Visceral artery aneurysms comprise a rare but clinically important vascular disease entity. Their incidence,
9 etiology, and natural history are not entirely understood, and patients frequently present emergently.45 The prevalence of visceral artery aneurysms in reported autopsy series ranges from 0.01%-10%.45,46 They involve the splenic (60%), hepatic (20%), superior mesenteric (5.5%), celiac (4%), gastric and gastroepiploic (4%), intestinal (jejunal, ileal, and colic; 3%), pancreaticoduodenal and pancreatic (2%), gastroduodenal (1.5%), and inferior mesenteric arteries (rare).45,46 Splenic artery aneurysms are the most common visceral artery aneurysms with the reported incidence in autopsy series ranging from 0.1%-7.1% (Fig. 7). The average age of patients with splenic aneurysms ranges from 48 to greater than 60 years, and they are twice more frequent in women than in men, with 20% being multiple. The reported risk of rupture ranges from 3.0%-9.6% with mortality rates between 10% and 25%.45 The risk is significantly higher in women during pregnancy. The exact mechanism behind
Figure 7 A 55-year-old woman undergoes CTA for abdominal pain. Axial source image shows a 3.5-cm splenic artery aneurysm (arrow) with mural thrombus and wall calcifications (A). The patient was treated with placement of a covered stent (Viabahn, W.L. Gore & Associates, Newark, DE). Spot film immediately following deployment of the stent (arrow) shows contrast trapped in the excluded aneurysm sac (B). This can persist for several days after placement and can simulate an endoleak on postprocedural CT scans. Follow-up CTA was obtained several months following the procedure and showed a patent covered stent (arrows), patent splenic artery and excluded aneurysm (C).
10 aneurysm formation is not clearly understood, and their etiology can be divided into 4 categories: degenerative, inflammatory, posttraumatic, and pregnancy related. In contrast to aneurysms of large vessels, atherosclerosis is not considered to be the primary etiologic factor for splenic aneurysms.46 Patients with portal hypertension and splenomegaly have also been found to have a higher incidence of splenic artery aneurysms.45,46 Inflammatory pseudoaneurysms are almost always associated with pancreatitis and the presence of pseudocysts and always require therapy. Very rarely, pseudoaneurysms are caused by other regional inflammatory diseases such as peptic ulcer disease. Most aneurysms are found incidentally on imaging performed for other causes, with CTA being the most sensitive study in our opinion. MRI or MRA is less sensitive (Fig. 5). The surgical literature recommends repair of splenic artery aneurysms when they are larger than 2 cm or are found to have been enlarged, with a more aggressive approach in pregnant women and women of childbearing age considering pregnancy.46 Hepatic artery aneurysms are the second most frequent visceral aneurysms. Overall, 66% of hepatic aneurysms are extrahepatic. Hepatic artery aneurysms are most frequently the result of penetrating, iatrogenic, or blunt trauma. Mycotic aneurysms can be found in patients with a history of intravenous drug abuse. Rare causes are vasculitides such as polyarteritis nodosa and periarterial inflammation caused by either cholecystitis or pancreatitis. Fibromuscular dysplasia, segmental mediolytic arteriopathy, and connective tissue diseases are other noninflammatory etiologies (Fig. 8). Most patients with hepatic artery aneurysms present with rupture.46 The aneurysms usually
Figure 8 A 69-year-old woman with Ehlers-Danlos syndrome and postprandial epigastric pain. Volume-rendered CTA image shows multiple aneurysms of the superior mesenteric artery (arrowheads) as well as a thrombosed splenic artery aneurysm (arrow). (Color version of figure is available online.)
K.D. Hagspiel et al rupture into the biliary system or the peritoneal cavity, and this is associated with very high mortality. Quincke triad is the classic finding of hepatic aneurysm rupture and consists of epigastric pain, hemobilia, and obstructive jaundice. SMA aneurysms are the third most common visceral aneurysm accounting for 5.5% of these lesions. They almost always involve the proximal 5 cm of the main SMA trunk.45 The SMA is the most common site for infection of a peripheral muscular artery, with mycotic aneurysms comprising 58% of these lesions.46 Of these, most patients are less than 50 years of age, and 63% of reported SMA aneurysms occur in men.45,46 Many patients with aneurysms of the SMA have subacute bacterial endocarditis. Dissecting aneurysms associated with medial defects are rare but affect this vessel more than any other visceral artery. SMA aneurysms require treatment even in asymptomatic patients because spontaneous rupture is frequent and mortality is high. Surgery is the preferred treatment option but can be complicated as inflammation and infection are common features of these aneurysms.
CTA and MRA for Treatment Planning and Following Surgical or Endovascular Therapy MDCTA is the preferred modality to plan therapy for both occlusive and aneurysmal diseases in our institution (Fig. 7). CTA easily allows detection and characterization of stenoses with higher accuracy than ceMRA. Also, calcifications, whose presence can have major effect on the choice of therapeutic procedure, are readily identifiable. The assessment of complex aneurysms with multiple afferent and efferent branches is best done with MDCTA; real-time assessment of the 3D data set using volume rendering on a dedicated workstation allows comprehensive assessment of these lesions and greatly facilitates both surgical treatment and endovascular therapy (Fig. 8). MDCTA is the most useful tool to follow patients after all currently used open or endovascular mesenteric revascularization procedures, including surgical embolectomy, thrombectomy, bypass graft placement, endarterectomy, surgical release of the median arcuate ligament, mechanical thrombectomy, angioplasty, catheter-directed thrombolysis, fenestration of the dissection membrane, stent placement, and endoluminal stent-graft placement.47 MRA is limited in the setting of metallic implants such as stents but has been shown to be equivalent to DSA for the evaluation of visceral artery aneurysms after coil embolization.48 CTA assessment of stent patency can be facilitated by reconstructing the images with a sharp (bone) kernel and a smaller field of view that minimizing the blooming artifact (Fig. 9). A rare immediate complication of successful surgical and endovascular revascularization is the development of reperfusion syndrome, which can lead to liver failure,
CTA and MRA imaging of the mesenteric vasculature
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Figure 9 A 69-year-old man who underwent previous placement of stents into the celiac trunk and superior mesenteric arteries for CMI presents with recurrent symptoms. A CTA was performed. Sagittal MPR of arterial phase CTA using the standard soft tissue kernel does not allow assessment of stent patency with certainty (A). Dedicated stent reconstruction using bone kernel, smaller FOV, and 50% overlap clearly demonstrates compression of the celiac stent (arrow) as well as narrowing of the SMA stent. There is also intimal hyperplasia in both stents seen as dark lines (arrowheads) (B). MPR, multiplanar reformation.
ascites, pancreatitis, and food intolerance caused by bowel and visceral organ hyperemia. CTA readily demonstrates hyperemia of the bowel and early filling of the mesenteric veins on arterial phase imaging.45 The assessment of complex aneurysms with multiple afferent and efferent branches is best done with MDCTA; real-time assessment of the 3D data set using volume rendering on a dedicated workstation allows comprehensive assessment of these lesions and greatly facilitates both surgical treatment and endovascular therapy (Fig. 8).
Conclusion Both MDCTA and ceMRA are highly accurate crosssectional vascular imaging modalities for the evaluation of the mesenteric vasculature. Owing to its availability, acquisition speed as well as ability to detect bowel wall abnormalities, MDCTA is the modality of choice for patients presenting with AMI. It is also well suited to follow patients after all endovascular and open surgical procedures for occlusive and aneurysmal mesenteric arterial disease. CeMRA has the advantage of not using ionizing radiation and iodinated contrast agents and can be appropriate in the nonacute setting.
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hypertension pre- and postintrahepatic shunt placement. Hepatology 24:1109-1115, 1996 Burkart DJ, Johnson CD, Ehman RL, et al: Related articles evaluation of portal venous hypertension with cine phase-contrast MR flow measurements: High association of hyperdynamic portal flow with variceal hemorrhage. Radiology 188:643-648, 1993 Wasser MN, Geelkerken RH, Kouwenhoven M, et al: Systolically gated 3D phase contrast MRA of mesenteric arteries in suspected mesenteric ischemia. J Comput Assist Tomogr 20:262-268, 1996 Chan FP, Li KC, Heiss SG, et al: A comprehensive approach using MR imaging to diagnose acute segmental mesenteric ischemia in a porcine model. Am J Roentgenol 173:523-529, 1999 Iozzelli A, D'Orta G, Aliprandi A, et al: The value of true-FISP sequence added to conventional gadolinium-enhanced MRA of abdominal aorta and its major branches. Eur J Radiol 72:489-493, 2009 [Epub 2008 Oct 15] Khoo MM, Deeab D, Gedroyc WM, et al: Renal artery stenosis: Comparative assessment by unenhanced renal artery MRA versus contrast-enhanced MRA. Eur Radiol 21:1470-1476, 2011 Wyttenbach R, Braghetti A, Wyss M, et al: Renal artery assessment with nonenhanced steady-state free precession versus contrastenhanced MR angiography. Radiology 245:186-195, 2007 Meaney JF, Prince MR, Nostrant TT, et al: Gadolinium-enhanced MR angiography of visceral arteries in patients with suspected chronic mesenteric ischemia. J Magn Reson Imaging 7:171-176, 1997 Baden JG, Racy DJ, Grist TM: Contrast-enhanced three-dimensional magnetic resonance angiography of the mesenteric vasculature. J Magn Reson Imaging 10:369-375, 1999 Heverhagen JT, Reitz I, Pavlicova M, et al: The impact of the dosage of intravenous gadolinium-chelates on the vascular signal intensity in MR angiography. Eur Radiol 17:626-637, 2007 Lum DP, Busse RF, Francois CJ, et al: Increased volume of coverage for abdominal contrast-enhanced MR angiography with twodimensional autocalibrating parallel imaging: Initial experience at 3.0 Tesla. J Magn Reson Imaging. 30:1093-1100, 2009 Nissen JC, Attenberger UI, Fink C, et al: Thoracic and abdominal MRA with gadofosveset: Influence of injection rate on vessel signal and image quality. Eur Radiol. 2009;19(8):1932-1938. Hany TF, Schmidt M, Schoenenberger AW, et al: Contrast-enhanced three-dimensional magnetic resonance angiography of the splanchnic vasculature before and after caloric stimulation. Original investigation. Invest Radiol 33:682-686, 1998 Shirkhoda A, Konez O, Shetty AN, et al: Mesenteric circulation: Three-dimensional MR angiography with a gadolinium-enhanced multiecho gradient-echo technique. Radiology 202:257-261, 1997 Kopka L, Rodenwaldt J, Vosshenrich R, et al: Hepatic blood supply: Comparison of optimized dual phase-contrast-enhanced threedimensional MR angiography and digital subtraction angiography. Radiology 211:51-58, 1999 Carlos RC, Stanley JC, Stafford-Johnson D, et al: Interobserver variability in the evaluation of chronic mesenteric ischemia with gadolinium-enhanced MR angiography. Acad Radiol 8:879-887, 2001 Ernst O, Asnar V, Sergent G, et al: Comparing contrast-enhanced breathhold MR angiography and conventional angiography in the
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evaluation of mesenteric circulation. Am J Roentgenol 174:433-439, 2000 Barger AV, Block WF, Toropov Y, et al: Time-resolved contrastenhanced imaging with isotropic resolution and broad coverage using an undersampled 3D projection trajectory. Magn Reson Med 48:297-305, 2002 Kramer U, Fenchel M, Laub G, et al: Low-dose, time-resolved, contrast-enhanced 3D MR angiography in the assessment of the abdominal aorta and its major branches at 3 Tesla. Acad Radiol 17:564-576, 2010 Wetzel SG, Law M, Lee VS, et al: Imaging of the intracranial venous system with a contrast-enhanced volumetric interpolated examination. Eur Radiol 13:1010-1018, 2003 Hagspiel KD, Angle JF, Spinosa DJ, et al: Mesenteric Ischemia: Angiography and Endovascular Interventions. in Longo W, Peterson GJ, Jacobs DL (eds.), Intestinal Ischemia Disorders: Pathophysiology and Management. St. Louis, MO: Quality Medical Publishing, Inc., 105-154, 1999 Barmase M, Kang M, Wig J, et al: Role of multidetector CT angiography in the evaluation of suspected mesenteric ischemia. Eur J Radiol 80:e582-e587, 2011 Bozlar U, Turba UC, Hagspiel KD: Nonocclusive mesenteric ischemia: Findings at multidetector CT angiography. J Vasc Interv Radiol 18:1331-1333, 2007 Ofer A, Abadi S, Nitecki S, et al: Multidetector CT angiography in the evaluation of acute mesenteric ischemia. Eur Radiol 19:24-30, 2009 Oliva IB, Davarpanah AH, Rybicki FJ, et al: ACR appropriateness criterias imaging of mesenteric ischemia. Abdom Imaging 38: 714-719, 2013 Michels NA, Siddarth P, Kornblith PL, et al: The variant blood supply to the small and large intestines: Its import in regional resections. J Int Coll Surg 39:127, 1963 Basmajian JV: The marginal anastomoses of the arteries to the large intestines. Surg Gynecol Obstet 99:614, 1954 Moskowitz M, Zimmerman H, Felson B: The meandering mesenteric artery of the colon. Am J Roentgenol 92:1088, 1964 Drummond H: Some points relating to the surgical anatomy of the arterial supply of the large intestine. Proc R Soc Med 7:185, 1913 Schaefer PJ, Pfarr J, Trentmann J, et al: Comparison of noninvasive imaging modalities for stenosis grading in mesenteric arteries. Rofo 185:628-634, 2013 Stanley JC: Abdominal visceral aneurysms. in Haimovici H (ed.), Vascular Emergencies. New York, NY: Appleton-Century-Crofts, 387-396, 1981 Shin T, Hagspiel KD: Visceral artery aneurysms: Endovascular management. in Kandarpa K (ed.), Peripheral Vascular Interventions. Philadelphia, PA: Lippincott Williams & Wilkins, 263-276, 2008 [chapter 15] Shih MC, Angle JF, Leung DA, et al: CTA and MRA in mesenteric ischemia: Part 2, normal findings and complications after surgical and endovascular treatment. Am J Roentgenol 188:462-471, 2007 Iryo Y, Ikushima I, Hirai T, et al: Evaluation of contrast-enhanced MR angiography in the follow-up of visceral arterial aneurysms after coil embolization. Acta Radiol 54:493-497, 2013
Introduction The blood supply to the intestinal tract is derived from the 3 major anterior branches of the abdominal aorta: the celiac artery (CA), the superior mesenteric artery (SMA), and the inferior mesenteric artery (IMA). Examination of patients with suspected mesenteric ischemia or mesenteric aneurysms requires detailed evaluation of these 3 arterial systems and their branches. Computed tomography angiography (CTA) and magnetic resonance angiography (MRA) are highly accurate cross-sectional vascular imaging modalities that have almost completely replaced diagnostic catheter angiography for the Department of Radiology and Medical Imaging, University of Virginia Health System, Charlottesville, VA. Address reprint requests to Klaus D. Hagspiel, MD, Department of Radiology and Medical Imaging, University of Virginia Health System, Charlottesville, VA 22908. E-mail: [email protected] 1089-2516/14/$ - see front matter & 2014 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1053/j.tvir.2014.12.002
evaluation of the mesenteric vasculature.1-4 Catheter-based angiography is nowadays reserved for endovascular therapy or when noninvasive studies are equivocal. The objective of this article is (1) to review the CT and MR imaging (MRI) technique to study the mesenteric vasculature, (2) to review the role of these techniques and the imaging findings in patients presenting with acute and chronic mesenteric ischemia and visceral aneurysms, and (3) to summarize their value for therapy planning and follow-up.
Imaging Technique Multidetector CTA (MDCTA) allows the acquisition of a 3-dimensional (3D)volume during the peak enhancement phase of the vessels of interest following intravenous injection of iodinated contrast material.5,6 State-of-the-art CT systems have gantry rotation times under 300 ms and can cover the entire abdomen and pelvis during a breath 1
2 hold with 0.6-mm isotropic collimation.7,8 Accurate scan timing is achieved by using automated bolus timing techniques. For the initial assessment of patients referred with symptoms of mesenteric ischemia, we perform a biphasic scan consisting of arterial and portal venous phases, the latter with a fixed scan delay of 70 seconds after the start of the contrast agent injection. To minimize the radiation dose, we do not perform an unenhanced CT scan as part of our mesenteric ischemia protocol.9 For the assessment of mesenteric aneurysms, we perform only an arterial phase scan. In patients who underwent treatment of an aneurysm with a covered stent, we perform a triphasic scan (unenhanced, arterial and portal venous phase) similar to that in patients after aortic aneurysm endografts.10 The unenhanced acquisition is helpful for detecting endoleaks. We do not use oral contrast or water before the scans. We review the maximum intensity projection images for delineation of stenoses and use axial source images and multiplanar reformation for evaluation of stent patency or vessels with calcification. Volume-rendering techniques can be helpful for the evaluation of complex visceral aneurysms. Radiation exposure is an ongoing concern with CT. All vendors actively pursue ways to reduce radiation dose while maintaining image quality. We incorporate iterative reconstruction techniques in all our scan protocols with significant dose reduction.11 Dualenergy CT (DECT) is another evolving CT technique using 2 simultaneous acquisitions at different energy levels, allowing differentiation of material based on quantifiable differences in X-ray attenuation.12 DECT characterizes iodine, calcium, and other materials within tissues by their different absorptiometric properties. In particular, DECTbased automated bone removal and calcified plaque removal are useful for mesenteric CTA. By creating monochromatic data sets, dual-energy CTA has the potential to minimize blooming and beam hardening artifacts that simulate or conceal vascular stenosis.13 Recent concerns about nephrogenic systemic fibrosis have led to increased interest in noncontrast-enhanced MRA, and a number of different techniques have been used to assess the mesenteric vasculature. Time-of-flight MRA, phase-contrast MRA, and MR oximetry have been used in the past but ultimately have been abandoned with the advent of newer, more reliable scan techniques.14-18 Steady-state free precession MRI is a newer noncontrast MRI technique that is useful for the assessment of the aorta, but less so for the smaller mesenteric arteries.19 More recently, cardiac-triggered 3D steady-state free precession sequences were developed for renal and mesenteric noncontrast MRA using respiratory gating.20,21 This allows scanning without breath holding; however, the sequence is not as robust as the contrast-enhanced MRA (ceMRA) techniques and is mainly useful for evaluation of the proximal celiac and mesenteric arteries. The use of 3D ceMRA forms the backbone of MR examinations of the mesenteric vasculature.22-24 A highresolution 3D T1-weighted gradient-echo pulse sequence is used in conjunction with intravenous injection of
K.D. Hagspiel et al gadolinium contrast material. With this technique, images of the aorta and its branches can be acquired during a breath hold. We repeat the sequence 3 times to obtain portal venous and systemic venous information in addition to the arterial phase. With the use of modern 1.5- or 3-T MR systems, phased-array coils and parallel imaging techniques, high-image quality, and depiction of small and distal branches can be achieved.25 Spatial resolution and slab thickness of the 3D imaging volume can be adjusted to tailor the acquisition time to the breath-hold interval. Typically, 60-88 sections of 1-2 mm in thickness constitute a 3D slab. Repetition time and echo time for the 3D gradient-echosequence are chosen as short as possible,22 with modern MR scanners allowing a repetition time of 3 ms or less, resulting in acquisition times between 10 and 20 seconds. The echo time is typically in the order of 1.0-1.5 ms, short enough to avoid the effects of spin dephasing that can cause signal loss in areas of turbulence and result in overestimation of stenosis. High-quality mesenteric ceMRA achieves sub 1-mm uninterpolated isotropic voxels; however, its resolution is still inferior to CTA. Arterial signal in ceMRA is based solely on the T1 shortening effect of the gadolinium bolus during its first pass through the vascular territory of interest. Therefore, correct timing and dosing of the gadolinium bolus is critical to achieve high arterial contrast and image quality. An extracellular paramagnetic MR contrast agent is infused via a peripheral venous access using an automated injector at a dose of 0.1 mmol/kg, which we find to be sufficient for high-quality abdominal MRA.24 The center of k-space is primarily responsible for image contrast, and peak arterial enhancement is timed to coincide with its acquisition. It is therefore important to adjust the acquisition timing to the type of k-space mapping, for example, sequential vs centric. The peripheral k-space lines determine image detail, and it is not necessary to maximize arterial contrast during this phase of data acquisition. For this reason, the gadolinium bolus needs only last for part of the scan duration, which allows for reduced contrast dose. The injection rate is adjusted to produce a contrast bolus lasting approximately one-half to two-thirds of the scan duration, and we use an automatic triggering technique. Typical injection rates range from 1-2 mL/ s.24,26 Several groups have investigated the influence of caloric stimulation on image quality with conflicting results and thus we do not use this technique.27,28 The use of anticholinergic agents has not been proven to affect positively on image quality.29 Compared with catheter angiography, state-of-the-art ceMRA has favorable interobserver variability in the common and proper hepatic arteries, the splenic artery, the SMA, as well as the portal, superior mesenteric, and splenic veins.30 However, agreement is poor, and catheter angiography is still necessary for the evaluation of the intrahepatic arteries, the SMA branches as well as the IMA.31 Despite continually improved technology, mesenteric ceMRA is clearly inferior to MDCTA. One of the advantages of performing ceMRA on 3-T system is the ability to reduce the contrast dose owing to the inherently higher signal of
CTA and MRA imaging of the mesenteric vasculature gadolinium at higher field strengths. However, to date, there is no convincing evidence for the diagnostic superiority of ceMRA at 3 T over 1.5 T for the abdominal vasculature. Time-resolved MR techniques have led to a significant reduction in acquisition times.32,33 They provide morphologic and hemodynamic flow information, similar to conventional digital subtraction angiography (DSA). Time-resolved MRA uses view-sharing techniques that undersample the periphery of k-space to increase temporal resolution as compared with traditional ceMRA. We use a sequence providing a voxel size of 1.0 1.0 4.0 mm with a temporal resolution of 2.2 seconds for a 3D data set. As its main advantage is the ability to assess flow dynamics, it can
3 be helpful to diagnose shunts owing to arteriovenous fistulas or delayed portomesenteric venous filling in patients with nonocclusive mesenteric ischemia. A study involving 22 patients undergoing low-contrast-dose time-resolved MRA of the abdominal aorta and its major branches at 3-T magnet concluded that the technique provides rapid and important anatomical and functional information in the evaluation of the abdominal vasculature, but owing to its limited spatial resolution, it is inferior to standard ceMRA in demonstrating fine vascular details.33 Enhanced T1-weighted breath-held gradient-echo fat-saturated sequences are an important component of our mesenteric MRA protocol. They are particularly beneficial for the assessment of arterial and venous thrombi and emboli.34
Figure 1 A 87-year-old man with a history of atrial fibrillation presents with sudden onset of severe abdominal pain. He developed abdominal distention and underwent CTA. Sagittal MPR shows abrupt occlusion of the SMA approximately 3 cm distal to its origin (arrow) (A). A coronal MPR shows the length of the embolus (B). A 2-chamber long-axis reconstruction of the heart demonstrates residual thrombus (arrow) in the left atrial appendage, the source of the embolus (C). MPR, multiplanar reformation.
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Acute Mesenteric Ischemia Acute interruption of the blood supply to the small bowel or colon or both is a catastrophic event, with a morbidity and mortality exceeding 60%.35 The 4 major causes of
acute mesenteric ischemia are SMA embolus, SMA thrombosis, mesenteric venous thrombosis, and nonocclusive mesenteric ischemia (NOMI).35 Aortic dissections have also been reported to cause acute mesenteric ischemia (AMI) on rare occasions.4
Figure 2 A 76-year-old woman develops acute abdominal pain following surgical repair of a juxtrarenal abdominal aortic aneurysm with a tube graft complicated by occlusion of the inferior mesenteric artery. CTA was performed emergently. A volume-rendered image shows the aortic tube graft as well as patent celiac trunk and superior mesenteric arteries (A). A coronal arterial phase CTA MPR shows an occluded inferior mesenteric artery (arrow) as well as lack of enhancement and stranding surrounding the descending colon (arrowheads) (B). An oblique portal venous phase MPR demonstrates the transition between normally enhancing large bowel and the nonenhancing necrotic bowel (arrowheads) (C). Lung windows show pneumatosis of the left colon (arrowheads) (D). MPR, multiplanar reformation. (Color version of figure is available online.)
CTA and MRA imaging of the mesenteric vasculature
Figure 3 A 75-year-old woman with CMI undergoes CTA. Sagittal thin-slab MIP of the arterial phase shows severe tandem ostial stenosis of the celiac trunk (arrowheads) and an occlusion of the SMA (arrow) (A). Coronal MIP shows the enlarged arc of Riolan that provides collateral flow from the IMA to the SMA territory (B). A volumerendered image shows the enlarged IMA (arrow), as well as the arc of Riolan (arrowheads) (C). MIP, maximum intensity projection. (Color version of figure is available online.)
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6 Acute emboli to the SMA account for approximately 40%-50% of all episodes of AMI,35 with the typical patient having a history of cardiovascular disease (Fig. 1). Most emboli in the SMA lodge just beyond the origin of the middle colic artery. Acute mesenteric arterial thrombosis is usually associated with a pre-existing atherosclerotic lesion and consequently a history of intestinal angina is present in up to 50% of cases.35 In contrast to the abrupt catastrophic onset of symptoms associated with an embolus to the SMA, the abdominal pain and symptoms associated with acute mesenteric arterial thrombosis may be more insidious owing to the development of collateral circulation. Thrombotic occlusion of the SMA occurs typically near the ostium, unlike embolic occlusion.35,36 CTA demonstrates calcified and noncalcified ostial plaques, thrombus, as well as collateral vessel.4 Occasionally, acute thrombosis complicates abdominal vascular surgical procedures (Fig. 2). Mesenteric venous thrombosis is rare and can be related to hypercoagulation, infection, portal hypertension, trauma, or malignancy among other causes. It does not typically cause severe bowel ischemia. Nonocclusive mesenteric ischemia (NOMI) is thought to be responsible for approximately 25% of cases of AMI, with a mortality rate as high as 70%.4 NOMI usually develops during an episode of cardiogenic shock or a state of hypoperfusion in which excessive sympathetic activity results in secondary splanchnic vasoconstriction. The response to intraarterial papaverine during DSA is both diagnostic and therapeutic, but the diagnosis can occasionally be made with CTA if there is lack of mesenteric venous enhancement on the portal phase scan in conjunction attenuated SMA branches.37 Approximately 5% of patients with aortic dissection develop mesenteric ischemia as a complication
of the dissection process.35 Isolated dissections of the SMA, either in association with cystic degeneration or as a complication of catheter angiography, are extremely rare but readily diagnosed on CTA. In acute cases, perivascular stranding is typical in isolated SMA dissections.4 Besides assessment of the mesenteric vessels, MDCTA permits the evaluation of secondary signs of bowel ischemia such as bowel dilatation, bowel wall thickening or thinning, edema, submucosal hemorrhage, abnormal wall contrast enhancement (either absent or decreased enhancement, or hyperenhancement), and pneumatosis intestinalis, as well as portomesenteric venous gas, mesenteric fat stranding, ascites, and pneumoperitoneum. In addition, it can provide alternative diagnoses in these patients. A recent study of 91 patients with suspected AMI resulted in the diagnosis of mesenteric ischemia in 18 patients, 14 of whom were of the thromboembolic type and 4 of the nonocclusive type. Positive CTA findings were confirmed by surgery in 13 patients and by clinical followup in 3 cases. Other etiologies for abdominal pain in this cohort were diagnosed by CT in 38 patients out of the remaining 74. There were 2 false-positive and 2 falsenegative CT results, with an overall accuracy of 95.6%. The authors concluded that MDCTA is a fast and accurate investigation for the diagnosis of acute mesenteric ischemia and in most cases can be used as the sole diagnostic procedure.38 The American College of Radiology recently published Appropriateness Criteria for Imaging of Mesenteric Ischemia,39 a document evaluating and rating the appropriateness of imaging to evaluate patients with clinically suspected mesenteric ischemia. The document stated
Figure 4 A 66-year-old man with typical symptoms for CMI. Sagittal thin-slab MIP of a ceMRA demonstrates highgrade ostial stenoses of the celiac trunk, SMA, and IMA (arrows) (A). An axial T1-weighted fat-suppressed 3D breath-hold image using the VIBE sequence demonstrates normal thickness and enhancement of both small and large bowel (B). MIP, maximum intensity projection; VIBE, volumetric interpolated breath-hold examination.
CTA and MRA imaging of the mesenteric vasculature “while catheter-based angiography has been considered the reference standard and enables diagnosis and treatment, advances in computed tomography have made it a first-line test in many patients because it is a fast, widely available, and noninvasive study.” MRA received a less favorable review because although providing “high sensitivity and
7 specificity for diagnosing severe stenosis or occlusion at the origins of the celiac axis and SMA, 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 not readily available in most practices.”39
Figure 5 A 76-year-old woman with chronic abdominal pain undergoes ceMRA for surveillance for an infrarenal abdominal aortic aneurysm. Sagittal MIP demonstrated a moderate to severe stenosis of the celiac trunk and a patent SMA (A). A coronal MIP showed the AAA (asterisk) as well as the main collateral pathway via the pancreaticoduodenal arcades (arrows) with several aneurysms (arrowheads) (B). A CTA performed a few weeks later for planning of an endovascular aneurysm repair shows a severe ostial stenosis of the celiac trunk (arrow) (C) as well as the aneurysms (D). Note the significantly higher spatial resolution of the CTA scan. AAA, abdominal aortic aneurysm; MIP, maximum intensity projection. (Color version of figure is available online.)
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Chronic Mesenteric Ischemia Chronic mesenteric ischemia (CMI) is almost always caused by severe atherosclerotic disease and characterized by a classical clinical triad of postprandial abdominal pain, weight loss, and food avoidance.35 Both CTA and MRA are suitable for the assessment of patients with suspected CMI4 (Figs. 3-5). Although atherosclerosis of the mesenteric circulation is frequent in the elderly, CMI is relatively uncommon, primarily owing to abundant mesenteric collateral circulation (Fig. 3). Knowledge of collateral pathways between the mesenteric arteries is of utmost importance for the correct interpretation of the imaging studies. More than 50 collateral pathways in the large and small bowel have been described.40 The marginal artery of Drummond is situated along the mesenteric border of the colon and formed by the anastomotic continuation between the right, middle, and left colic arteries. The arc of Riolan is situated more centrally within the mesentery and is an inconstant anastomosis between the middle and left colonic arteries (Fig. 3). The meandering artery is also situated within the mesentery and is a very large tortuous vessel communicating between the SMA and IMA. It potentially represents an enlarged arc of Riolan. The dominant collateral pathway between the CA and the SMA is via the gastroduodenal artery and the pancreaticoduodenal arcades (Fig. 5). The arc of Buhler is a persistent embryonic artery and a direct
communication between the CA and SMA. The arc of Barkow (greater omental arcade) consists of arteries and veins within the greater omentum that anastomose between the left and right gastroepiploic arteries.41-43 This mesenteric collateral network can make it difficult to estimate the degree of mesenteric vascular stenosis necessary to cause intestinal angina. It is generally accepted that at least 2 of the 3 main vessels have to be affected by stenoocclusive disease to produce clinical symptoms.35 CTA has been used in the evaluation of CMI with an accuracy approaching 95%-100%.1 However, extensive calcification may limit the diagnostic value of CTA. Drawbacks to CTA include the use of iodine-based contrast agents and radiation. ceMRA is an alternative to CTA in the evaluation of patients suspected of having CMI. The sensitivity and specificity of 3D contrast MRA is approximately 95%100%. A limitation of MRI are the current inability to scan patients with pacemakers, the issue of claustrophobia, availability, lengthy examination time, and the inability to assess patients with mesenteric stents. A recent prospective study comparing stenosis grading of the celiac trunk and the SMA using duplex sonography, CTA, and MRA at 1.5 T in 52 patients with DSA as the reference found that CTA provided the best image quality, reached the highest level of agreement and significance in correlation in stenosis grading, and offered the best diagnostic accuracy44 (Fig. 5). A number of nonatherosclerotic vascular pathologies can cause CMI.4 Fibromuscular dysplasia is a rare but
Figure 6 A 80-year-old woman with chronic abdominal pain undergoes CTA. Finding of sagittal MIP in inspiration was read as normal. Note high-grade ostial stenosis of the IMA (arrow) (A). Owing to suspicion for median arcuate ligament syndrome, the patient returned for repeat scan in expiration. This demonstrated moderate narrowing of the SMA (arrowhead) as well as the IMA stenosis (arrow) (B). MIP, maximum intensity projection.
CTA and MRA imaging of the mesenteric vasculature well-recognized cause of CMI. Median arcuate ligament syndrome is caused by extrinsic compression of the celiac trunk or the celiac neural plexus or both by the central tendon of the crura of the diaphragm. The classic finding on a lateral view of the aorta consists of a smooth indentation of the superior aspect of the proximal CA, which is more marked on expiration than on inspiration4 (Fig. 6). Median arcuate ligament compression can occasionally involve the proximal SMA and even renal arteries. CTA or MRA scans should be done in expiration if this entity is suspected. Aortic dissections can cause both acute and chronic mesenteric ischemia.4 Chronic mesenteric ischemia has also been described as one of the many manifestations of vasculitides, especially Takayasu arteritis.4
Visceral Artery Aneurysms Visceral artery aneurysms comprise a rare but clinically important vascular disease entity. Their incidence,
9 etiology, and natural history are not entirely understood, and patients frequently present emergently.45 The prevalence of visceral artery aneurysms in reported autopsy series ranges from 0.01%-10%.45,46 They involve the splenic (60%), hepatic (20%), superior mesenteric (5.5%), celiac (4%), gastric and gastroepiploic (4%), intestinal (jejunal, ileal, and colic; 3%), pancreaticoduodenal and pancreatic (2%), gastroduodenal (1.5%), and inferior mesenteric arteries (rare).45,46 Splenic artery aneurysms are the most common visceral artery aneurysms with the reported incidence in autopsy series ranging from 0.1%-7.1% (Fig. 7). The average age of patients with splenic aneurysms ranges from 48 to greater than 60 years, and they are twice more frequent in women than in men, with 20% being multiple. The reported risk of rupture ranges from 3.0%-9.6% with mortality rates between 10% and 25%.45 The risk is significantly higher in women during pregnancy. The exact mechanism behind
Figure 7 A 55-year-old woman undergoes CTA for abdominal pain. Axial source image shows a 3.5-cm splenic artery aneurysm (arrow) with mural thrombus and wall calcifications (A). The patient was treated with placement of a covered stent (Viabahn, W.L. Gore & Associates, Newark, DE). Spot film immediately following deployment of the stent (arrow) shows contrast trapped in the excluded aneurysm sac (B). This can persist for several days after placement and can simulate an endoleak on postprocedural CT scans. Follow-up CTA was obtained several months following the procedure and showed a patent covered stent (arrows), patent splenic artery and excluded aneurysm (C).
10 aneurysm formation is not clearly understood, and their etiology can be divided into 4 categories: degenerative, inflammatory, posttraumatic, and pregnancy related. In contrast to aneurysms of large vessels, atherosclerosis is not considered to be the primary etiologic factor for splenic aneurysms.46 Patients with portal hypertension and splenomegaly have also been found to have a higher incidence of splenic artery aneurysms.45,46 Inflammatory pseudoaneurysms are almost always associated with pancreatitis and the presence of pseudocysts and always require therapy. Very rarely, pseudoaneurysms are caused by other regional inflammatory diseases such as peptic ulcer disease. Most aneurysms are found incidentally on imaging performed for other causes, with CTA being the most sensitive study in our opinion. MRI or MRA is less sensitive (Fig. 5). The surgical literature recommends repair of splenic artery aneurysms when they are larger than 2 cm or are found to have been enlarged, with a more aggressive approach in pregnant women and women of childbearing age considering pregnancy.46 Hepatic artery aneurysms are the second most frequent visceral aneurysms. Overall, 66% of hepatic aneurysms are extrahepatic. Hepatic artery aneurysms are most frequently the result of penetrating, iatrogenic, or blunt trauma. Mycotic aneurysms can be found in patients with a history of intravenous drug abuse. Rare causes are vasculitides such as polyarteritis nodosa and periarterial inflammation caused by either cholecystitis or pancreatitis. Fibromuscular dysplasia, segmental mediolytic arteriopathy, and connective tissue diseases are other noninflammatory etiologies (Fig. 8). Most patients with hepatic artery aneurysms present with rupture.46 The aneurysms usually
Figure 8 A 69-year-old woman with Ehlers-Danlos syndrome and postprandial epigastric pain. Volume-rendered CTA image shows multiple aneurysms of the superior mesenteric artery (arrowheads) as well as a thrombosed splenic artery aneurysm (arrow). (Color version of figure is available online.)
K.D. Hagspiel et al rupture into the biliary system or the peritoneal cavity, and this is associated with very high mortality. Quincke triad is the classic finding of hepatic aneurysm rupture and consists of epigastric pain, hemobilia, and obstructive jaundice. SMA aneurysms are the third most common visceral aneurysm accounting for 5.5% of these lesions. They almost always involve the proximal 5 cm of the main SMA trunk.45 The SMA is the most common site for infection of a peripheral muscular artery, with mycotic aneurysms comprising 58% of these lesions.46 Of these, most patients are less than 50 years of age, and 63% of reported SMA aneurysms occur in men.45,46 Many patients with aneurysms of the SMA have subacute bacterial endocarditis. Dissecting aneurysms associated with medial defects are rare but affect this vessel more than any other visceral artery. SMA aneurysms require treatment even in asymptomatic patients because spontaneous rupture is frequent and mortality is high. Surgery is the preferred treatment option but can be complicated as inflammation and infection are common features of these aneurysms.
CTA and MRA for Treatment Planning and Following Surgical or Endovascular Therapy MDCTA is the preferred modality to plan therapy for both occlusive and aneurysmal diseases in our institution (Fig. 7). CTA easily allows detection and characterization of stenoses with higher accuracy than ceMRA. Also, calcifications, whose presence can have major effect on the choice of therapeutic procedure, are readily identifiable. The assessment of complex aneurysms with multiple afferent and efferent branches is best done with MDCTA; real-time assessment of the 3D data set using volume rendering on a dedicated workstation allows comprehensive assessment of these lesions and greatly facilitates both surgical treatment and endovascular therapy (Fig. 8). MDCTA is the most useful tool to follow patients after all currently used open or endovascular mesenteric revascularization procedures, including surgical embolectomy, thrombectomy, bypass graft placement, endarterectomy, surgical release of the median arcuate ligament, mechanical thrombectomy, angioplasty, catheter-directed thrombolysis, fenestration of the dissection membrane, stent placement, and endoluminal stent-graft placement.47 MRA is limited in the setting of metallic implants such as stents but has been shown to be equivalent to DSA for the evaluation of visceral artery aneurysms after coil embolization.48 CTA assessment of stent patency can be facilitated by reconstructing the images with a sharp (bone) kernel and a smaller field of view that minimizing the blooming artifact (Fig. 9). A rare immediate complication of successful surgical and endovascular revascularization is the development of reperfusion syndrome, which can lead to liver failure,
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Figure 9 A 69-year-old man who underwent previous placement of stents into the celiac trunk and superior mesenteric arteries for CMI presents with recurrent symptoms. A CTA was performed. Sagittal MPR of arterial phase CTA using the standard soft tissue kernel does not allow assessment of stent patency with certainty (A). Dedicated stent reconstruction using bone kernel, smaller FOV, and 50% overlap clearly demonstrates compression of the celiac stent (arrow) as well as narrowing of the SMA stent. There is also intimal hyperplasia in both stents seen as dark lines (arrowheads) (B). MPR, multiplanar reformation.
ascites, pancreatitis, and food intolerance caused by bowel and visceral organ hyperemia. CTA readily demonstrates hyperemia of the bowel and early filling of the mesenteric veins on arterial phase imaging.45 The assessment of complex aneurysms with multiple afferent and efferent branches is best done with MDCTA; real-time assessment of the 3D data set using volume rendering on a dedicated workstation allows comprehensive assessment of these lesions and greatly facilitates both surgical treatment and endovascular therapy (Fig. 8).
Conclusion Both MDCTA and ceMRA are highly accurate crosssectional vascular imaging modalities for the evaluation of the mesenteric vasculature. Owing to its availability, acquisition speed as well as ability to detect bowel wall abnormalities, MDCTA is the modality of choice for patients presenting with AMI. It is also well suited to follow patients after all endovascular and open surgical procedures for occlusive and aneurysmal mesenteric arterial disease. CeMRA has the advantage of not using ionizing radiation and iodinated contrast agents and can be appropriate in the nonacute setting.
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