Dr. Close is a fellow in vascular and interventional radiology in the Department of Radiology at the University of Michigan Medical Center, Ann Arbor, MI.

Dr. Cho is the William Martel Professor of Radiology in the Department of Radiology at the University of Michigan Medical School, Ann Arbor, MI.

Magnetic resonance angiography (MRA) was first shown to be clinically feasible in 1985. ¹ Since that time, MRA has become useful both from a clinical and a research standpoint in the assessment of the vascular system and its pathologies. MR imaging offers several advantages over computed tomography (CT) and conventional angiography. It is inexpensive relative to invasive angiography and allows cross-sectional imaging without the risks of ionizing radiation, iodinated contrast material, or arterial puncture. ²

MRA facilitates planning for interventions and increases the number of interventions, such as percutaneous transluminal angioplasty (PTA) and stent placement. From an interventional radiologist's standpoint, the initial use of MRA as a screening modality for vascular disease should increase referrals for vascular interventional procedures. By knowing in advance the location and extent of vascular pathology, MRA should help the interventionalist perform procedures more efficiently. Furthermore, a preprocedure MRA allows the diagnostic angiogram to be tailored to a more limited study that reduces the iodinated contrast agent load and the degree of catheter manipulation required.

Technical considerations

At the University of Michigan Medical Center, a 1.5-T superconducting magnet with a body coil and Software Release 8.3 (Signa Horizon LX; GE Medical Systems, Milwaukee, WI) is used for MR angiography (figure 1). The use of postprocessing techniques to improve the image quality of three-dimensional (3D) gadolinium (Gd)-enhanced MR angiography is done on a computer workstation (figure 2).

MR angiography requires several basic pulse sequences for imaging the vascular system and associated lesions. These include T1-weighted spin-echo imaging ("black blood" imaging), time-of-flight (TOF) imaging ("bright blood" imaging), phase-contrast (PC) imaging ("bright blood" imaging) and gadolinium-enhanced 3D MR angiography ("bright blood" imaging). The T1-weighted spin-echo imaging provides the anatomic information for organs and large vessels including the aorta, vena cava, and portal vein. ³ These sequences have limited spatial resolution with complex signal patterns from the varying velocity and turbulence of flowing blood, which may be difficult to interpret (figure 3). ⁴

The "bright blood" techniques, because of their MRA appearance, are especially useful to differentiate slow flow from thrombus, which both appear as high signal on T1- and T2-weighted images. The time-of-flight imaging sequences rely on the inflow of unsaturated blood into the imaging volume, so that the vessel appears brighter than the stationary saturated tissue. ⁴ Postprocessing of two-dimensional (2D) or 3D gradient-echo (GRE) sequences leads to a projective format similar to a conventional angiogram. ¹ Usually, post-processing is performed using a maximum-intensity projection (MIP) algorithm. With MIP, the brightest pixels in a certain direction are used to create the projection image. These MIP projections are then created to visualize vessels in a 3D format. The drawback of TOF imaging is in the evaluation of diseased vessels in which the MR signal is degraded by slow, turbulent, or in-plane flow. Maximum-intensity projection also has its drawbacks, which include evaluation of the edges of blood vessels and small vessels with slow flow. Because these vessels may have slow flow, they have poor flow contrast and may be obscured by overlap with brighter stationary tissue. This can then cause false stenoses.

Phase-contrast imaging is another "bright blood" technique, which is also flow-sensitive. Slow flow is well depicted in this sequence. ¹ It is more sensitive to slow flow than TOF. ³ Phase-contrast imaging can also be used to determine the direction of flow. Blood in the direction of the flow encoding axis is bright, stationary tissue is gray, and flow in the opposite direction is dark. ³

With hemodynamically significant stenosis, spin dephasing (signal dropout) is identified on 3D phase-contrast images (figure 4).

The newest clinically accepted technique is 3D Gd-enhanced MRA. This largely eliminates motion and flow artifacts because it does not depend on blood inflow. By imaging during the infusion of Gd, there is selective visualization of arteries without excessive venous or background tissue enhancement. ⁵ It is considered the state-of-the-art technique for MRI evaluation of the abdominal vasculature. ⁶ Usually, 3D contrast-enhanced MRA uses Gd, which is a paramagnetic contrast agent. Gd-MRA has been shown to be accurate for evaluation of the aorta and its major branches. ³ The principle behind the use of Gd lies in the fact that the contrast agent makes the T1 relaxation time of blood much shorter than the surrounding tissues when Gd is administered rapidly. ³ 3D Gd-enhanced MRA allows extra signal-to-noise ratio over other bright blood techniques such that rapid 3D volume imaging can image entire vascular structures, such as the portal vein, easily in a 30-second breath-hold. Other advantages of this technique include the ability to image other organ parenchyma, such as the kidney and liver. In addition, Gd exhibits no clinically detectable nephrotoxicity and thus may be used safely in cases of renal failure. ⁷ It has a low incidence of allergic reactions ³ and therefore can be used in patients with a history of allergic reaction to iodinated contrast.

The technique of 3D contrast-enhanced MRA consists of imaging in different phases of the bolus. For arterial phase imaging, bolus timing is most critical and may be performed by a variety of methods, including: 1) the operator can inject contrast and then scan 10 to 15 seconds later (the empirical-timing method); 2) the operator can use an automated sequence such as SmartPrep (GE Medical Systems, Milwaukee, WI) (figure 5), Bolustrack (Philips Medical Systems, Shelton, Conn), or Care Bolus (Siemens Medical Systems, Iselin, NJ); and
3) MR fluoroscopy may be used after a test bolus. ³

Patient preparation

The use of an MR system is contraindicated for patients with electrically, magnetically, or mechanically activated implants, such as cardiac pacemakers, because the magnetic and electromagnetic fields produced by the MR system may interfere with the operation of such devices. The magnetic field of the MR system can cause a ferrous implant such as an aneurysm clip, surgical clip, or a cochlear implant to move and be displaced. Therefore, before the MR examination, the procedure should be explained in detail to the patient. The patient must be informed about the potential complications that can occur. In particular, the patient should be screened for any metallic implants. Table 1 presents a patient questionnaire used at our institution that must be completed by the patient or referring physician prior to the study.

A mild sedative is given prior to the examination to relieve anxiety secondary to claustrophobia. The oral dose of 5 or 10 mg diazepam (Valium, Roche Pharmaceuticals, Roche Products, Inc., Puerto Rico) is usually effective when given approximately a half-hour prior to scanning.

Clinical applications of MR angiography

MR angiography should be used in the evaluation of the vascular anatomy and suspected vascular lesions when conventional angiography is contraindicated. Such contraindications include hypersensitivity to iodinated contrast material and renal insufficiency (serum creatinine level >2.0 mg/dL). Even in patients without such contraindications, MR angiography is used in the evaluation of the vascular anatomy in a variety of disorders and suspected arterial lesions. Table 2 lists clinical applications for the use of MR angiography.

Thoracic MRA

We have found that MR angiography provides excellent assessment of the thoracic aorta and related lesions, including aneurysm, dissection, aortitis, atherosclerosis, penetrating ulcers, coarctation, and occlusive disease of the great vessels. Pulse sequences include a coronal single-shot fast spin echo (FSE), axial 2D TOF, and 3D contrast MR acquisition in the coronal or sagittal plane.

MR angiography is a very useful diagnostic examination in patients with suspected dissection (figure 6). MR angiography can establish the presence of aortic dissection and define the origin and extent of the dissection. Multiplanar reformations of the 3D data set can help elucidate whether branch vessels originate from the true or false lumen. The true lumen is usually identified by the relative increase in signal intensity caused by the Gd from faster-flowing blood. The true lumen is also usually identified by being smaller and more oval, and by being parallel to the inner curve of the aorta. Patency of the false lumen and entry and re-entry tears can usually be identified. ⁸ However, some physicians still may choose to use helical CT to evaluate aortic dissection because it is faster, more widely available, and particularly useful for imaging unstable patients connected to multiple mechanical devices.

For the evaluation of thoracic aortic aneurysms, the size and extent of the lumen and its relationship to aortic side branches is easily obtained. The 3D quality of the technique allows the data set to be reformatted in any plane.

Postoperatively, 3D contrast MRA is helpful in the evaluation of aortic grafts for the surgical treatment of aneurysm repair. All of these grafts are now MR-compatible. ⁹ The development of aneurysms or stenoses at graft anastomoses is well depicted using the multiplanar reformatting capability of 3D MRA.

After endovascular interventions, such as fenestration and stent-graft placement, MR angiography is useful in assessing the blood flow in the false and true lumen and the status of organ perfusion. In chronic aortic dissection, MR angiography is used to follow the progress of the disease with measurement of the size of the dissection.

We recently examined a patient with multiple penetrating atherosclerotic ulcers of the descending thoracic aorta and a 5-cm aneurysm using 3D contrast MR angiography for back pain. She subsequently underwent percutaneous transfemoral digital subtraction aortography in the left anterior oblique and lateral projections, and intravascular ultrasound (IVUS) as preparation for stent-graft placement. All three images showed penetrating ulcers well (figure 7).

Pulmonary MRA

Pulmonary 3D contrast MR angiography using multiple-bolus infusions can image the pulmonary arterial and venous anatomy (figure 8). Schoenberg et al ⁶ have shown that segmental arteries or veins could reliably be assessed for patency. Others have shown that lobar or segmental arteries were visualized in 100% of cases and subsegmental pulmonary arteries in 81% of cases. ¹⁰ There are many clinical applications, including suspected thromboemboli in the pulmonary veins and preoperative resection of pulmonary arteriovenous malformation or carcinoma.

Radionuclide scanning (V/Q scanning) and spiral CT are usually the initial imaging examinations in patients with suspected pulmonary embolism (PE). Pulmonary angiography continues to be the gold standard for the diagnosis of PE. A recent study from our institution showed that 3D contrast MR angiography is a safe and reliable technique for the detection of PE with a diagnostic accuracy of 75% to 100% sensitivity and 95% to 100% specificity. ¹¹ Presently, the resolution of MRA is not good enough to replace helical CT or contrast angiography in patients suspected of having PE. However, MRA is useful as an alternative imaging technique when the use of iodinated contrast material or radiation is contraindicated.

Abdominal MRA

Prince ⁵ has shown that Gd-enhanced MR abdominal aortography had an 88% sensitivity and a 97% specificity for detection of stenoses or occlusions, as well as a 100% sensitivity and a 100% specificity for detection of aortic or iliac artery aneurysms (figure 9). Abdominal aortic aneurysm dimensions are well evaluated with the MIP images from 3D MRA. The large field of view allows easy visualization of the extent of the aneurysm, especially into the iliac arteries. Assessment in the coronal plane illustrates the relationship to the renal arteries and important venous and renal anomalies. Post-contrast T1-weighted spin-echo or gradient-echo image analysis is crucial in order to assess regions of thrombosis and the aortic wall. For instance, a thick circumferential rind of enhancement of the aortic wall or periaortic tissues may indicate an inflammatory process, such as retroperitoneal fibrosis or an inflammatory aneurysm. All of these findings are taken into consideration with either open surgical repair or the newer endovascular management of abdominal aortic aneurysms using aortic stent-grafts.

Iliac MRA

Before and after an iliac artery intervention, MRA may be used to detect significant (>50%) stenoses and evaluate patency. Percutaneous transluminal angioplasty has been shown to be a widely recognized therapeutic modality for treatment of iliac narrowing or occlusion. ¹² Because the iliac arteries are difficult or impossible to image by color duplex ultrasound, evaluation is performed by other noninvasive vascular laboratory tests, conventional angiography, or MRA. Johnston et al ¹² reported that MRA before PTA of the iliac arteries was 95% sensitive and 97% specific in assessing the site and degree of stenosis and in determining balloon size. Unfortunately, MRA usually cannot be employed as a post-stent imaging modality, as most stents create MR imaging artifacts, precluding adequate evaluation of the lumen. The most MR-compatible stents are composed of nitinol, which is totally nonmagnetic.

Renal MRA

At our institution, our complete imaging sequence to evaluate for renal artery stenosis consists of a T1-weighted spin-echo localizer, a single-shot fast spin-echo localizer, an axial 2D T2-weighted sequence with fat saturation (for characterization of masses), a 3D Gd-enhanced MRA, and a 3D phase-contrast sequence. Postprocessing is performed by the radiologist. ¹³

Applications for MRA of the renovascular system include evaluating the extent of tumor thrombus from renal cell carcinoma in the renal vein and inferior vena cava, and whether it extends to the hepatic vein or above the diaphragm (figure 10). MR imaging has been shown to have 100% sensitivity for detection of tumor thrombus beyond the distal renal vein. ^14,15 The renal vein and inferior vena cava can be evaluated by 3D Gd-enhanced MRA during the venous and equilibrium phases (figure 11). ¹³

Other applications include the evaluation for suspected renal artery stenosis. This clinical scenario affects a small percentage of patients with hypertension. It is usually a manifestation of systemic atherosclerosis with involvement of the cerebral, coronary, and peripheral vessels, but atherosclerotic renal artery stenosis is isolated in 15% to 20% of cases. ¹³ It is important to detect because PTA/stenting or surgical revascularization can reduce the blood pressure. This may also help to reduce the loss of renal parenchyma and subsequent progression to renal failure. The MRA techniques of 2D and 3D TOF and PC imaging have shown benefit in diagnosing renal artery stenosis. ¹ If loss of signal (dephasing) on the 3D PC acquisitions is identified in the region of renal stenosis, the narrowing is considered hemodynamically significant and the dephasing represents turbulent flow (figure 4). Severe spin dephasing usually corresponds to a stenosis of at least 75%. ¹³ Atherosclerotic narrowing is usually present in the aorta and typically narrows the ostium or the proximal 1 to 2 cm of the renal arteries. Atherosclerosis is rarely isolated to the distal renal artery or its branches. Other findings associated with a hemodynamically significant stenosis include poststenotic dilatation as well as functional changes in the renal parenchyma, such as loss of corticomedullary differentiation and reduction in parenchymal thickness, delayed renal enhancement, and asymmetric concentration of Gd in the collecting systems. At our institution, patients with suspected renal artery stenosis are referred to MRA. In most instances, all the necessary vascular information is obtained by MRA, and therefore a "tailored" angiogram is performed with either carbon dioxide or Gd before stenting to reduce the risk of contrast nephropathy (figure 12).

Techniques used to evaluate renal artery stenosis have included TOF, PC, and 3D contrast-enhanced MRA. ¹⁶ 3D tilted optimized nonsaturating excitation (TONE) sequence evaluation of the renal arteries showed a detection of severe stenosis (>= 60%) with a sensitivity of 100% and a specificity of 89%. ¹⁷ MRA performed with a high dose of Gd has been shown in other studies to detect renal artery stenosis with sensitivities and specificities exceeding 90%. ¹³

A current limitation of renal MRA is in the detection of supernumerary renal arteries, ¹⁶ which may occur in an estimated 30% of patients. ¹⁸ These aberrant renal arteries usually arise from the aorta but, rarely, may originate from a common iliac artery. Accessory renal arteries are known to be especially common in patients with a horseshoe kidney. The spatial resolution of the 3D TOF techniques is too low to resolve all accessory arteries, ¹⁷ but this limitation will probably disappear as resolution improves. The literature has shown that MRA has been successful in depicting accessory renal arteries in 86% to 100% of patients with a normal aorta or aortic occlusive disease. ¹⁹ In addition, renal MRA depiction of the distal portions of the renal arteries is a known limitation of the technique. ¹⁶

Fibromuscular dysplasia (FMD) is the second most common cause of renal artery stenosis. It affects medium-sized and small arteries ²⁰ and usually is diagnosed in the renal and carotid arteries. Other less common locations include the subclavian, axillary, mesenteric, hepatic, splenic, and iliac arteries. It is classically found in young (<40 years of age) female patients, usually bilaterally with the medial fibroplasia subtype manifesting as a 'string-of-beads' appearance in the distal two-thirds of the main renal artery, with web-like stenoses interspersed with small fusiform or saccular aneurysms. Since MRA cannot always demonstrate abnormalities in the distal main renal arteries, the accuracy of MRA for diagnosing FMD is not established. ¹³ Therefore, we currently recommend angiography in all patients with suspected FMD because percutaneous renal catheterization is needed for both diagnosis and intervention.

Other applications of renal MRA include planning for renal revascularization or for repair of abdominal aortic aneurysm, assessing renal bypass grafts (including anastomoses to renal transplants), and evaluating renal malignancy and its relationship to vascular structures.

Mesenteric MRA

3D contrast MR angiography has sufficient resolution to evaluate the origins of the splanchnic vessels. Because reformations may be made from the 3D data set, visceral anatomy may be evaluated, even if it is complex in nature. MRA of the mesenteric circulation is usually only applied to questions of chronic mesenteric ischemia (figure 13), as acute mesenteric ischemia is usually considered a surgical emergency. Other clinical applications include the evaluation of visceral artery aneurysms, tumor encasement, and pre- and post-liver transplantation.

The MR evaluation of chronic mesenteric ischemia usually consists of a data set that is collected before, during, and after the administration of intravenous Gd. The images obtained during the administration of intravenous Gd are excellent for evaluating the proximal portions of the celiac axis, the superior mesenteric artery, and the inferior mesenteric artery, as well as their branches. The delayed data set can be used to evaluate patency of the portal vein and hepatic veins. In order to evaluate for more distal, segmental occlusions, the small and large bowel should be evaluated for the normal enhancement characteristics following intravenous Gd.

Early diagnosis of mesenteric ischemia is important because surgical revascularization or PTA and/or stenting offers an excellent treatment option. Contrast-enhanced 3D MRA can clearly evaluate for stenosis of the celiac trunk and the superior mesenteric artery, with sensitivities of 100% and specificities of 92% to 95%. ⁹

Hepatic/portal MRA

MRA of the portal vein is complicated by the fact that flow may not uncommonly be multidirectional. As a result of this complexity, sequences must image in both coronal and axial planes. ³ For Gd-MRA of the portal vein, the operator must give a triple dose of Gd (0.3 mmol/kg) because of dilution and extraction of contrast that occurs en route to the portal circulation, at 2 cc/sec. Phase-contrast MRA can determine the direction of portal venous blood flow. Advantages over the sonographic evaluation of the portal vein include its large field of view. ¹

MRA applications to the hepatic/ portal venous system include the pre-liver transplant patient. It is crucial to know in advance of a liver transplant if there is celiac stenosis, as this can lead to transplant ischemia. MRA is also useful in planning the liver transplant surgery and in excluding certain patients from the transplant list, such as those with portal venous thrombosis. ³ Before placing a patient on the liver transplant list, it is necessary to demonstrate a patent portal vein. If ultrasound is unable to adequately visualize the portal vein, 3D contrast MRA is an excellent option.

MRA is also useful after a liver transplant. In this case, the surgeon or interventionalist is frequently searching for the not-uncommon complication of hepatic artery stenosis. The classic workup initially consists of ultrasound. This is frequently followed by MRA, since MRA can easily visualize hepatic artery thrombosis, portal vein stenosis or thrombosis, or IVC stenosis. ³ Gd-MRA can depict these accurately, with accuracy equivalent to a conventional angiogram. ³ Infarct, abscess, or biloma are also within the differential of the failing transplant and can be seen with the source images of the MR angiogram.

Other applications of MRA in the liver include the pre-TIPS (transjugular intrahepatic portosystemic shunt) evaluation in order to determine the patency of the hepatic veins and the portal vein (figure 14). MR angiography can identify spontaneous splenorenal shunts as well as assess the degree of varix formation.

MR angiography has an advantage over ultrasound in the evaluation of surgical shunts, especially in evaluation of the distal splenorenal shunt, because bowel gas tends to obscure sonographic evaluation.

Tumor encasement with narrowing of the splenic vein, superior mesenteric vein, or portal vein from pancreatic carcinoma has been assessed with MRA. This type of vascular narrowing has been caused by cholangiocarcinoma as well. However, abnormalities of the mesenteric veins are nonspecific, because they can also be caused by inflammatory etiologies. ³

Hepatic vein occlusion/Budd-Chiari Syndrome is well evaluated by MRA, usually by TOF and GRE sequences. ³ Budd-Chiari Syndrome is characterized by heterogeneous enhancement of the liver with a feathery appearance to hepatic veins (figure 14).

Peripheral MRA

Conventional contrast-enhanced arteriography has been the standard method of evaluating the peripheral vascular system before interventional therapy. However, this method of imaging is associated with certain risks, such as contrast reaction in almost 5% of patients, ²¹ as well as other minor and major complications well known to interventionalists. Additionally, conventional arteriography may not demonstrate suitable target vessels for surgical bypass in up to 70% of patients with severe peripheral vascular occlusive disease. ²² In such cases, MRA of the lower legs can be performed and occasionally will demonstrate suitable target vessels for bypass surgery. This scenerio in which vessels are identified by MRA, but not by conventional arteriography, occurs most often in the infrapopliteal arteries. ²²

Dynamic contrast-enhanced MR angiography has been shown to have 100% sensitivity and 69% specificity for distinction of vessels in the lower extremities with >50% stenosis from normal or mildly stenotic vessels. ²³ In this study, results were evaluated both above and below the knee, demonstrating the diagnostic potential for infrapopliteal diagnosis. The authors did acknowledge, however, that results were somewhat better above than below the knee, possibly due to a larger vessel size and higher intravascular signal above the knee. A serious limitation of MRA is in the assessment of vascular bypass grafts with adjacent surgical clips. This may lead to clip artifacts that can obscure clinically important underlying disease. In a 1993 study, Owen ²² concluded, "two-dimensional TOF MR angiography is an excellent technique for evaluation of patients with peripheral vascular disease." Their group concluded that it is a viable alternative to conventional arteriography for the preoperative assessment of peripheral vascular occlusive disease.

Now that 3D contrast MRA has been developed, this can augment 2D TOF techniques in certain areas. The advantages of 3D contrast MRA over 2D TOF methods include more accurate determination of the length of an occluded segment and better evaluation of the pelvic arterial system (due to 3D-contrast MRA being flow-insensitive) (figure 15). ⁹ One of the disadvantages of MRA is the fact that MRA tends to exaggerate stenoses in the peripheral vascular system. ¹

Conclusion

MR angiography has had exponential growth in recent years and has changed the workup of vascular disease. It is commonly used for the preoperative evaluation of a variety of disorders and for follow-up studies after surgical or endovascular interventions. Because of the safety of gadolinium contrast and the lack of ionizing radiation, MRA will be used increasingly as a screening modality. *