Review

Correspondence *Division of Cardiovascular Medicine, The Ohio State University, 244 Davis Heart & Lung Research Institute, 473 West 12th Avenue, Columbus, OH 43210, USA

Email sanjay.rajagopalan@osumc.edu

Introduction

Peripheral arterial disease (PAD) is a frequent manifestation of systemic atherosclerosis. The prevalence of PAD can be as high as 30% among individuals of advanced age with diabetes mellitus and a history of smoking.^{1, 2} PAD can be asymptomatic and clinical presentation can range from intermittent claudication to, in severe cases, critical limb ischemia. The occurrence of limb-threatening ischemia in individuals with PAD is, however, overshadowed by the risk for recurrent cardiovascular events, including myocardial infarction, ischemic stroke and cardiac death.^{3, 4} As a consequence, the prevention of adverse vascular events and the improvement of limb function and quality of life are the cornerstones of PAD therapy.

The initial diagnostic approach for the evaluation of PAD includes the accurate assessment of patient history and a physical examination in conjunction with ankle–brachial index (ABI) measurement (gained by dividing the ankle pressure by the arm pressure as obtained by Doppler interrogation; values <0.9 identify patients with PAD). In the clinical setting, ABI is an ideal initial screening approach for PAD because of its simplicity and high predictive accuracy.⁵ Diagnostic modalities performed subsequently, such as evaluation of segmental pressures and waveforms (derived by placing blood-pressure cuffs at multiple locations in the lower extremities and measuring the pressure and waveform changes), can then help broadly localize the disease and direct therapy in the majority of patients.⁶ Additional imaging-based assesment is almost always needed in patients requiring revascularization—whether percutaneous or surgical—in patients presenting with atypical symptoms, or in those with typical symptoms but discordant vascular results (e.g. an ABI >0.9) and/or involvement of contiguous vascular beds (e.g. aortic aneurysm, aortic dissection, renal artery stenosis). In these patients and in those in whom an overall vascular evaluation is required, magnetic resonance angiography (MRA) or CT angiography can be considered.^{7, 8} MRA combines high versatility and accuracy with a favorable overall safety profile for the evaluation of patients with PAD.

This Review provides a broad overview of current MRA methodologies and ongoing technical improvements as they apply to the evaluation of lower extremity vessels. The role of MRA in the management of patients with PAD and the performance of this technique in comparison with other diagnostic modalities will also be discussed. We have provided explanations of key terms in Box 1.

MRA for the evaluation of peripheral vessels

The various techniques used for MRA evaluation are described. Magnetic resonance scanners with adequate magnetic field strength (at least 1.5 Tesla), high performance gradients, and dedicated phased-array surface coils are typically used for image acquisition in peripheral MRA.

Vessel wall ('black-blood') imaging

Magnetic resonance techniques for vascular imaging can be broadly classified as 'black-blood' or 'bright-blood' modalities on the basis of the appearance of the vascular lumen in resultant images. Black-blood MRA relies on sequences in which signal produced by flowing blood is intentionally suppressed (Figure 1). Fast or turbo spin-echo acquisition sequences (Box 1) result in images with complete nulling of intraluminal signal and excellent delineation of the vessel wall, especially when combined with electrocardiographic gating and appropriate preparatory pulses (Box 1).^{9, 10} Studies conducted in patients with atherosclerotic involvement of the carotid arteries or the aorta have demonstrated that adequate plaque characterization can be obtained by evaluating signal intensity and morphologic appearance of plaque components in T1-weighted, proton density-weighted or T2-weighted magnetic resonance images (Box 1).^{11, 12, 13} Only a few studies, however, have evaluated the value of dark-blood imaging in patients with PAD and these studies have focused on the study of postangioplasty remodeling in peripheral vessels.^{14, 15, 16, 17} Although this application might prove to be an important use of MRA imaging for PAD, plaque characterization sequences are not routinely incorporated in lower extremity studies as they are currently time consuming and have yet to be validated for this vascular territory.

Figure 1 Black-blood imaging of the superficial femoral artery (magnified in the insert) revealing the absence of atherosclerotic disease.

The image was obtained at the level of the mid left thigh by applying an electrocardiographic-gated turbo spin-echo sequence in the axial plane.

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Lumen ('bright-blood') imaging

With bright-blood MRA techniques, a luminogram is obtained by the use of specifically designed magnetic resonance pulse sequences.

3D gradient-echo angiographic pulse sequences

Contrast-enhanced MRA (CE-MRA) is the preferred approach for the imaging of peripheral vessels. Fast spoiled gradient-echo sequences (Box 1), described as turbo fast low angle shot (FLASH), spoiled gradient recalled acquisition in the steady state (SPGR), fast field echo (FFE) or radio-frequency-spoiled Fourier acquired steady state (RF-FAST) depending on the manufacturer, is the workhorse sequence for three-dimensional (3D) CE-MRA.⁷ Individual 3D volumes oriented in the coronal plane are acquired sequentially at multiple points or 'stations' along the patient's body (i.e. abdomen, pelvis, thighs and legs), chasing a gadolinium-based contrast agent as it flows down into the peripheral vessels. Fast spoiled gradient-echo sequences are heavily T1-weighted (Box 1). Gadolinium results in a marked shortening of the T1 relaxation time for blood, enabling delineation of the blood-filled lumen from surrounding structures. Subtraction of the postcontrast images from the precontrast images improves vessel conspicuity. Usually, the large vessels in the aorto-iliac and femoral territories are imaged faster, sacrificing resolution (approximately 1.5 mm³ isotropic voxels) in order to facilitate higher resolution images in the distal stations (1 mm³ voxels or less). The positioning of the 3D volumes is critical and the application of an overlap between contiguous volumes helps to avoid exclusion of vascular territories near the image edges and edge artifacts (Figure 2).

Figure 2 Contrast-enhanced magnetic resonance angiography of the peripheral vasculature.

Localizer images (A) are used to position the three-dimensional volumes accurately. (B) Three-station peripheral contrast-enhanced magnetic resonance angiography. The positioning of the three-dimensional volumes is critical to avoid the exclusion of important vascular territories and to ensure overlap between sequential volumes. The arrow indicates a right common iliac occlusion.

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2D time-of-flight magnetic resonance angiography

Bright-blood images of the peripheral vessels can also be obtained through time-of-flight (TOF) MRA techniques.¹⁸ TOF-MRA also employs a gradient-echo sequence (Box 1), but does not rely on the injection of a contrast agent for the generation of intraluminal contrast. With this technique, the delineation of the vessel lumen from surrounding structures is based on the arrival of fresh protons with the flowing blood in the scanned image section ('flow-related enhancement'). Ideally, a scanning plan perfectly perpendicular to the imaged vessel needs to be selected for an optimum flow-related enhancement. The clinical utility of TOF-MRA is seriously limited by the long duration of image acquisition and a tendency for stenosis overestimation. Two-dimensional (2D) TOF-MRA is currently not used routinely for the evaluation of PAD, but it can be of some help as a back-up modality in patients who cannot receive contrast or in patients with a nondiagnostic CE-MRA study.

MRA of lower-extremity arteries: technical considerations

MRA studies of lower-extremity arteries are currently based on the application of a multistation moving-table technique. With this technique, images are acquired at multiple body levels (stations), as the patient is moved inside the scanner to follow the flow of the contrast bolus in the lower-extremity arteries (Figure 2).

Venous contamination (i.e. contrast opacification of the venous system precluding adequate visualization of arteries) in images obtained at the level of the distal station is an issue, especially in subjects with rapid arteriovenous transit times (such as those with critical limb ischemia). By obtaining time-resolved MRA or dedicated CE-MRA of the distal station in addition to multistation CE-MRA, the procurement of at least one acceptable angiographic data set at the level of the distal calf and pedal vessels is assured. A typical MRA protocol for the imaging of arteries in the lower extremities is, thus, comprised of multiple components conducted in the following sequence: localizer images; dedicated CE-MRA of the calf and pedal vessels; and moving-table CE-MRA (3–4 stations).

In CE-MRA, image data sets are acquired in coronal planes with a large (40–50 cm) field of view (FOV). As the distance between the upper abdominal aorta and the feet is typically more than 100 cm, a single FOV is not sufficient for complete coverage of the peripheral vessels. By moving the scanner table rapidly through the isocenter of the magnet and acquiring 3D data sets at 3–4 overlapping FOVs, it is possible to image the arteries of the entire lower half of the body during a single contrast injection (Figure 3).

Figure 3 Peripheral contrast-enhanced magnetic resonance angiography with moving-table technique.

(A–D) Representation of patient's position in sequential phases during bolus injection and concomitant image acquisition.

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Contrast agents used for MRA are gadolinium chelates. Gadolinium has strong paramagnetic properties and, as mentioned above, markedly reduces the T1 relaxation time (Box 1) of water protons in blood. This effect enables high-quality contrast separation of the vessel from surrounding structures. Commonly used gadolinium chelates are extravascular agents that rapidly extravasate into the interstitial space. Precise timing is, therefore, necessary to obtain images during peak arterial opacification.

Correct timing of image acquisition in relation to contrast injection to ensure adequate arterial opacification while avoiding venous contamination is of critical importance for the procurement of high-quality images, especially at the last station. There are two main techniques used to ensure correct timing: the test-bolus method and the bolus-detection method. With the test-bolus technique, the time taken for a small amount of contrast material (1–2 ml) to travel from the antecubital injection site to the area of interest (typically the abdominal aorta immediately below the renal arteries) is measured using repetitive low-resolution axial images (1 image per second). The time measured is then used to calculate the delay between contrast injection and the actual image acquisition. The bolus-detection technique employs a contrast-detection pulse sequence that recognizes the increase in signal that occurs with the arrival of contrast in the region of interest, and then either automatically or manually triggers the CE-MRA sequence. Neither of these methods is intrinsically superior to the other and the selection is made on the basis of operator preference. Intravascular or 'blood pool' agents are currently under evaluation for MRA applications as in theory their ability to remain in the blood should enable imaging of the vasculature without having to time peak arterial contrast precisely.¹⁹

Strategies to reduce venous contamination

Several different strategies can be used, separately or simultaneously, to prevent or reduce venous contamination in the images obtained at the level of the distal station.

A strategy for resolving venous contamination in the calf vasculature is the use of dedicated high-resolution imaging at the lower leg level, performed before moving-table CE-MRA (so-called 'hybrid technique').²⁰ The use of hybrid imaging techniques that use dedicated calf-station acquisition might provide better delineation of distal bypass targets and change the management of patients with critical limb ischemia.²¹ As an alternative, time-resolved acquisition techniques, such as time-resolved intravascular contrast kinetics (TRICKS) and time-resolved echo-shared angiographic technique (TREAT), can be applied to the study of the distal vessels.^{22, 23} The dynamic visualization of contrast as it arrives in the vessels can provide incremental information on flow dynamics and collateral vessels (Figure 4). Initial attempts to develop a multistation protocol for time-resolved MRA of lower-extremity vessels have been described.²⁴

Figure 4 Dedicated time-resolved contrast-enhanced magnetic resonance angiography of the legs showing progressive contrast opacification of distal circulation during (A) initial, (B) intermediate and (C) late time frames.

Images reveal a one-vessel run-off in the right leg and two-vessel run-off in the left leg.

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The application of mid-thigh blood-pressure cuffs (at a pressure of 50 mmHg) or a venous compression foam block at the level of the popliteal fossa markedly reduces the degree of venous contamination.^{25, 26} Diminution of venous pooling of the agent with consequent higher concentrations of contrast agent in the arterial circulation has been postulated as one mechanism by which cuff occlusion exerts its effects.

In addition, venous contamination at the level of the calf can be minimized by completing imaging of the proximal stations in less than 45–50 s and by using biphasic administration of gadolinium—an initial fast infusion followed by a second infusion performed at a slow rate—which is superior to a single prolonged infusion at constant rate.²⁷ The slower secondary rate approximates the tissue extraction rate, which would theoretically enable selective arterial opacification without venous filling.

MRA in the clinical management of patients with PAD

For patients with known or suspected PAD, the diagnostic approach should be individualized according to the severity of symptoms and the functional status of the patient.²⁸ An algorithm-based approach (Figure 5), although valuable in streamlining practice, might not be applicable in all patients. For example, even mild claudication can indicate the need to proceed with diagnostic imaging, especially if it occurs in an active individual. By contrast, severe symptoms in an elderly individual with an inactive lifestyle could be managed medically without need for imaging.

Figure 5 Suggested diagnostic algorithm in patients with known or suspected peripheral artery disease.

The central role of peripheral MRA for the management of patients with peripheral artery disease is clearly outlined. In infrequent cases of patients with contraindication to MRA (i.e. severe claustrophobia, metallic implants), CTA represents a valuable alternative. Of note, conventional invasive angiography may be justified only as part of a planned percutaneous revascularization. Abbreviations: CTA, CT angiography; MRA, magnetic resonance angiography.

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In general, after completion of clinical history and physical examination, resting ABI and segmental pressures and waveforms should be obtained in all patients presenting with lower extremity arterial symptoms, as these data help in the diagnosis and localization of disease. In most cases, identification of moderate-to-severe iliofemoral disease in symptomatic patients is an indication for early percutaneous revascularization (Figure 6).²⁹ Patients with diffuse atherosclerotic involvement of peripheral vessels, or predominant femoropopliteal or infrapopliteal disease, who have mild-to-moderate symptoms, can be managed medically. In cases where medical therapy has failed, MRA might be indicated to evaluate the possibility for intervention (Figure 7A).

Figure 6 Ilio-femoral arterial disease detected by contrast-enhanced magnetic resonance angiography.

(A) Severe stenosis at the origin of the right superficial femoral artery (arrow) also involving the origin of the profunda femoris artery. (B) Long-segment occlusion of the left superficial femoral artery (arrowhead) and bilateral significant stenosis of the profunda femoris arteries (arrows).

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Figure 7 Multistation contrast-enhanced magnetic resonance angiographies for peripheral vessel disease.

(A) Major stenoses are observed at the origin of the left external iliac artery and in the proximal segment of the right superficial femoral artery (arrows). The latter vessel is occluded distally (arrowhead). A severe bilateral tibio-peroneal disease is visualized, with a one-vessel run-off on the right leg and two-vessel run-off on the left leg. (B) A patient with a peripheral bypass. Bilateral occlusion of the superficial femoral arteries with a patent femoro-distal bypass graft extending in the right leg from the common femoral artery to the dorsalis pedis artery (arrowheads).

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In patients with symptoms of critical limb ischemia, proceeding directly to MR or CT angiography is justified in order to assess the suitability of the patient for surgical or percutaneous treatment options. CE-MRA in critical limb ischemia has been demonstrated to be superior to conventional angiography in identifying bypass targets.²¹

In postsurgical bypass evaluation, MRA is valuable for the assessment of graft position, course and patency (Figure 7B).³⁰ The visualization of bypass grafts by MRA can sometimes be challenging. Firstly, bypass stenoses are often located at anastomotic regions, where clip artifacts can interfere with visualization of the lumen, and secondly, the imaging of venous grafts can be challenging in terms of the appropriate timing of image acquisition for optimum contrast opacification.

Comparison of MRA with other diagnostic approaches in PAD

In comparison with other diagnostic modalities used for the imaging of peripheral vessels, MRA has a number of important advantages, including the absence of ionizing radiation, need for iodinated contrast agents, absence of calcium induced artifacts (as in CT) and dynamic imaging, which support its preferential use in the evaluation of patients with PAD (Table 1).

Table 1 Major advantages and disadvantages of the principal diagnostic modalities employed for clinical imaging of peripheral vessels.

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MRA versus invasive angiography

Conventional digital subtraction angiography still is the historic standard in the assessment of lower extremity arteries. This invasive modality exposes patients to radiation, uses iodinated, potentially nephrotoxic, contrast agents and has a complication rate of approximately 1%. Compared with conventional angiography, multiple studies have shown that CE-MRA has sensitivity and specificity greater than 95% in the detection of significant peripheral stenoses (Table 2). The diagnostic accuracy of CE-MRA is thus at least comparable with and perhaps superior to conventional angiography, when considering that traditional x-ray angiography is somewhat of a flawed standard. The superiority of CE-MRA is evident, especially for imaging the distal vessels around the ankle and in the foot; studies have consistently demonstrated that CE-MRA is able to identify more run-off vessels than conventional invasive angiography in this area.^{21, 31, 32, 33} Hence, in a number of centers in which CE-MRA is available, this modality has replaced invasive angiography as the initial imaging test in PAD evaluation.^{34, 35, 36}

Table 2 Diagnostic accuracy of contrast-enhanced magnetic resonance angiography for the detection of significant stenosis in patients with known or suspected peripheral arterial disease.

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Peripheral vascular imaging as part of whole-body MRA

In whole-body MRA, several contiguous angiographic data sets that span the entire body (4–6 depending on the body size) are collected as part of a single examination. In one approach, a rolling platform is placed on the pre-existing scanner table.45,46 The phased-array coil is anchored to the stationary table and remains fixed, while the patient is moved using a rolling platform, creating an extended longitudinal FOV with the possibility of acquiring up to six stations sequentially. A different approach to whole-body MRA is based on the introduction of a new multiple-channel whole-body system with surface-coil technology—up to 76 coil elements in total, with up to 32 coil elements simultaneously used in the FOV.^{47, 48} These dedicated multielement coils have been designed to avoid coil repositioning during the study, maximizing the advantages of parallel imaging for MRA. At present, the feasibility and diagnostic performance of whole-body MRA has been tested only in limited series of patients (Table 3), but the fast growth in the number of imaging systems with whole-body MRA capability will undoubtedly provide more solid data from larger study populations in the next future.

Table 3 Initial experience with the application of whole-body magnetic resonance angiography.

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Conclusions

MRA is a safe and accurate technique for the diagnosis and characterization of lower-extremity arterial disease. Owing to its ability to provide rapid yet comprehensive information that allows decision making in clinical practice, assessment of lower-extremity arteries in patients with suspected PAD is a class I indication for MRA.⁴⁹ In centers that can perform high-quality MRA examinations, there is no indication for conventional invasive angiography as a routine diagnostic imaging strategy. The evaluation of PAD by MRA will probably evolve to incorporate other techniques for disease characterization (e.g. atherosclerosis imaging) and to allow whole-body MRA approaches.

Acknowledgments

Charles P Vega, University of California, Irvine, CA, is the author of and is solely responsible for the content of the learning objectives, questions and answers of the Medscape-accredited continuing medical education activity associated with this article.

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