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Magnetic resonance angiographic techniques for the diagnosis of arterial disease
Cardiol Clin 20 (2002) 501–512
Magnetic resonance angiographic techniques for the diagnosis of arterial disease Sanjay Rajagopalan, MD*, Martin Prince, MD, PhD Division of Cardiology, Section of Vascular Medicine, University of Michigan, L311 Women’s Hospital, 1500 E. Medical Center Drive, Ann Arbor, MI 48107, USA
Magnetic resonance angiography (MRA) techniques use inherent magnetization properties of tissues in combination with pharmacologic contrast agents, such as gadolinium, that shorten T1 relaxation time. The availability of powerful magnetic field gradients along with a variety of post-processing algorithms make MRA possible. MRA is widely used for the diagnosis of disease in a variety of vessels, including aorta, carotids, renals, mesenteric, and peripheral vessels. Performance of high-quality 3D contrast MRA requires appropriate understanding of MR methodologies, including the critical dependence of bolus timing and ways to optimize it. Additionally, recognition of artifacts and learning to avoid them is important. Fundamentals of magnetic resonance physics The magnetic resonance (MR) techniques in use are dependent on signals from hydrogen atoms (protons). The abundance of the hydrogen atoms in the human body and the large magnetic moment created by the single proton in the nucleus of the atom make hydrogen atoms extremely sensitive to MR. Resonance is referred to as the property of an atom to absorb energy only at a certain frequency (x), called the Larmor frequency, where x ¼ dB0 (where d represents a constant called the gyromagnetic ratio, and B represents the magnetic field strength). An atom absorbs external energy only if that energy is delivered at the resonant frequency x. * Corresponding author. E-mail address: [email protected] (S. Rajagopalan).
When a patient is placed in the MR scanner, a small fraction of hydrogen nuclei align with the main magnetic field (B0), creating a net magnetization vector. The time required for this to occur is known as T1. The net magnetization vector is aligned with the B0. In MR imaging, energy in the radiofrequency (RF) range is used to deflect the net magnetization vector from the longitudinal to the transverse plane (transverse magnetization) (Fig. 1). The angle of net magnetization-deflection created after the end of the RF pulse is referred to as the flip angle. The stronger the RF energy applied to the protons, the greater the angle of deflection for the magnetization. Common flip angles in MR are 90 and 180. A 90 pulse flips the magnetization into the x-y plane. A 180 pulse flips the magnetization through the x-y plane and into the opposite direction of B0. After the RF pulse tip spins out of alignment with B0, new protons begin to align with B0 at a characteristic rate, T1. When spins are tipped into the transverse plane (created with a 90 flip angle) and a receiver coil or antenna is nearby, an oscillating voltage is induced within the receiver coil. The magnitude of the signal oscillation is dependent on the magnetization in the transverse plane. As the transverse magnetization starts to decay due to the loss of phase coherence, the protons eventually realign with B0. This signal, or ‘‘echo,’’ produced by the decay of transverse magnetization is called free induction decay. The MRI amplitude signal becomes smaller over time at a rate known as T2. Transverse relaxation is the return of transverse magnetization to equilibrium and is termed T2 decay. Simultaneously, the longitudinal magnetization begins to recover and return to a state
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Fig. 1. The effect of RF pulse at Larmor frequency (x) on longitudinal magnetization (M0). Once the net M0 is tipped away from the B0 direction into the transverse place (Mxy), it proceeds. The precession of the magnetic field induces a current via Faraday’s Law of Induction by a conductor nearby (surface coil).
of equilibrium. Longitudinal relaxation is the return of longitudinal magnetization to equilibrium (B0) and is termed T1 recovery. Longitudinal and transverse magnetizations occur simultaneously but are two different processes that inherit properties of various tissues in the body. For instance, fat has a very short T1 and T2 recovery time, whereas water and CSF have some of the longest T1 and T2 recovery times. One way to distinguish between various tissues is to take advantage of these differences in T2 decay and T1 recovery to form T1 and T2 weighted images. In addition to the transverse decay of the macroscopic magnetization caused by T2 relaxation, there are other ‘‘dephasing’’ mechanisms, including field and tissue inhomogeneity, that result in rapid loss of transverse magnetization (T2* effects). In spin echo imaging, this dephasing is refocused with a 180 RF pulse. In gradient echo imaging (see below), where this 180 pulse is omitted, the T2* free induction decay is observed. The reader is referred to more detailed reviews on the mechanisms of MR contrast [1].
Magnetic field gradients, Fourier transforms, and fast MRI techniques Field gradients are what make MRI possible by allowing the signal to be localized in space. The gradients are applied in three planes as slice select (Gss), phase encode, and frequency (read-out) gradients, which spread out the proton resonance in a specific fashion. Unlike back projection reconstruction used in CT, whereby one-dimensional radial projections are sampled, MR uses Fourier reconstruction methods. Many RF pulses are
delivered, and for each RF pulse, an echo is collected. The time between successive echoes is referred to as repetition time (TR), and the time between RF pulse and echo is referred to as echo time (TE). The echoes are then digitized and stored in a data acquisition matrix. This data matrix is referred to as k-space. Two-dimensional Fourier transform (2D-FT) uses the same slice select and readout gradients for each pulse while the phaseencoding gradient is stepped through many different steps from very high to very low amplitude (and to very high amplitude again). The lowamplitude gradient acquisitions sample low spatial frequency k-space data, whereas the pulses during high-amplitude phase-encoding gradient sample high spatial frequency k-space data. A variety of techniques can be used to reduce the time to obtain images to facilitate fast MRI with a single breath hold. Scan time in 2D-FT techniques ¼ TRnNEX (where n ¼ number of phase encode steps, and NEX ¼ number of excitations). For three-dimensional acquisitions, the phase encoding occurs along two axis, ny and nz, which requires additional time. The techniques that can be used to speed up scanning include (i) reducing TR, (ii) reducing the number of phase encode steps, (iii) reducing NEX, (iv) partial Fourier methods that involve acquiring part of the data and using techniques such as conjugate data synthesis and zero filling or padding to make up the remaining data, and (v) parallel imaging. Tissue contrast is principally determined by the center of k-space (central phase encoding lines) while the periphery encodes image detail. MR data are acquired so that contrast and detail are incorporated. The order in which k-space lines are collected can be varied and strongly influences
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tissue contrast. In conventional MRI, the k-space acquisition is sequential, whereas in fast MRI, techniques for 3D contrast angiography, centric, or elliptic-centric acquisition is often used.
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gadolinium chelates with the highest relaxivity and by having a high gadolinium concentration in the blood. Dosage of gadolinium used in MRA
Gadolinium-based MRA Paramagnetic contrast agents Gadolinium is an element in the transition group IIIb of the periodic table. It has eight unpaired electrons in its outer shell, which confers its paramagnetic effect. Gadolinium by itself can cause heavy metal poisoning but when bound to a chelator is safe for intravenous injection. Gadolinium shortens T1 of blood in the region of the gadolinium molecule according to the following equation [2]: 1/T1 ¼ 1/1200þ(R1[Gd]), where R1 is the T1 relaxivity of the gadolinium chelate, [Gd] is the gadolinium concentration in the blood, and 1200 is the blood T1 (in milliseconds) without gadolinium. The blood [Gd] must be greater than 1.0 mmol/L for T1 to be less than 270 milliseconds, which is the T1 of fat at 1.5 T (Fig. 2). This is the property that is important for increasing the MR signal intensity of blood on contrast-enhanced spoiled gradient echo (SPGR) images (see below). This T1 shortening effect is maximized by using
Fig. 2. Blood T1 plotted against Gadolinium concentration [Gd]. A [Gd] of [2 in the blood translates into a T1 of 100, which is well below that of fat. Assuming a resting cardiac output of 5 L/min, achieving this T1 requires an injection rate of at least 0.2 mL/s (12 mL/min). This injection rate sustained over a 3-minute scan duration translates into a minimum gadolinium dose of 36 mL.
To make blood bright compared with all background tissues, it is necessary to give a sufficient dosage of gadolinium at a sufficient rate of injection. Generally, two bottles (20 mL each) of the gadolinium contrast agent (about 0.3 mmol/kg gadolinium) is sufficient for an average person when imaging in the equilibrium phase. However, arteries are best imaged during the arterial phase of gadolinium infusion to take advantage of the higher arterial signal-to-noise ratio (SNR) and to eliminate overlapping venous enhancement. It may seem that an extremely fast acquisition is essential to capture the contrast agent bolus during the brief moment that the agent is present in the arteries but not yet in the veins. However, three important effects make it possible for a relatively slower MR acquisition to capture an arterialphase image without having to use large amounts of gadolinium: 1. Phase reordering (mapping of k-space): To obtain an arterial-phase image in which arteries are bright and veins are dark, it is essential that the central k-space data (ie, the low spatial frequency data) are acquired while the gadolinium concentration in the arteries is high but relatively lower in the veins. This technique allows a relatively long MR acquisition to achieve the image contrast associated with a brief window of time. That brief window of time is the instant when central k-space data are acquired. Therefore, it is critical to time the bolus for maximum arterial [Gd] during acquisition of central k-space data. With perfect bolus timing, high signalto-noise arterial-phase images are possible with small doses of gadolinium. 2. Extraction of gadolinium by the capillary bed: This extraction results in venous blood tending to have a lower concentration of gadolinium relative to arterial blood, even for relatively long, sustained infusions lasting several minutes. This effect is not present in the cerebrovascular circulation because of the blood-brain barrier. Consequently, arterialphase imaging in the central nervous system is more difficult. 3. Infusion rate of gadolinium: Arterial [Gd] is maximized by relaxing the patient to reduce
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cardiac output and by using a high infusion rate. However, fast infusion rates lasting for at least half of the acquisition time require large doses of gadolinium. The dose can be kept to a reasonable level by scanning rapidly. Fast acquisitions (\45 seconds) are possible with high-performance gradient systems that allow short repetition and echo times without requiring a wide bandwidth. Fast acquisition has the additional benefit of making it possible for the cooperative patient to suspend breathing and to hold perfectly still. Spoiled gradient echo imaging (FLASH or SPGR) Gradient echo sequences are used for 3D contrast MR angiography (MRA) because of their speed and short echo times, which allow breathholding and ensure patient through-put. Spoiling helps by suppressing background signal and thereby enhances the signal from the contrast agent in the vasculature. Additional background signal suppression can be achieved with fat saturation pulses, but this incurs additional time. Unlike conventional angiography, the quality of MRA improves when it is performed rapidly. Although faster scanning is associated with a reduction in SNR related to diminished signal averaging, there is an increase in signal intensity associated with shorter T1 associated with injecting the same dose of contrast more rapidly with faster scans. Shortening the TR fourfold reduces the scan time by fourfold and allows a reduction in contrast bolus duration. However, this apparent decrease in contrast dose is offset by requiring an approximately fourfold increase in the injection rate to recover the same amount of longitudinal magnetization in between pulses. Thus, there is no net effect on the contrast dose if the signal-to-noise ratio is to remain unchanged for faster scans. The shorter TR, however, leads to better background suppression and thereby enhances contrast-to-noise ratio (CNR). Because image quality in contrast MRA is dependent on SNR and CNR, shorter imaging times due to shorter TR result in improved vessel visibility. Parameters for an optimal MRA examination Time to echo Time to echo (TE) timing for MRA is usually between 1 and 3 milliseconds. TE is chosen to minimize the dephasing effects (T2*) and to maximize
differences between fat and water (chemical shift artifact). Repetition time Repetition time (TR) timing is kept to the minimum to reduce overall scanning time. Manufacturers have designed special gradient echo (GRE) sequences that are ultrafast (UFGRE) and permit the shortest possible TR, which facilitates the completion of the entire study with a single breath-hold. Flip angle MRA is not dependent to a large extent on flip angle settings. Any angle in the range of 20 to 60 is appropriate. As TR decreases, the flip angle should be shortened. For a TR ¼ 2, a flip angle of 20 is appropriate. Bandwidth Adjusting bandwidth is a powerful way to manipulate SNR, TR, and TE. Increasing bandwidth reduces SNR and decreases TR and TE. Therefore, the bandwidth represents a compromise between a setting that provides for the least scan time versus one that provides for maximal SNR. Typically, we use 32 kHz for gadolinium MRA. Post-processing of MR data Substantial improvement in image quality, and especially image contrast, can be attained through post-processing techniques. Zero padding Apparent image resolution on reconstructions, such as maximum intensity projection (MIP) images, can be increased with interpolation schemes such as zero filling. This method involves filling out peripheral lines of k-space data with zeroes before performing the Fourier transform. No additional time is required for data collection, and the Fourier transform reconstructs more images with a smaller spacing. For example, with twofold zero padding, if the partition thickness is 3 mm, the Fourier transform reconstructs additional images that also have a 3-mm slice thickness but at 1.5-mm spacing with 50% overlap. This helps eliminate volume averaging and creates smooth visualization of small vessels on the reformatted MIP images. Twofold zero padding in the slice direction is recommended. MR digital subtraction angiography Image contrast can be improved by digital subtraction of pre-contrast image data from dynamic-,
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arterial-, or venous-phase image data. This subtraction can be performed slice-by-slice or before the Fourier transform by using a complex subtraction method. The improvement in contrast achieved with digital subtraction angiography (DSA) may reduce the gadolinium dosage required. However, there must be no change in the patient position between the pre-contrast and dynamic contrast-enhanced imaging. This requirement for no motion is easily met in the pelvis and legs, which can be sandbagged and strapped down. It is more difficult to achieve in the chest and abdomen, where respiratory, cardiac, and peristaltic motions are more difficult to avoid. The scanner generally performs complex subtraction automatically before creating any of the images. Another benefit of the subtraction is that it can be performed on the upslope or downslope of contrast enhancement. This may result in selective visualization of arteries and veins, respectively. Multiplanar reconstructions and MIP images Multiplanar 3D reformations are useful in assessing spatial relationships of vessels and to avoid vessel overlap. MIP images are produced by ray-tracing algorithms. The maximum intensity encountered along any predefined direction is assigned to the designated pixel. The advantage of MIP images is the similarity to conventional angiographic images that most vascular physicians are used to interpreting. Can stents be visualized with 3D contrast MRA? Stent-related artifacts associated with vascular endoprosthesis could arise from the metal in the stent and the geometry of the stent. This is a problem when imaging some of the older stents that are made from stainless steel or cobalt-based alloys (eg, the Palmaz and the Wallstent), which result in large signal voids in the stent region. With Nitinol or platinum stents, the artifacts are minor, with the stent frame filaments appearing as a signal void, enabling one to assess stent structure and rule out significant stenosis ([50%). Improved visualization within the stent lumen can be achieved by using a larger flip angle (typically 75) to overcome the Faraday cage effects of stents, which cause RF shielding. Time of flight MRA techniques Time of flight (TOF) techniques are dependent on the inflow of unsaturated blood outside the field of view into the stationary tissue within a sec-
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tion that is already saturated because of its exposure to repeated pulses. The unsaturated blood appears bright compared with background tissue. There are several parameters that dictate successful TOF imaging. 1. Section thickness: The sections should be thin enough to allow for sufficient inflow between RF pulse repetitions but thick enough to ensure adequate SNR and anatomic coverage. Section thickness of 3 to 4 mm can provide for adequate images with larger vessels (ie, aorta, inferior vena cava, iliacs), whereas 1.5- to 2-mm slices are often required for imaging smaller vessels (ie, pedal vessels and carotid). 2. Optimal TR and flip angle: The typical TR setting for TOF is around 20 to 50 milliseconds. For successful TOF imaging, a relatively short TR keeps background tissue saturated. The TR should not be too short because it should allow for satisfactory inflow of unsaturated blood (spins) between successive repetitions. The flip angle is usually maintained between 30 and 60. The use of a high flip angle, although effective in suppressing background tissue, may saturate flowing blood and reduce the contrast separation. Furthermore, with phasic flow (as in the arteries of the extremity), systolic flow signal may be increased (because of the greater transverse magnetization created), and the diastolic signal may be decreased, creating view-to-view intensity changes and phase artifacts from pulsatile variations. Pulsation artifact is greater at higher flip angles. 3. Maintenance of phase: The phase of blood must be kept coherent. This requires the use of gradient moment nulling techniques (flow compensation), short TE, and cardiac or peripheral gating. The short sampling time allows for avoidance of phase errors that may result from pulsatile flow. 4. Saturation pulses: The placement of saturation pulses superior or inferior to the section being imaged reduces pulsation artifacts secondary to overlying arteries and veins. For example, the application of superiorly placed saturation pulse when imaging a longitudinally placed artery such as the carotid may help reduce artifact secondary to venous flow (flowing downward). Conversely, inferiorly placed saturation pulses while imaging jugular veins may prevent imaging the carotid
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artery. 2D-TOF arteriograms and venograms have no ability intrinsically to distinguish arteries from veins but depict directional flow. Saturation pulses may cause inadvertent saturation of desired blood vessels with complex spatial relationships. 3D-TOF consists of a gradient echo acquisition of a volume into which blood is flowing. The major advantages of 3D-TOF techniques are higher SNR and improved resolution in the section direction. This technique is most helpful in vessels with rapid steady blood flow without respiratory motion (eg, intracranial vessels such as the circle of Willis). Unlike 2D-TOF, which does not benefit from the administration of contrast agents, blood within the imaged volume is partially saturated in 3DTOF. The administration of gadolinium aids in the prompt recovery of the longitudinal magnetization and increases signal intensity, unlike in 2D-TOF, where contrast agents do not improve image quality but interfere with the ability to suppress veins. MRA techniques for the diagnosis of peripheral arterial disease Assessment of the patient with peripheral arterial disease (PAD) requires a systematic evaluation of the inflow and outflow vessels. There are three approaches for accomplishing the challenge of obtaining meaningful information in the entire leg. The most widely used approach is to use contrast-based techniques for the iliac vessels and 2D-TOF (flow based) for the infra-inguinal circulation. The introduction of moving tables (floating tables) has facilitated ‘‘bolus chase’’ threedimensional contrast MRA approaches, where a single bolus of contrast is followed down to the foot (see Fig. 3 for setting up for bolus-chase imaging) [3]. This technique works extremely well to the level of the popliteal arteries; however, the c Fig. 3. Patient set-up for 2D projection MRA and floating table (moving table) examination for PAD. (A,B) Positioning for 2D-MRDSA of pedal vessels and calf vessels, respectively. Time for contrast arrival from panel B is used for setting up bolus stations. (C ) Leveling of knee and ankle on the same plane. Landmark is set at the level of the sternum. (D–F ) Sequential stations (pelvis, thigh, and calf) for obtaining mask images followed by injection of the Gadolinium and bolus chase acquisition. The first station uses reverse centric k-space acquisition, and the second and third use centric k-space acquisition.
image resolution with the fast 3D sequences does not allow satisfactory visualization of the smaller vessels of the tibio-peroneal circulation. Although one may theoretically improve the image by choosing thinner slices, at higher matrix size (ie, 512) and
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larger contrast doses, this prolongs scan time. In patients with short arterial-venous transit time, image quality in the tibio-peroneal vessels is compromised by venous overlay because of the longer scan times (1 to 2 minutes). Alternate approaches that eliminate these concerns are the use of a separate injection for infra-popliteal arteries with time-resolved imaging (ie, time-resolved imaging on contrast kinetics [TRICKS] or two-dimensional MRDSA [2D-MRDSA]). A recent modification involves thick-slab, two-dimensional MRDSA of the tibial run-off and pedal vessels [4]. Highresolution scans may be performed with 5 to 7 mL of dye using local coils (head coil, extremity coil). Dynamic 2D-MRDSA is ideally suited as a prelude to the bolus chase examination because it provides information on bolus timing for the bolus chase part of the examination [4]. 2D-TOF for lower extremity imaging Time of flight is effective for infra-popliteal vessels as an alternative to 2D-DSA examinations [5]. Typical TOF settings for imaging of the lower extremities include: TR ¼ 30 to 45 milliseconds, TE ¼ 6.9 milliseconds with gradient moment nulling, flip ¼ 60, field of view of 24 to 32 cm, and a 256128 acquisition matrix. Because of the variation of flow with the cardiac cycle, EKG gating may improve image quality. A spatial pre-saturation pulse is often placed inferior to the slice to prevent venous signal. The pitfalls of TOF include excessive scan times that reduce patient through-put and flow artifacts caused by the pulsatile nature of arterial flow. The presence of collateral vessels in PAD patients often leads to flow in the opposite direction, complicating the use of spatial pre-saturation for eliminating venous signal. Three-dimensional TRICKS Most scanners require 20 seconds to acquire a standard 3D data set. This represents inadequate temporal resolution. 3D-TRICKS is a scheme to increase frame rates up to 2 seconds per 3D volume and relies on a number of post-processing b Fig. 4. Multi-station 3D MRA using 3D-TRICKS. Coronal time-resolved examination using a dedicated peripheral vascular coil (TR/TE/Flip ¼ 7/1.8/45; field of view ¼ 483688 mm; matrix size ¼ 51218244, zerofilling). Interpretation: Bilateral SFA disease with patent femoro-popliteal grafts. Multiple high-grade lesions are seen on the right SFA with an occluded left SFA with evidence of profunda collaterals.
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algorithms that facilitate rapid acquisition of data within a single breath-hold. This method combines more frequent sampling of central k-space data relative to the periphery of k-space, zero-filling, and temporal interpolation of data and seems to offer better resolution than conventional bolus chase techniques that do not incorporate 2DMRDSA techniques for the visualization of infrapopliteal vessels (Fig. 4) [6].
MRA for the diagnosis of renovascular and abdominal aortic disease Magnetic resonance angiography is emerging as a highly effective and safe modality for the assessment of aortic and renal disease [7]. Examinations can be performed with breath-holding for comprehensive evaluation of the entire renal artery and the concomitant presence of aortic disease up to this level. Renal MRA can provide anatomic and physiologic information on the severity of renal artery stenosis and information on the presence of neoplastic renal or peri-renal masses. At our institutions, the following sequences are obtained for renal artery imaging [8]: 1. Sagittal locator: This could be a spin echo sequence (interleaved acquisition) or a singleshot fast spin-echo sequence, using a field of view large enough to cover the entire region of interest (40 to 44 cm). This T1-weighted locator sequence is useful to measure renal parenchyma size.
2. Axial T2 sequence with fat saturation: This sequence helps to evaluate anatomy and rule out the presence of neoplasms of the kidney and retroperitoneum. 3. Coronal 3D gadolinium-enhanced MRA: 3D dynamic spoiled-gradient echo imaging is performed with breath-hold in the coronal plane. The sequence is repeated three times: pre-contrast, during the arterial phase, and during the venous or equilibrium phase of contrast administration. The number of slices, slice thickness, and phase encode steps may be adjusted to set up subsequent scans within the patients breath-hold effort. To obtain arterial phase images, central k-space data are acquired when the gadolinium is maximally present in the arterial circulation. For this, an automated system such as Smartprep (GE Medical Systems, Milwaukee, Wisconsin) or Care Bolus (Siemens Medical Solutions, Malvern, Pennsylvania) is used. Alternately, a time-resolved examination at high frame rates can be accomplished (3D frame rate of 5 to 10 seconds per image), which results in a time-resolved examination (multiphase renal MRA) (Fig. 5). 4. Axial 3D phase contrast (PC) MRA: This sequence provides another high-resolution look at the renal arteries and helps in the evaluation of hemodynamic significance of renal artery stenosis (Fig. 6). Performance of the sequence after gadolinium contrast imaging takes advantage of the extra SNR produced by the contrast agent.
Fig. 5. Multiphase 3D contrast MRA (time-resolved examination) showing bilateral renal artery stenosis in coronal MIP projections.
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Image analysis The four pulse sequences are analyzed systematically beginning with the sagittal sequence [8]. The 3D data set is post-processed on a computer workstation with the construction of MIP images and re-formations. The severity of renal artery stenosis is decided initially on the basis of 3D gadolinium MRA. This is further evaluated on 3D PC images by the presence of signal ‘‘dephasing’’ (Fig. 6). Normal renal artery caliber on 3D PC indicates normal renal arteries or at most mild renal artery stenosis. Severe signal dephasing is evidence of hemodynamically significant renal artery stenosis [9]. If the stenosis is apparent on 3D gadolinium MRA and 3D PC but there is no dephasing, then it is graded as moderate (Fig. 6). Post-stenotic dila-
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tation, loss of cortical medullary differentiation, delayed renal enhancement, and asymmetric concentration of gadolinium in the collecting system during the equilibrium phase are additional signs of hemodynamic significance [8].
Mesenteric-portal MRA The sequence for mesenteric MRA is similar to renal MRA and includes a sagittal locator sequence followed by axial T2 images and coronal 3D contrast-enhanced MRA. Include the portal veins and mesenteric vessels while specifying the 3D volume. Additional sequences that may be optional include a 2D-TOF sequence that provides views of the IVC, hepatic veins, and the portal veins
Fig. 6. (A) Coronal MIP reconstructed from a 3D-MRA examination of the aorta and renal arteries, demonstrating high-grade stenosis of the proximal left renal artery with reduced opacification of left kidney. (B) Axial MIP reformation demonstrating the same stenosis. (C) The severity of the stenosis is confirmed by signal ‘‘dephasing’’ on the axial 3D-phase images.
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with high SNR and axial 3D phase contrast MRA sequence to assess for concomitant renal artery lesions.
MRA for the diagnosis of extra-cranial carotid and arch disease 3D contrast MRA of the carotid and thoracic aorta has revolutionized noninvasive examination of the extra-cranial carotid and arch. Before the evolution of 3D gadolinium contrast MRA as a standard part of MRA, it was routine to use 2D-
TOF and 3D-multislab TOF MRA alone. The 2D-TOF techniques are complementary, and it is important to use them together to accurately diagnose stenosis. The flow dependence of these techniques and their consequent susceptibility to flow artifacts are their limitations [10]. The advantages of gadolinium-enhanced MRA for carotid angiography include the ability to image plaque ulcerations, which are often not seen on TOF; no flow-related artifacts so that tortuous vessels are not degraded by in-plant saturation; short imaging times with excellent SNR; and coverage from aortic arch to circle of Willis in 30 to 40 seconds.
Fig. 7. (A) 3D fast-gradient echo acquisition of aortic arch and great vessels that demonstrates an occlusion of the right subclavian. The right vertebral is seen opacifying slower than the left. (B) Delayed images obtained a few seconds later reveal retrograde filling of the right subclavian through the right vertebral compatible with a radiographic subclavian steal. (C) The retrograde flow in the right vertebral is confirmed by 2D phase contrast that demonstrates retrograde flow (white arrow) along the same direction as flow in the jugular vein. Arterial flow is black.
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3D gadolinium-enhanced MRA of the carotids 3D contrast MRA is usually obtained in the coronal plane. Arterial-venous transit time in the cerebral circulation is extremely rapid and necessitates split-second timing. There are a variety of techniques that may be used to successfully image carotid arteries. An automated contrast detection method, such as SmartPrep (GE Medical Systems, Milwaukee, Wisconsin), can be used as in peripheral MRA. Recently, a fluoroscopically triggered acquisition has been described and seems to provide superior temporal and spatial resolution [11]. The acquisition is performed with true centric k-space weighting or with the center of k-space slightly recessed in from the beginning of the scan to avoid jugular venous enhancement. Multi-phase acquisition, using the 3D-TRICKS technique (3D frame rate of 3 to 4 per second), ensures short acquisition times such that at least one of the volumes includes the arterial phase [12]. With timeresolved acquisition, however, there may be some compromise in spatial resolution. Post-processing of the carotid MRA examination involves digital subtraction with mask images. Subtraction of background tissue signal improves the fidelity of MIP reconstructions, especially in the region of stenosis. The source images are reformatted at different angles to display stenoses at a variety of angels. Breath-holding improves the sharpness of the aortic arch and great vessel origins but has no effect on the visualization of the carotid vessels [13]. Breath-holding also runs the risk of arching the neck, which moves the carotid arteries anteriorly and potentially out of the coronal imaging volume. 3D gadolinium-enhanced MRA of the aortic arch Atherosclerotic disease involving the arch can be accurately assessed by MRA. Involvement of a subclavian artery or vertebral artery (the left is more commonly involved than the right) may give rise to ‘‘subclavian steal syndrome’’ (Fig. 7). This may be confirmed using phase-contrast measurements that may reveal the retrograde nature of flow in the vertebral arteries. Assessment for inflammatory involvement of the arch and the great vessels may require additional T2-weighted sequences or delayed T1-weighted EKG-gated spin echo sequences in the axial plane with fat saturation at 6- to 8-mm intervals. Flow compensation with phase re-ordering and respiratory compensation are also prerequisites. Axial gradient echoes obtained post-contrast should be collected
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with a large flip angle to take advantage of the presence of gadolinium-induced T1 shortening. With active aortitis, the wall is often bright on T2 and on post-gadolinium images. Safety checks and MR artifacts Box 1 demonstrates a rough safety check to assess MR compatibility of metallic objects before performing an MR scan. The reader is referred to more comprehensive sources for additional details [14]. MRI is associated with a number of artifacts that require recognition to avoid confusing them with normal anatomy or pathology (Box 2). Artifacts, such as those arising from metal clips or wrap around, are relatively common. Signal drop-out may arise as a consequence of low SNR that may have multiple potential etiologies. Conclusions Magnetic resonance angiographic techniques use inherent magnetization properties of tissues in combination with pharmacologic contrast agents such as gadolinium that shorten T1 relaxation time. The availability of powerful magnetic field gradients along with a variety of post-processing
Box 1. Artifacts from MRA Technical issues that may exaggerate stenosis • Long TE • Vessel not fully in 3D slab • Low spatial resolution Inadequate SNR (deterioration of image) • Insufficient inflow or Gd dosage too low • Bad Gd timing • Slices too thin • Field of view too small • Inadequate field strength/gradient performance Miscellaneous artifacts • • • •
Metal clips Wrap from arms Bright fat, hemorrhage/Gl contents Overlap on MIPs
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Box 2. Safety screening before MT examination Absolute contraindications • Pacemaker, automatic implantable cardioverter defibrillator (AICD) • Brain aneurysm clip • Metal in eye • Cochlear implant • Electronic implants No contraindications • Stents, coils, and filters (after 4 to 6 weeks of introduction) • Clips outside brain • Vascular access ports • Dental devices and materials • Orthopedic metal • Heart valves after 1983 algorithms make MRA possible. MRA is widely used in a variety of vessels, including aorta, carotids, renals, mesenteric, and peripherals. Performance of high-quality 3D contrast MRA requires appropriate understanding of MR methodologies, including the critical dependence of bolus timing with this technique and ways to optimize this. Additionally, recognition of artifacts and learning to avoid them is important. References [1] Nitz WR, Reimer P. Contrast mechanisms in MR imaging. Eur Radiol 1999;9:1032–46. [2] Prince MR, Grist TM, Debatin JF. 3D Contrast MR Angiography, 1st edition. Berlin: SpringerVerlag; 1999. [3] Wang Y, Lee HM, Khilnani NM, et al. Bolus-chase MR digital subtraction angiography in the lower extremity. Radiology 1998;207:263–9.
[4] Wang Y, Winchester PA, Khilnani NM, et al. Contrast-enhanced peripheral MR angiography from the abdominal aorta to the pedal arteries: combined dynamic two-dimensional and boluschase three-dimensional acquisitions. Invest Radiol 2001;36:170–7. [5] Owen RS, Carpenter JP, Baum RA, et al. Magnetic resonance imaging of angiographically occult runoff vessels in peripheral arterial occlusive disease. N Engl J Med 1992;326:1577–81. [6] Hany TF, Carroll TJ, Omary RA, et al. Aorta and runoff vessels: single-injection MR angiography with automated table movement compared with multiinjection time-resolved MR angiography– initial results. Radiology 2001;221:266–72. [7] Dong Q, Schoenberg SO, Carlos RC, et al. Diagnosis of renal vascular disease with MR angiography. Radiographics 1999;19:1535–54. [8] Prince MR. Renal MR angiography: a comprehensive approach. J Magn Reson Imaging 1998;8: 511–6. [9] Prince MR, Schoenberg SO, Ward JS, et al. Hemodynamically significant atherosclerotic renal artery stenosis: MR angiographic features. Radiology 1997;205:128–36. [10] Cloft HJ, Murphy KJ, Prince MR, et al. 3D gadolinium-enhanced MR angiography of the carotid arteries. Magn Reson Imaging 1996;14:593–600. [11] Fellner FA, Fellner C, Wutke R, et al. Fluoroscopically triggered contrast-enhanced 3D MR DSA and 3D time-of-flight turbo MRA of the carotid arteries: first clinical experiences in correlation with ultrasound, x-ray angiography, and endarterectomy findings. Magn Reson Imaging 2000;18:575–85. [12] Carroll TJ, Korosec FR, Petermann GM, et al. Carotid bifurcation: evaluation of time-resolved three-dimensional contrast-enhanced MR angiography. Radiology 2001;220:525–32. [13] Carr JC, Ma J, Desphande V, et al. High-resolution breath-hold contrast-enhanced MR angiography of the entire carotid circulation. Am J Roentgenol 2002;178:543–9. [14] Shellock FG, Kanal E. Magnetic resonance: bioeffects and safety. St. Louis: Mosby; 1998.
Magnetic resonance angiographic techniques for the diagnosis of arterial disease Sanjay Rajagopalan, MD*, Martin Prince, MD, PhD Division of Cardiology, Section of Vascular Medicine, University of Michigan, L311 Women’s Hospital, 1500 E. Medical Center Drive, Ann Arbor, MI 48107, USA
Magnetic resonance angiography (MRA) techniques use inherent magnetization properties of tissues in combination with pharmacologic contrast agents, such as gadolinium, that shorten T1 relaxation time. The availability of powerful magnetic field gradients along with a variety of post-processing algorithms make MRA possible. MRA is widely used for the diagnosis of disease in a variety of vessels, including aorta, carotids, renals, mesenteric, and peripheral vessels. Performance of high-quality 3D contrast MRA requires appropriate understanding of MR methodologies, including the critical dependence of bolus timing and ways to optimize it. Additionally, recognition of artifacts and learning to avoid them is important. Fundamentals of magnetic resonance physics The magnetic resonance (MR) techniques in use are dependent on signals from hydrogen atoms (protons). The abundance of the hydrogen atoms in the human body and the large magnetic moment created by the single proton in the nucleus of the atom make hydrogen atoms extremely sensitive to MR. Resonance is referred to as the property of an atom to absorb energy only at a certain frequency (x), called the Larmor frequency, where x ¼ dB0 (where d represents a constant called the gyromagnetic ratio, and B represents the magnetic field strength). An atom absorbs external energy only if that energy is delivered at the resonant frequency x. * Corresponding author. E-mail address: [email protected] (S. Rajagopalan).
When a patient is placed in the MR scanner, a small fraction of hydrogen nuclei align with the main magnetic field (B0), creating a net magnetization vector. The time required for this to occur is known as T1. The net magnetization vector is aligned with the B0. In MR imaging, energy in the radiofrequency (RF) range is used to deflect the net magnetization vector from the longitudinal to the transverse plane (transverse magnetization) (Fig. 1). The angle of net magnetization-deflection created after the end of the RF pulse is referred to as the flip angle. The stronger the RF energy applied to the protons, the greater the angle of deflection for the magnetization. Common flip angles in MR are 90 and 180. A 90 pulse flips the magnetization into the x-y plane. A 180 pulse flips the magnetization through the x-y plane and into the opposite direction of B0. After the RF pulse tip spins out of alignment with B0, new protons begin to align with B0 at a characteristic rate, T1. When spins are tipped into the transverse plane (created with a 90 flip angle) and a receiver coil or antenna is nearby, an oscillating voltage is induced within the receiver coil. The magnitude of the signal oscillation is dependent on the magnetization in the transverse plane. As the transverse magnetization starts to decay due to the loss of phase coherence, the protons eventually realign with B0. This signal, or ‘‘echo,’’ produced by the decay of transverse magnetization is called free induction decay. The MRI amplitude signal becomes smaller over time at a rate known as T2. Transverse relaxation is the return of transverse magnetization to equilibrium and is termed T2 decay. Simultaneously, the longitudinal magnetization begins to recover and return to a state
0733-8651/02/$ - see front matter 2002, Elsevier Science (USA). All rights reserved. PII: S 0 7 3 3 - 8 6 5 1 ( 0 2 ) 0 0 0 8 8 - 7
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Fig. 1. The effect of RF pulse at Larmor frequency (x) on longitudinal magnetization (M0). Once the net M0 is tipped away from the B0 direction into the transverse place (Mxy), it proceeds. The precession of the magnetic field induces a current via Faraday’s Law of Induction by a conductor nearby (surface coil).
of equilibrium. Longitudinal relaxation is the return of longitudinal magnetization to equilibrium (B0) and is termed T1 recovery. Longitudinal and transverse magnetizations occur simultaneously but are two different processes that inherit properties of various tissues in the body. For instance, fat has a very short T1 and T2 recovery time, whereas water and CSF have some of the longest T1 and T2 recovery times. One way to distinguish between various tissues is to take advantage of these differences in T2 decay and T1 recovery to form T1 and T2 weighted images. In addition to the transverse decay of the macroscopic magnetization caused by T2 relaxation, there are other ‘‘dephasing’’ mechanisms, including field and tissue inhomogeneity, that result in rapid loss of transverse magnetization (T2* effects). In spin echo imaging, this dephasing is refocused with a 180 RF pulse. In gradient echo imaging (see below), where this 180 pulse is omitted, the T2* free induction decay is observed. The reader is referred to more detailed reviews on the mechanisms of MR contrast [1].
Magnetic field gradients, Fourier transforms, and fast MRI techniques Field gradients are what make MRI possible by allowing the signal to be localized in space. The gradients are applied in three planes as slice select (Gss), phase encode, and frequency (read-out) gradients, which spread out the proton resonance in a specific fashion. Unlike back projection reconstruction used in CT, whereby one-dimensional radial projections are sampled, MR uses Fourier reconstruction methods. Many RF pulses are
delivered, and for each RF pulse, an echo is collected. The time between successive echoes is referred to as repetition time (TR), and the time between RF pulse and echo is referred to as echo time (TE). The echoes are then digitized and stored in a data acquisition matrix. This data matrix is referred to as k-space. Two-dimensional Fourier transform (2D-FT) uses the same slice select and readout gradients for each pulse while the phaseencoding gradient is stepped through many different steps from very high to very low amplitude (and to very high amplitude again). The lowamplitude gradient acquisitions sample low spatial frequency k-space data, whereas the pulses during high-amplitude phase-encoding gradient sample high spatial frequency k-space data. A variety of techniques can be used to reduce the time to obtain images to facilitate fast MRI with a single breath hold. Scan time in 2D-FT techniques ¼ TRnNEX (where n ¼ number of phase encode steps, and NEX ¼ number of excitations). For three-dimensional acquisitions, the phase encoding occurs along two axis, ny and nz, which requires additional time. The techniques that can be used to speed up scanning include (i) reducing TR, (ii) reducing the number of phase encode steps, (iii) reducing NEX, (iv) partial Fourier methods that involve acquiring part of the data and using techniques such as conjugate data synthesis and zero filling or padding to make up the remaining data, and (v) parallel imaging. Tissue contrast is principally determined by the center of k-space (central phase encoding lines) while the periphery encodes image detail. MR data are acquired so that contrast and detail are incorporated. The order in which k-space lines are collected can be varied and strongly influences
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tissue contrast. In conventional MRI, the k-space acquisition is sequential, whereas in fast MRI, techniques for 3D contrast angiography, centric, or elliptic-centric acquisition is often used.
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gadolinium chelates with the highest relaxivity and by having a high gadolinium concentration in the blood. Dosage of gadolinium used in MRA
Gadolinium-based MRA Paramagnetic contrast agents Gadolinium is an element in the transition group IIIb of the periodic table. It has eight unpaired electrons in its outer shell, which confers its paramagnetic effect. Gadolinium by itself can cause heavy metal poisoning but when bound to a chelator is safe for intravenous injection. Gadolinium shortens T1 of blood in the region of the gadolinium molecule according to the following equation [2]: 1/T1 ¼ 1/1200þ(R1[Gd]), where R1 is the T1 relaxivity of the gadolinium chelate, [Gd] is the gadolinium concentration in the blood, and 1200 is the blood T1 (in milliseconds) without gadolinium. The blood [Gd] must be greater than 1.0 mmol/L for T1 to be less than 270 milliseconds, which is the T1 of fat at 1.5 T (Fig. 2). This is the property that is important for increasing the MR signal intensity of blood on contrast-enhanced spoiled gradient echo (SPGR) images (see below). This T1 shortening effect is maximized by using
Fig. 2. Blood T1 plotted against Gadolinium concentration [Gd]. A [Gd] of [2 in the blood translates into a T1 of 100, which is well below that of fat. Assuming a resting cardiac output of 5 L/min, achieving this T1 requires an injection rate of at least 0.2 mL/s (12 mL/min). This injection rate sustained over a 3-minute scan duration translates into a minimum gadolinium dose of 36 mL.
To make blood bright compared with all background tissues, it is necessary to give a sufficient dosage of gadolinium at a sufficient rate of injection. Generally, two bottles (20 mL each) of the gadolinium contrast agent (about 0.3 mmol/kg gadolinium) is sufficient for an average person when imaging in the equilibrium phase. However, arteries are best imaged during the arterial phase of gadolinium infusion to take advantage of the higher arterial signal-to-noise ratio (SNR) and to eliminate overlapping venous enhancement. It may seem that an extremely fast acquisition is essential to capture the contrast agent bolus during the brief moment that the agent is present in the arteries but not yet in the veins. However, three important effects make it possible for a relatively slower MR acquisition to capture an arterialphase image without having to use large amounts of gadolinium: 1. Phase reordering (mapping of k-space): To obtain an arterial-phase image in which arteries are bright and veins are dark, it is essential that the central k-space data (ie, the low spatial frequency data) are acquired while the gadolinium concentration in the arteries is high but relatively lower in the veins. This technique allows a relatively long MR acquisition to achieve the image contrast associated with a brief window of time. That brief window of time is the instant when central k-space data are acquired. Therefore, it is critical to time the bolus for maximum arterial [Gd] during acquisition of central k-space data. With perfect bolus timing, high signalto-noise arterial-phase images are possible with small doses of gadolinium. 2. Extraction of gadolinium by the capillary bed: This extraction results in venous blood tending to have a lower concentration of gadolinium relative to arterial blood, even for relatively long, sustained infusions lasting several minutes. This effect is not present in the cerebrovascular circulation because of the blood-brain barrier. Consequently, arterialphase imaging in the central nervous system is more difficult. 3. Infusion rate of gadolinium: Arterial [Gd] is maximized by relaxing the patient to reduce
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cardiac output and by using a high infusion rate. However, fast infusion rates lasting for at least half of the acquisition time require large doses of gadolinium. The dose can be kept to a reasonable level by scanning rapidly. Fast acquisitions (\45 seconds) are possible with high-performance gradient systems that allow short repetition and echo times without requiring a wide bandwidth. Fast acquisition has the additional benefit of making it possible for the cooperative patient to suspend breathing and to hold perfectly still. Spoiled gradient echo imaging (FLASH or SPGR) Gradient echo sequences are used for 3D contrast MR angiography (MRA) because of their speed and short echo times, which allow breathholding and ensure patient through-put. Spoiling helps by suppressing background signal and thereby enhances the signal from the contrast agent in the vasculature. Additional background signal suppression can be achieved with fat saturation pulses, but this incurs additional time. Unlike conventional angiography, the quality of MRA improves when it is performed rapidly. Although faster scanning is associated with a reduction in SNR related to diminished signal averaging, there is an increase in signal intensity associated with shorter T1 associated with injecting the same dose of contrast more rapidly with faster scans. Shortening the TR fourfold reduces the scan time by fourfold and allows a reduction in contrast bolus duration. However, this apparent decrease in contrast dose is offset by requiring an approximately fourfold increase in the injection rate to recover the same amount of longitudinal magnetization in between pulses. Thus, there is no net effect on the contrast dose if the signal-to-noise ratio is to remain unchanged for faster scans. The shorter TR, however, leads to better background suppression and thereby enhances contrast-to-noise ratio (CNR). Because image quality in contrast MRA is dependent on SNR and CNR, shorter imaging times due to shorter TR result in improved vessel visibility. Parameters for an optimal MRA examination Time to echo Time to echo (TE) timing for MRA is usually between 1 and 3 milliseconds. TE is chosen to minimize the dephasing effects (T2*) and to maximize
differences between fat and water (chemical shift artifact). Repetition time Repetition time (TR) timing is kept to the minimum to reduce overall scanning time. Manufacturers have designed special gradient echo (GRE) sequences that are ultrafast (UFGRE) and permit the shortest possible TR, which facilitates the completion of the entire study with a single breath-hold. Flip angle MRA is not dependent to a large extent on flip angle settings. Any angle in the range of 20 to 60 is appropriate. As TR decreases, the flip angle should be shortened. For a TR ¼ 2, a flip angle of 20 is appropriate. Bandwidth Adjusting bandwidth is a powerful way to manipulate SNR, TR, and TE. Increasing bandwidth reduces SNR and decreases TR and TE. Therefore, the bandwidth represents a compromise between a setting that provides for the least scan time versus one that provides for maximal SNR. Typically, we use 32 kHz for gadolinium MRA. Post-processing of MR data Substantial improvement in image quality, and especially image contrast, can be attained through post-processing techniques. Zero padding Apparent image resolution on reconstructions, such as maximum intensity projection (MIP) images, can be increased with interpolation schemes such as zero filling. This method involves filling out peripheral lines of k-space data with zeroes before performing the Fourier transform. No additional time is required for data collection, and the Fourier transform reconstructs more images with a smaller spacing. For example, with twofold zero padding, if the partition thickness is 3 mm, the Fourier transform reconstructs additional images that also have a 3-mm slice thickness but at 1.5-mm spacing with 50% overlap. This helps eliminate volume averaging and creates smooth visualization of small vessels on the reformatted MIP images. Twofold zero padding in the slice direction is recommended. MR digital subtraction angiography Image contrast can be improved by digital subtraction of pre-contrast image data from dynamic-,
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arterial-, or venous-phase image data. This subtraction can be performed slice-by-slice or before the Fourier transform by using a complex subtraction method. The improvement in contrast achieved with digital subtraction angiography (DSA) may reduce the gadolinium dosage required. However, there must be no change in the patient position between the pre-contrast and dynamic contrast-enhanced imaging. This requirement for no motion is easily met in the pelvis and legs, which can be sandbagged and strapped down. It is more difficult to achieve in the chest and abdomen, where respiratory, cardiac, and peristaltic motions are more difficult to avoid. The scanner generally performs complex subtraction automatically before creating any of the images. Another benefit of the subtraction is that it can be performed on the upslope or downslope of contrast enhancement. This may result in selective visualization of arteries and veins, respectively. Multiplanar reconstructions and MIP images Multiplanar 3D reformations are useful in assessing spatial relationships of vessels and to avoid vessel overlap. MIP images are produced by ray-tracing algorithms. The maximum intensity encountered along any predefined direction is assigned to the designated pixel. The advantage of MIP images is the similarity to conventional angiographic images that most vascular physicians are used to interpreting. Can stents be visualized with 3D contrast MRA? Stent-related artifacts associated with vascular endoprosthesis could arise from the metal in the stent and the geometry of the stent. This is a problem when imaging some of the older stents that are made from stainless steel or cobalt-based alloys (eg, the Palmaz and the Wallstent), which result in large signal voids in the stent region. With Nitinol or platinum stents, the artifacts are minor, with the stent frame filaments appearing as a signal void, enabling one to assess stent structure and rule out significant stenosis ([50%). Improved visualization within the stent lumen can be achieved by using a larger flip angle (typically 75) to overcome the Faraday cage effects of stents, which cause RF shielding. Time of flight MRA techniques Time of flight (TOF) techniques are dependent on the inflow of unsaturated blood outside the field of view into the stationary tissue within a sec-
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tion that is already saturated because of its exposure to repeated pulses. The unsaturated blood appears bright compared with background tissue. There are several parameters that dictate successful TOF imaging. 1. Section thickness: The sections should be thin enough to allow for sufficient inflow between RF pulse repetitions but thick enough to ensure adequate SNR and anatomic coverage. Section thickness of 3 to 4 mm can provide for adequate images with larger vessels (ie, aorta, inferior vena cava, iliacs), whereas 1.5- to 2-mm slices are often required for imaging smaller vessels (ie, pedal vessels and carotid). 2. Optimal TR and flip angle: The typical TR setting for TOF is around 20 to 50 milliseconds. For successful TOF imaging, a relatively short TR keeps background tissue saturated. The TR should not be too short because it should allow for satisfactory inflow of unsaturated blood (spins) between successive repetitions. The flip angle is usually maintained between 30 and 60. The use of a high flip angle, although effective in suppressing background tissue, may saturate flowing blood and reduce the contrast separation. Furthermore, with phasic flow (as in the arteries of the extremity), systolic flow signal may be increased (because of the greater transverse magnetization created), and the diastolic signal may be decreased, creating view-to-view intensity changes and phase artifacts from pulsatile variations. Pulsation artifact is greater at higher flip angles. 3. Maintenance of phase: The phase of blood must be kept coherent. This requires the use of gradient moment nulling techniques (flow compensation), short TE, and cardiac or peripheral gating. The short sampling time allows for avoidance of phase errors that may result from pulsatile flow. 4. Saturation pulses: The placement of saturation pulses superior or inferior to the section being imaged reduces pulsation artifacts secondary to overlying arteries and veins. For example, the application of superiorly placed saturation pulse when imaging a longitudinally placed artery such as the carotid may help reduce artifact secondary to venous flow (flowing downward). Conversely, inferiorly placed saturation pulses while imaging jugular veins may prevent imaging the carotid
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artery. 2D-TOF arteriograms and venograms have no ability intrinsically to distinguish arteries from veins but depict directional flow. Saturation pulses may cause inadvertent saturation of desired blood vessels with complex spatial relationships. 3D-TOF consists of a gradient echo acquisition of a volume into which blood is flowing. The major advantages of 3D-TOF techniques are higher SNR and improved resolution in the section direction. This technique is most helpful in vessels with rapid steady blood flow without respiratory motion (eg, intracranial vessels such as the circle of Willis). Unlike 2D-TOF, which does not benefit from the administration of contrast agents, blood within the imaged volume is partially saturated in 3DTOF. The administration of gadolinium aids in the prompt recovery of the longitudinal magnetization and increases signal intensity, unlike in 2D-TOF, where contrast agents do not improve image quality but interfere with the ability to suppress veins. MRA techniques for the diagnosis of peripheral arterial disease Assessment of the patient with peripheral arterial disease (PAD) requires a systematic evaluation of the inflow and outflow vessels. There are three approaches for accomplishing the challenge of obtaining meaningful information in the entire leg. The most widely used approach is to use contrast-based techniques for the iliac vessels and 2D-TOF (flow based) for the infra-inguinal circulation. The introduction of moving tables (floating tables) has facilitated ‘‘bolus chase’’ threedimensional contrast MRA approaches, where a single bolus of contrast is followed down to the foot (see Fig. 3 for setting up for bolus-chase imaging) [3]. This technique works extremely well to the level of the popliteal arteries; however, the c Fig. 3. Patient set-up for 2D projection MRA and floating table (moving table) examination for PAD. (A,B) Positioning for 2D-MRDSA of pedal vessels and calf vessels, respectively. Time for contrast arrival from panel B is used for setting up bolus stations. (C ) Leveling of knee and ankle on the same plane. Landmark is set at the level of the sternum. (D–F ) Sequential stations (pelvis, thigh, and calf) for obtaining mask images followed by injection of the Gadolinium and bolus chase acquisition. The first station uses reverse centric k-space acquisition, and the second and third use centric k-space acquisition.
image resolution with the fast 3D sequences does not allow satisfactory visualization of the smaller vessels of the tibio-peroneal circulation. Although one may theoretically improve the image by choosing thinner slices, at higher matrix size (ie, 512) and
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larger contrast doses, this prolongs scan time. In patients with short arterial-venous transit time, image quality in the tibio-peroneal vessels is compromised by venous overlay because of the longer scan times (1 to 2 minutes). Alternate approaches that eliminate these concerns are the use of a separate injection for infra-popliteal arteries with time-resolved imaging (ie, time-resolved imaging on contrast kinetics [TRICKS] or two-dimensional MRDSA [2D-MRDSA]). A recent modification involves thick-slab, two-dimensional MRDSA of the tibial run-off and pedal vessels [4]. Highresolution scans may be performed with 5 to 7 mL of dye using local coils (head coil, extremity coil). Dynamic 2D-MRDSA is ideally suited as a prelude to the bolus chase examination because it provides information on bolus timing for the bolus chase part of the examination [4]. 2D-TOF for lower extremity imaging Time of flight is effective for infra-popliteal vessels as an alternative to 2D-DSA examinations [5]. Typical TOF settings for imaging of the lower extremities include: TR ¼ 30 to 45 milliseconds, TE ¼ 6.9 milliseconds with gradient moment nulling, flip ¼ 60, field of view of 24 to 32 cm, and a 256128 acquisition matrix. Because of the variation of flow with the cardiac cycle, EKG gating may improve image quality. A spatial pre-saturation pulse is often placed inferior to the slice to prevent venous signal. The pitfalls of TOF include excessive scan times that reduce patient through-put and flow artifacts caused by the pulsatile nature of arterial flow. The presence of collateral vessels in PAD patients often leads to flow in the opposite direction, complicating the use of spatial pre-saturation for eliminating venous signal. Three-dimensional TRICKS Most scanners require 20 seconds to acquire a standard 3D data set. This represents inadequate temporal resolution. 3D-TRICKS is a scheme to increase frame rates up to 2 seconds per 3D volume and relies on a number of post-processing b Fig. 4. Multi-station 3D MRA using 3D-TRICKS. Coronal time-resolved examination using a dedicated peripheral vascular coil (TR/TE/Flip ¼ 7/1.8/45; field of view ¼ 483688 mm; matrix size ¼ 51218244, zerofilling). Interpretation: Bilateral SFA disease with patent femoro-popliteal grafts. Multiple high-grade lesions are seen on the right SFA with an occluded left SFA with evidence of profunda collaterals.
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algorithms that facilitate rapid acquisition of data within a single breath-hold. This method combines more frequent sampling of central k-space data relative to the periphery of k-space, zero-filling, and temporal interpolation of data and seems to offer better resolution than conventional bolus chase techniques that do not incorporate 2DMRDSA techniques for the visualization of infrapopliteal vessels (Fig. 4) [6].
MRA for the diagnosis of renovascular and abdominal aortic disease Magnetic resonance angiography is emerging as a highly effective and safe modality for the assessment of aortic and renal disease [7]. Examinations can be performed with breath-holding for comprehensive evaluation of the entire renal artery and the concomitant presence of aortic disease up to this level. Renal MRA can provide anatomic and physiologic information on the severity of renal artery stenosis and information on the presence of neoplastic renal or peri-renal masses. At our institutions, the following sequences are obtained for renal artery imaging [8]: 1. Sagittal locator: This could be a spin echo sequence (interleaved acquisition) or a singleshot fast spin-echo sequence, using a field of view large enough to cover the entire region of interest (40 to 44 cm). This T1-weighted locator sequence is useful to measure renal parenchyma size.
2. Axial T2 sequence with fat saturation: This sequence helps to evaluate anatomy and rule out the presence of neoplasms of the kidney and retroperitoneum. 3. Coronal 3D gadolinium-enhanced MRA: 3D dynamic spoiled-gradient echo imaging is performed with breath-hold in the coronal plane. The sequence is repeated three times: pre-contrast, during the arterial phase, and during the venous or equilibrium phase of contrast administration. The number of slices, slice thickness, and phase encode steps may be adjusted to set up subsequent scans within the patients breath-hold effort. To obtain arterial phase images, central k-space data are acquired when the gadolinium is maximally present in the arterial circulation. For this, an automated system such as Smartprep (GE Medical Systems, Milwaukee, Wisconsin) or Care Bolus (Siemens Medical Solutions, Malvern, Pennsylvania) is used. Alternately, a time-resolved examination at high frame rates can be accomplished (3D frame rate of 5 to 10 seconds per image), which results in a time-resolved examination (multiphase renal MRA) (Fig. 5). 4. Axial 3D phase contrast (PC) MRA: This sequence provides another high-resolution look at the renal arteries and helps in the evaluation of hemodynamic significance of renal artery stenosis (Fig. 6). Performance of the sequence after gadolinium contrast imaging takes advantage of the extra SNR produced by the contrast agent.
Fig. 5. Multiphase 3D contrast MRA (time-resolved examination) showing bilateral renal artery stenosis in coronal MIP projections.
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Image analysis The four pulse sequences are analyzed systematically beginning with the sagittal sequence [8]. The 3D data set is post-processed on a computer workstation with the construction of MIP images and re-formations. The severity of renal artery stenosis is decided initially on the basis of 3D gadolinium MRA. This is further evaluated on 3D PC images by the presence of signal ‘‘dephasing’’ (Fig. 6). Normal renal artery caliber on 3D PC indicates normal renal arteries or at most mild renal artery stenosis. Severe signal dephasing is evidence of hemodynamically significant renal artery stenosis [9]. If the stenosis is apparent on 3D gadolinium MRA and 3D PC but there is no dephasing, then it is graded as moderate (Fig. 6). Post-stenotic dila-
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tation, loss of cortical medullary differentiation, delayed renal enhancement, and asymmetric concentration of gadolinium in the collecting system during the equilibrium phase are additional signs of hemodynamic significance [8].
Mesenteric-portal MRA The sequence for mesenteric MRA is similar to renal MRA and includes a sagittal locator sequence followed by axial T2 images and coronal 3D contrast-enhanced MRA. Include the portal veins and mesenteric vessels while specifying the 3D volume. Additional sequences that may be optional include a 2D-TOF sequence that provides views of the IVC, hepatic veins, and the portal veins
Fig. 6. (A) Coronal MIP reconstructed from a 3D-MRA examination of the aorta and renal arteries, demonstrating high-grade stenosis of the proximal left renal artery with reduced opacification of left kidney. (B) Axial MIP reformation demonstrating the same stenosis. (C) The severity of the stenosis is confirmed by signal ‘‘dephasing’’ on the axial 3D-phase images.
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with high SNR and axial 3D phase contrast MRA sequence to assess for concomitant renal artery lesions.
MRA for the diagnosis of extra-cranial carotid and arch disease 3D contrast MRA of the carotid and thoracic aorta has revolutionized noninvasive examination of the extra-cranial carotid and arch. Before the evolution of 3D gadolinium contrast MRA as a standard part of MRA, it was routine to use 2D-
TOF and 3D-multislab TOF MRA alone. The 2D-TOF techniques are complementary, and it is important to use them together to accurately diagnose stenosis. The flow dependence of these techniques and their consequent susceptibility to flow artifacts are their limitations [10]. The advantages of gadolinium-enhanced MRA for carotid angiography include the ability to image plaque ulcerations, which are often not seen on TOF; no flow-related artifacts so that tortuous vessels are not degraded by in-plant saturation; short imaging times with excellent SNR; and coverage from aortic arch to circle of Willis in 30 to 40 seconds.
Fig. 7. (A) 3D fast-gradient echo acquisition of aortic arch and great vessels that demonstrates an occlusion of the right subclavian. The right vertebral is seen opacifying slower than the left. (B) Delayed images obtained a few seconds later reveal retrograde filling of the right subclavian through the right vertebral compatible with a radiographic subclavian steal. (C) The retrograde flow in the right vertebral is confirmed by 2D phase contrast that demonstrates retrograde flow (white arrow) along the same direction as flow in the jugular vein. Arterial flow is black.
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3D gadolinium-enhanced MRA of the carotids 3D contrast MRA is usually obtained in the coronal plane. Arterial-venous transit time in the cerebral circulation is extremely rapid and necessitates split-second timing. There are a variety of techniques that may be used to successfully image carotid arteries. An automated contrast detection method, such as SmartPrep (GE Medical Systems, Milwaukee, Wisconsin), can be used as in peripheral MRA. Recently, a fluoroscopically triggered acquisition has been described and seems to provide superior temporal and spatial resolution [11]. The acquisition is performed with true centric k-space weighting or with the center of k-space slightly recessed in from the beginning of the scan to avoid jugular venous enhancement. Multi-phase acquisition, using the 3D-TRICKS technique (3D frame rate of 3 to 4 per second), ensures short acquisition times such that at least one of the volumes includes the arterial phase [12]. With timeresolved acquisition, however, there may be some compromise in spatial resolution. Post-processing of the carotid MRA examination involves digital subtraction with mask images. Subtraction of background tissue signal improves the fidelity of MIP reconstructions, especially in the region of stenosis. The source images are reformatted at different angles to display stenoses at a variety of angels. Breath-holding improves the sharpness of the aortic arch and great vessel origins but has no effect on the visualization of the carotid vessels [13]. Breath-holding also runs the risk of arching the neck, which moves the carotid arteries anteriorly and potentially out of the coronal imaging volume. 3D gadolinium-enhanced MRA of the aortic arch Atherosclerotic disease involving the arch can be accurately assessed by MRA. Involvement of a subclavian artery or vertebral artery (the left is more commonly involved than the right) may give rise to ‘‘subclavian steal syndrome’’ (Fig. 7). This may be confirmed using phase-contrast measurements that may reveal the retrograde nature of flow in the vertebral arteries. Assessment for inflammatory involvement of the arch and the great vessels may require additional T2-weighted sequences or delayed T1-weighted EKG-gated spin echo sequences in the axial plane with fat saturation at 6- to 8-mm intervals. Flow compensation with phase re-ordering and respiratory compensation are also prerequisites. Axial gradient echoes obtained post-contrast should be collected
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with a large flip angle to take advantage of the presence of gadolinium-induced T1 shortening. With active aortitis, the wall is often bright on T2 and on post-gadolinium images. Safety checks and MR artifacts Box 1 demonstrates a rough safety check to assess MR compatibility of metallic objects before performing an MR scan. The reader is referred to more comprehensive sources for additional details [14]. MRI is associated with a number of artifacts that require recognition to avoid confusing them with normal anatomy or pathology (Box 2). Artifacts, such as those arising from metal clips or wrap around, are relatively common. Signal drop-out may arise as a consequence of low SNR that may have multiple potential etiologies. Conclusions Magnetic resonance angiographic techniques use inherent magnetization properties of tissues in combination with pharmacologic contrast agents such as gadolinium that shorten T1 relaxation time. The availability of powerful magnetic field gradients along with a variety of post-processing
Box 1. Artifacts from MRA Technical issues that may exaggerate stenosis • Long TE • Vessel not fully in 3D slab • Low spatial resolution Inadequate SNR (deterioration of image) • Insufficient inflow or Gd dosage too low • Bad Gd timing • Slices too thin • Field of view too small • Inadequate field strength/gradient performance Miscellaneous artifacts • • • •
Metal clips Wrap from arms Bright fat, hemorrhage/Gl contents Overlap on MIPs
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Box 2. Safety screening before MT examination Absolute contraindications • Pacemaker, automatic implantable cardioverter defibrillator (AICD) • Brain aneurysm clip • Metal in eye • Cochlear implant • Electronic implants No contraindications • Stents, coils, and filters (after 4 to 6 weeks of introduction) • Clips outside brain • Vascular access ports • Dental devices and materials • Orthopedic metal • Heart valves after 1983 algorithms make MRA possible. MRA is widely used in a variety of vessels, including aorta, carotids, renals, mesenteric, and peripherals. Performance of high-quality 3D contrast MRA requires appropriate understanding of MR methodologies, including the critical dependence of bolus timing with this technique and ways to optimize this. Additionally, recognition of artifacts and learning to avoid them is important. References [1] Nitz WR, Reimer P. Contrast mechanisms in MR imaging. Eur Radiol 1999;9:1032–46. [2] Prince MR, Grist TM, Debatin JF. 3D Contrast MR Angiography, 1st edition. Berlin: SpringerVerlag; 1999. [3] Wang Y, Lee HM, Khilnani NM, et al. Bolus-chase MR digital subtraction angiography in the lower extremity. Radiology 1998;207:263–9.
[4] Wang Y, Winchester PA, Khilnani NM, et al. Contrast-enhanced peripheral MR angiography from the abdominal aorta to the pedal arteries: combined dynamic two-dimensional and boluschase three-dimensional acquisitions. Invest Radiol 2001;36:170–7. [5] Owen RS, Carpenter JP, Baum RA, et al. Magnetic resonance imaging of angiographically occult runoff vessels in peripheral arterial occlusive disease. N Engl J Med 1992;326:1577–81. [6] Hany TF, Carroll TJ, Omary RA, et al. Aorta and runoff vessels: single-injection MR angiography with automated table movement compared with multiinjection time-resolved MR angiography– initial results. Radiology 2001;221:266–72. [7] Dong Q, Schoenberg SO, Carlos RC, et al. Diagnosis of renal vascular disease with MR angiography. Radiographics 1999;19:1535–54. [8] Prince MR. Renal MR angiography: a comprehensive approach. J Magn Reson Imaging 1998;8: 511–6. [9] Prince MR, Schoenberg SO, Ward JS, et al. Hemodynamically significant atherosclerotic renal artery stenosis: MR angiographic features. Radiology 1997;205:128–36. [10] Cloft HJ, Murphy KJ, Prince MR, et al. 3D gadolinium-enhanced MR angiography of the carotid arteries. Magn Reson Imaging 1996;14:593–600. [11] Fellner FA, Fellner C, Wutke R, et al. Fluoroscopically triggered contrast-enhanced 3D MR DSA and 3D time-of-flight turbo MRA of the carotid arteries: first clinical experiences in correlation with ultrasound, x-ray angiography, and endarterectomy findings. Magn Reson Imaging 2000;18:575–85. [12] Carroll TJ, Korosec FR, Petermann GM, et al. Carotid bifurcation: evaluation of time-resolved three-dimensional contrast-enhanced MR angiography. Radiology 2001;220:525–32. [13] Carr JC, Ma J, Desphande V, et al. High-resolution breath-hold contrast-enhanced MR angiography of the entire carotid circulation. Am J Roentgenol 2002;178:543–9. [14] Shellock FG, Kanal E. Magnetic resonance: bioeffects and safety. St. Louis: Mosby; 1998.