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937
Review
Article
MR Angiography Robert
R. Edelman,1
Heinrich
P. Mattle,1-2
Dennis
J. Atkinson,1’3
The capability for studying blood flow noninvasively with was recognized long before the implementation of the first MR imaging systems [1-3]. MR imaging quickly proved superior to CT for assessing blood vessels. However, early studies, which relied on the conventional spin-echo (SE) pulse sequence, had significant limitations. Flowing blood may produce complex signal patterns, depending on the flow velocity, direction, and profile, and these appearances may not be evaluated unambiguously on SE images [4]. The introduction of newer techniques such as two-dimensional (2-D) and threedimensional (3-0) gradient-echo (GRE) pulse sequences, flow compensation, and RF presaturation has vastly expanded MR’s capabilities for showing vessel patency and direction of flow, and for quantifying flow velocities and flow volumes [5, 6]. These techniques became the foundation for the field of MR angiography. In this article, technical and clinical developments in the field of MR angiography will be reviewed, with an emphasis on current and future clinical applications as well as practical limitations. MR
Flow Effects Contrast
and Techniques
for Manipulating
Flow
The process of creating an MR image involves the application of RF and gradient pulses. Fresh spins first entering the imaging volume have not been recently affected by RF pulses and are unsaturated; they therefore produce an intense signal. This effect, which is most pronounced in the entrance
and
Henri
slice, is called flow-related or paradoxical enhancement. A competing effect is that caused by the washout of flowing spins from the slice during the imaging process [7]. When images are obtained with an SE pulse sequence, spins must remain in the slice sufficiently long to be exposed to both the 90#{176} and 1 80#{176} RF pulses (i.e., for a time interval of at least Y2TE). With fast flow, washout effects tend to dominate, so that flowing blood appears dark. Washout effects can be accentuated by the use of thin slices and/or long TE; this is one method for obtaining “black-blood” images. Presaturation techniques, which incorporate one or more additional RF pulses prior to the pulse sequence, are also useful to produce black-blood images [8, 9]. The basic principle is that an extra RF pulse (typically near 90#{176}) can be applied outside the imaging volume to saturate inflowing spins without altering the signal intensity of stationary tissues within the imaging volume. The inflowing, presaturated spins then appear dark when imaged with the regular pulse sequence. The technique eliminates ghost artifacts from pulsatile flow and readily distinguishes thrombus from flowing blood. Flowing blood can be made to appear bright by the combination of the GRE pulse sequence and flow compensation. In the GRE sequence, the echo is refocused without a 180#{176} RF pulse simply by a reversal of the imaging gradients, so that stationary spins have no net phase shift at the echo time (TE) [10]. The absence of the 180#{176} pulse makes washout effects negligible. However, phase shifts produced by flow across the magnetic field gradients [ii] interfere with the
Received September 14, 1989; accepted after revision November 27, 1989. Department of Aadiology. Beth Israel Hospital. 330 Brookline Ave., Boston, MA 02215. Address reprint 2Department of Aadiology. New England Deaconess Hospital, 185 Pilgrim Ad., Boston, MA 02215. 3Siemens
Medical
Systems,
D#{233}partement de Aadiologie, AJR 154:937-946,
Iselin,
NJ 08830.
H#{244}pital Cantonal,
May 1990 0361 -803X/90/1
1700 Fribourg,
545-0937
Switzerland.
© American
Roentgen
M. Hoogewoud1’4
Aay Society
requests
to A. A. Edelman.
EDELMAN
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creation of bright blood GRE images. These phase shifts result in flow-related dephasing and signal loss [1 2]. In order to make the flowing spins appear brighter, flow compensation (also called gradient motion rephasing, gradient motion nulling, or motion artifact suppression technique) is applied [13, 1 4]. The pulse sequence is modified by the addition of one or more gradient pulses, which are precisely calibrated to eliminate phase shifts from both stationary and flowing spins. At least three gradient pulses are needed to correct for firstorder (velocity) phase shifts, and more pulses are needed for higher-order effects (e.g., acceleration, jerk). Given that the additional gradient pulses needed for higher-order flow compensation prolong the TE, there is little clinical benefit in applying flow compensation of higher than first order. The efficacy of flow compensation is improved by using a very short TE. This can be achieved by shifting the center of the readout period with respect to the peak of the echo (asymmetric sampling), at the expense of some loss of spatial resolution.
MR Angiography Abnormalities involving large blood vessels, such as abdominal aortic aneurysms, are usually well evaluated by using standard 2-D SE and GRE images. However, detailed evaluation of vascular anatomy in smaller vessels, such as the renal or carotid arteries, requires the application of a more sophisticated approach. In order to overcome the restrictions inherent to tomographic images for evaluating blood vessels crossing several image slices, a variety of projection imaging techniques have been developed. Similar to a conventional angiogram, a projection image displays some, or all, blood vessels coursing through a large thickness of the body. Two general approaches have been studied for producing such MR angiograms. The first approach involves acquiring a series of contiguous, thin-slice “bright-blood” images with a 3-D or 2-D GRE pulse sequence, and then postprocessing these images. The second method involves the direct acquisition of an image encompassing the blood vessels within a large thickness of the body. MR angiography may be further categorized according to the means for generating flow contrast. Techniques that rely on the inflow of unsaturated spins into the imaging volume, in order to make blood vessels appear brighter than stationary spins, are classified as timeof-flight or magnetization recovery. Techniques that rely on the application of gradient pulses, in order to produce different phase shifts for flowing and stationary spins, are called phase contrast.
3-0
Time-of-Flight
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then produced by phase-encoding the excited slab along the slice-selection axis, in addition to the standard in-plane phaseencoding process. The individual slices are postprocessed by using a maximum-intensity-projection (MIP) algorithm (Fig. 1). The computer projects a line (or ray) through the slices along a user-defined viewing angle. The brightest pixel along this line is then placed into the projection image; on GRE images, this pixel usually represents flowing blood. The procedure is repeated for each pixel in the projection image. In the final projection angiogram, blood vessels appear bright and stationary tissues appear dark. An advantage of this method is that, once the images have been acquired, they may be postprocessed along any viewing angle to eliminate vascular overlap and permit optimal assessment of stenoses.
Sequential
2-0 Acquisition
The 3-D GRE acquisition has significant drawbacks for the evaluation of veins and severely diseased arteries, because blood flowing slowly within the thick imaging volume becomes saturated and flow contrast is lost. Three-dimensional acquisitions are also particularly sensitive to motion such as respiration or swallowing. The sequential 2-D acquisition method helps to overcome these limitations [1 5]. A series of contiguous or overlapping 2-D flow-compensated GRE images are acquired sequentially, spanning the region of interest. The images are then postprocessed by using the MIP algorithm to produce projection images. Unlike a 3-D acquisition, which requires several minutes, the individual 2-D acquisitions can each be completed in just a few seconds. This is fast enough that breath-holding can be used to eliminate respiratory artifacts (Fig. 2). We have found that the efficiency of the sequential 2-D study is markedly improved by acquiring multiple slices simultaneously during each breath-hold. This can be done without compromising flow contrast if thin slices are used and they are separated by a gap of several times the slice thickness. For instance, typical scan variables for each breath-hold acquisition would be 51/i 0/30#{176}/i(TR/TE/flip an-
Acquisition
Three-dimensional GRE imaging allows a series of very thin (1-2 mm), contiguous slices to be obtained, with better signal to noise and shorter TE than is available by 2-D methods. The 3-D sequence differs from a 2-D sequence in one important respect. First, a relatively thick volume or “slab” of tissue (typically 32 mm or thicker), rather than a thin slice, is excited by the RF pulse. Thin, contiguous slices, or partitions, are
Fig. 1.-Schematic of maximum-intensity-projection algorithm, as applied to sequential 2-D study of renal arteries. Brightest pixels are extracted from slices, along a ray projected through images at user-defined viewing angle. These pixels are then combined into a projection image, which overcomes limitations inherent to tomographic images for displaying tortuous blood vessels.
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Fig. 2.-Sequential 2-D angiogram of chest in a normal subject. Scan variables: 30/10/30#{176}/i (TR/TE/ flip angle/NEX), one slice per breath-hold, 5-mm slice thickness, and i-mm overlap between sequential slices.
MR
ANGIOGRAPHY
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Fig. 3.-A, Effect of flip angle on flow contrast for 3-D time-of-flight MR angiogram. Large flip angles (e.g., 60#{176}, lower right) produce best flow contrast for inflowing spins within first few centimeters of carotid arteries. Smaller flip angles (e.g., 15#{176}, upper left) provide better visualization of vessels deep within imaging volume, such as intracranial arteries. (Courtesy of G. Laub.) B, Saturation effects are largely avoided by using an axial excitation. MR angiogram of normal carotid bifurcations, obtained with a 3-D flow-compensated gradient-echo acquisition, axial excitation, and coronal signal readout. Scan variables: 49/9/20#{176}/i (TR/TE/flip angle/NEX), 10cm-thick axial excitation volume, 64 partitions, 1.5-mm partition thickness, 256 x 192 acquisition matrix, 25-cm field of view, and 8-mm scan time. Excellent vascular detail was obtained with this method. Presaturation eliminated signal from jugular veins as well as wraparound along sliceselection direction.
gle/number of excitations [NEX]), 256 x 256 acquisition matrix, 38-cm field of view, and three slices acquired simultaneously with a slice thickness of 5 mm and 20-mm interslice gap. Compared with the 3-D method, angiograms acquired by using the sequential 2-D method consistently show better flow contrast for vessels with low or moderate flow velocities, because the thin slice thickness maximizes flow-related enhancement and minimizes in-plane saturation. Sequential 2-D acquisitions are better than 3-D acquisitions for showing abdominal and intracranial venous structures and small arteres. Conversely, rapid arterial flow in stationary body parts (e.g., in the circle of Willis) is rendered better by 3-D than 2D methods, because flow-related dephasing is reduced by the thinner slices (i.e., smaller voxel) and shorter TE available with 3-D imaging. With either 2-D or 3-D methods, the proper selection of flip angle is essential to maximize flow-related enhancement while minimizing saturation (Fig. 3A). With 2-D methods, satisfactory results are usually obtained with a TR of approximately 30 msec and a flip angle of approximately 30#{176}. With 3-0 methods, large flip angles (e.g., 60#{176}) produce the best flow contrast for inflowing spins within the first few centimeters of the imaging volume, but smaller flip angles (e.g., 20#{176}) provide better visualization of vessels deep within the imaging volume [16]. Also, thick imaging volumes (e.g., 100 mm) produce more saturation and worse flow contrast than relatively thinner volumes (e.g., 32 mm). A potential compromise is to perform sequential 3-0 acquisitions by using thin slabs and a
reduced number of partitions to preserve flow contrast while obtaining the benefits of a 3-0 sequence. Gd-DTPA enhancement can also be used to improve flow contrast, but its use entails certain drawbacks. First, tissues other than blood vessels (e.g., nasal mucosa, choroid plexus, pituitary gland) will enhance and be shown inappropriately on MR angiograms that use MIP postprocessing. Second, presaturation is rendered ineffective by the shortened Ti relaxation time of gadolinium-enhanced blood [17]. The choice of transmitter coil is also of significance. For instance, when the head coil is used as the transmitter for imaging of the carotid bifurcation, the RF excitation is limited to the head and upper neck. As a result, there is prominent flow-related enhancement within the carotid arteries. On the other hand, if the body coil is used as the transmitter for a sagittal or coronal acquisition, then the RF excitation will affect the great vessels within the chest, as well as within the neck. This results in saturation of the spins flowing into the carotid bifurcation, and loss of flow contrast. The problem may be overcome by use of an axial RF excitation through the neck, which does not affect the chest, followed by readout in the coronal or sagittal plane (Fig. 3B). Projection
Acquisition
Methods
Methods that use direct acquisition of projection images differ substantially from those already discussed in that the acquired images span a large thickness of the body. The acquisition strategy is to uniquely identify moving spins by
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EDELMAN
changing their appearance in the two images, while maintaining an identical appearance of stationary spins. By simply subtracting one image from the other, the signals from the background tissues are eliminated and only the blood vessels are shown. The basic principle of the technique is analogous to digital subtraction angiography; however, modifications to the pulse sequence substitute for the effect of an iodinated contrast agent. An early implementation of the projection acquisition method used cardiac gating to produce differences in vascular signal. Vascular signal is greater on SE images during slow diastolic flow than during rapid systolic flow. By subtracting a projection image gated to diastole from one gated to systole, Wedeen et al. [i 8] created MR angiograms of the peripheral arterial circulation. Better results are obtained if flow-sensitizing gradients are also used. One projection image is acquired with flow compensation to enhance vascular signal, and another with dephasing gradients to eliminate it. A limitation of this method is that it may be difficult to completely dephase very slow flow (e.g., in severely stenotic arteries), so that flow contrast may be limited. Dumoulin et al. [1 9, 20] proposed an alternative projection acquisition approach. Two projection images are acquired with bipolar flow-sensitizing gradients of opposite polarities, which produce phase shifts (0) of opposite sign for moving spins. Complex image subtraction then produces flow contrast proportional to 2 sin 0. One drawback of this phasecontrast method is aliasing: if the phase shift is more than 360#{176}, then the phase shift becomes ambiguous. For instance, rapid flow with a phase shift of 400#{176} may be interpreted identically to slower flow with a shift of 40#{176}. As a result of aliasing, there may be low signal and poor flow contrast despite brisk flow. Therefore, the flow-sensitizing gradients should be calibrated for the specific range of velocities that exists within the vessel of interest. The combination of flow-sensitizing gradients and complex image subtraction has also been incorporated into 3-D acquisitions (3-0 phase-contrast angiography) [21 ]. For small antenies and veins in stationary tissues (e.g., brain on hand), the method produces better flow contrast than the time-of-flight 3-0 methods described above [22]. However, the phasecontrast method requires 3-0 data to be acquired with multipIe permutations of the flow-sensitizing gradients, so that acquisition times are much longer than for the time-of-flight approach. Moreover, it requires much more intensive postprocessing of the data, and is sensitive to aliasing. The complex subtraction used for phase-contrast angiognaphy is also extremely sensitive to spurious phase shifts produced by gradient-induced eddy currents, so that use of properly calibrated eddy current compensation is essential. Active gradient shielding has proved helpful to achieve this. A number of other methods for MR angiognaphy have been proposed, although to date no substantial clinical results have been obtained with them. For instance, flow contrast can be produced in a pain of projection images by acquiring one image with, and one without, presatunation on preinvension [23, 24]. However, the effectiveness of presatunation for eliminating vascular signal decreases with distance from the
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presatunation slab, so that the method is not useful for largefield-of-view applications (e.g., imaging the aorta). Other proposed methods include line-scan angiognaphy [25] and a modified driven-equilibrium sequence [26].
Flow Measurement A variety of methods are available for measuring flow velocities. These methods fall into two groups, depending on whether they assess changes in proton phase or magnetization. Phase techniques rely on the fact that constant velocity flow along a magnetic field gradient produces shifts ‘in the phase of the MR signal that are proportional to the velocity [27]. The phase information is not apparent on standard images, which are reconstructed from the signal magnitude. However, phase-sensitive images can also be reconstructed. In these images, the pixel intensity is directly proportional to phase and, therefore, velocity. Phase imaging methods have been applied to large vessels such as the aorta [28] and pulmonary arteries, for instance, permitting cardiac shunts to be quantified, to separate the true and false lumens of an aortic dissection [29], on to distinguish thrombus from slow flow [30]. Time-of-flight methods rely on specific temporal and spatial changes in longitudinal magnetization rather than phase [31]. An example is bolus tracking. If a bolus of blood is “tagged” by a thin presaturation slab, then the motion of the bolus can be imaged oven the cardiac cycle by obtaining multiple data readouts with a cine GRE pulse sequence [32]. The tagged bolus appears dark, contrasting sharply with the adjoining bright flowing blood. Velocity is quantified simply as distance traveled divided by the time between tagging and data readouts. Replay of the images in a closed movie loop permits a visual appreciation of the flow velocities and profiles. Unlike the case of arterial flow, cardiac gating is not required for flow measurements in most veins, since venous flow is relatively steady. This permits chest and abdominal flow measurements to be completed within a breath-hold.
Clinical
Results
Despite the variety of methods now available for MR angiognaphy, there has been a dearth of clinical studies. Pending the performance of well-controlled studies at multiple institutions, applying standardized techniques to large numbers of subjects, any conclusions one may draw about the clinical utility of MR angiognaphy must be considered tentative.
Extracranial
Carotid
Circulation
Atherosclerosis affecting the extracnanial carotid circulation is a significant cause of thromboembolic stroke. The gold standard to assess atherosclerotic changes is contrast angiognaphy. Duplex sonography has proved to be an accurate, inexpensive screening technique for disease affecting the extracranial carotid. However, it provides incomplete plaque characterization, patent vessels may be falsely diagnosed as occluded, and it can evaluate the intracranial cerebral cm-
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Fig. 4.-A and B, Carotid artenogram (A) and 3-DMA angiogram (B) in a patient with moderate stenosis of proximal internal carotid artery. Scan variables: 40/8/15#{176}/i (TR/TE/flip angle/NEX), 40-mm 3-D slab thickness, and 32 partitions with 1.25-mm slice thickness. There is good correlation between the two images. However, MA angiogram exaggerates degree of stenosis. Ulceration (arrows).
A
culation only when combined with transcranial Doppler sonography. Masanyk et al. [33] have used time-of-flight 3-D acquisitions, postpnocessed by using the MIP algorithm, for studies of the carotid bifurcation (Fig. 4). MR angiognaphy correctly classified 21 of 22 stenoses and occlusions of the internal carotid artery. One problem was that lessen stenoses were sometimes ovengraded as severe stenoses. This error is produced by the presence of turbulent (i.e., chaotic) flow distal to the stenosis, which results in signal loss that is not entirely recovered by the application of flow compensation. The problem is ameliorated, but not eliminated, by the use of a very short TE (e.g., 7 msec). In addition, with the low flow velocities that can exist in severely stenotic arteries, flow contrast will be reduced by saturation effects as the blood flows within the imaging volume. Keller et al. [34] have applied sequential 2-0, rather than 3-0, acquisitions with very thin slices (e.g., nominal slice thickness of 1 mm) to reduce these saturation effects, with promising results. However, the signal-to-noise ratios of these images are poorer than those obtained by 3-D acquisitions. Both methods are also suboptimal for detecting plaque ulcerations, because the relative stasis of blood within these lesions fails to produce adequate flow contrast. Better evaluation of ulcerations might be obtamed by using more anatomic black-blood imaging methods. Because of its greater availability and lower cost, duplex sonognaphy remains the screening method of choice for carotid bifurcation disease, although MR angiognaphy may be useful for selected cases with technically inadequate or ambiguous sonography. In particular, we expect that MR will prove more accurate for differentiating a severely stenotic vessel from a thrombosed one. This distinction is important, because a stenotic vessel, unlike a thrombosed one, may be amenable to surgical treatment [35]. However, further study is needed to determine whether MR might obviate conventional angiography in this application. Intracranial
Vessels
Preliminary studies suggest a useful role in the evaluation
that MR angiography may have of a variety of cenebrovascular
B
disorders. One study of intracranial aneurysms, that used both SE imaging and MR angiography detected 17 of 19 aneurysms [36]. MR angiography increased the sensitivity for aneurysms, compared with SE images alone. However, there are several pitfalls in the use of MR angiognaphy for this diagnosis. MR angiognaphy fails to detect thrombosed aneurysms, as well as those containing very slow flow, and will underestimate the size of aneurysms containing turbulent flow. Moreover, substances having short Ti relaxation times such as extracellulan methemoglobin and proteinaceous solutions, which may be present in subarachnoid or intracerebral hemorrhages and in thrombosed vessels, can appear bright on MR angiognams, which use MIP postpnocessing. For optimal evaluation, it is therefore essential that both black-blood SE images and bright-blood angiognams be obtained (Fig. 5). In the setting of relatively modest clinical suspicion (e.g., family history of berry aneurysms involving the circle of Willis), MR may be useful for the initial imaging evaluation. However, one should note that the 89% accuracy reported in the study of Masaryk et al. [36] is inferior to the results with thin-section contrast-enhanced CT [37]. Also, MR should not, at the present stage of development, substitute for contrast angiography in patients with high clinical suspicion (e.g., evidence of subarachnoid hemorrhage). MR imaging, with conventional SE techniques, has proved to be a good means for detecting and characterizing intracranial arteniovenous malformations. Rapidly flowing blood appears dank, but may be impossible to differentiate from calcification; this differentiation is better made by MR angiognaphy [38, 39]. It has been shown that 3-0 MR angiognaphy delineates the nidus and major feeding vessels, whereas sequential 2-D MR angiognaphy better renders the draining veins (Fig. 6) [40]. Moreover, presaturation techniques allow the different vascular territories contributing to the malformation to be precisely mapped. In order to accomplish this, a presaturation slab is applied to a single feeding vessel, such as a middle cerebral artery, without affecting other major intracranial arteries. The presatunation eliminates signal only within that portion of the malformation supplied by the presaturated vessel. Thus, by using this technique of selective MR arteri-
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Fig. 5.-A, Giant aneurysm at top of basilar artery seen on sagittal 3-D angiogram. Methemoglobin or proteinaceous substances, as well as flowing spins, may appear bright on gradientecho images; therefore, clot can be mistaken for flow. B, SE MR image obtained with presaturation more accurately delineates extent of clot from open lumen of aneurysm. (Reprinted with permission from Edelman et al. [5].)
Fig. 6.-Left parietotemporal arteriovenous malformation. A, Conventional carotid angiogram. B, Axial 3-D MR angiogram. C, SE MR image with flow presaturation. Nidus is well seen
on both SE image
ography, it is not essential that the entire vascular tree be shown for functional information about the malformation to be determined. MR angiography can also be applied to the study of collatenal circulation in the cenebrovasculan system (Fig. 7) [41]. Currently, the only noninvasive means for demonstrating cross-flow through the circle of Willis is by using transcranial Doppler imaging. This technique is a useful bedside tool for the evaluation of stroke patients [42]. However, there are many possible pitfalls, especially in the assessment of the posterior circulation. On the other hand, MR angiography with time-of-flight or phase-contrast 3-D techniques shows vasculan anatomy but, as it is usually implemented, fails to provide functional information. Selective MR angiography with presaturation is an accurate means for showing origin and directionality of flow. Collateral flow on the presence of a fetal posterior circulation, which may not be apparent on standard MR angiognams, is readily shown by the selective method. MR venography of the cerebral sinuses and veins is also feasible [15]. For this purpose, sequential 2-0 MR angiography is performed with presatunation of the arterial inflow, so
and MA angiogram.
(Reprinted
with permission
from Edelman
et al. [40].)
that only veins are depicted. The effect of presatunation does not carry through to the veins, because the flowing spins nemagnetize during the few seconds of transit through the capillary circulation. This technique may prove useful for the evaluation of suspected sinus thrombosis and venous malfonmations. MR can also be applied to the measurement of intracranial venous flow, which is not possible by other noninvasive means. For instance, bolus tracking has been used to measure blood flow within the superior sagittal sinus, which might be an indicator of cortical blood flow [43]. Dynamic changes in cerebral blood flow with maneuvers such as hyperventilation are readily shown. In animals and humans, regional perfusion of the brain [44], heart [45], and kidneys [46] has also been assessed qualitatively by dynamic firstpass MR imaging with panamagnetic or superparamagnetic contrast agents, although quantitation is a more difficult task. Body
Angiography
Sequential the evaluation
breath-hold 2-0 acquisitions can be applied to of the vasculature within the chest and abdo-
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ANGIOGRAPHY
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Fig. 7.-A, Conventional arteriogram in patient with occlusion of left internal carotid artery shows collateral flow from right to left internal carotid artery territory over anterior communicating artery. B, Axial 2-D gradient-echo MA image, 30/10/ 30#{176}/i(TA/TE/flip angle/NEX), shows flow in both middle cerebral arteries. Information about origin of flow is not available from this image. c, Presaturation of right carotid artery eliminated signal in left middle cerebral artery, indicating origin of flow from right side. D, Presaturation of left carotid artery does not affect signal in right middle cerebral artery. (Reprinted with permission from Edelman et al. [41].)
men (Figs. 2 and 8A) [1 5]. Venograms of the hepatic and portal venous systems are created, without overlap from arteries, by applying presaturation to the distal thoracic aorta. Esophageal, gastric, and splenic vanices are demonstrated without regard to body habitus, a significant advantage compared with sonography (Fig. 8B). Patency of the main portal vein and the flow velocity and direction are quickly determined with MR by using bolus tracking (Figs. 8C and 8D) [47]. Projection acquisition techniques such as phase-contrast angiognaphy have also been applied to the study of the abdominal vasculature [48]. Although sonognaphy may remain as the initial technique for evaluation of patients with portal hypertension, the role of MR angiography is increasing. MR may be superior to CT in depicting abdominal aortic aneurysms because of its capability for showing the entire length of the lesion in a single image. However, the interpretation of complex signal intensities in regions of slow or turbulent flow is difficult. MR may also prove useful for the initial evaluation of patients with suspected renovascular hypertension (Fig. 9). In a prospective study of 25 patients with 55 renal arteries, MR angiography with the sequential 2-D approach had a sensitivity of 100% for detecting renal artery stenoses of moderate (50%) or more severe degree [49]. MR incorrectly ovengraded the degree of renal artery stenosis in four of 55 renal arteries (specificity = 92%). MR also
correctly determined the number of renal arteries in all cases. However, MR was not adequate for evaluation of the distal portions of the renal arteries. Aortic plaque, which appears dark on GRE images, is well shown. Perhaps of even greaten potential clinical value, MR angiognaphy has been used to quantify flow volumes in the renal veins, which allows the hemodynamic significance of renal artery stenoses to be assessed. This is not possible by other noninvasive means on conventional angiognaphy. Renal vein flow is nearly equal to renal blood flow. In 1 2 healthy subjects, side-to-side differences in renal vein flow were minimal. Howeven, in five patients with unilateral renal artery stenosis, a marked reduction in blood flow was shown on the side of the stenosis (Hoogewoud HM, Edelman RR, Mattle HP, et al., unpublished data). Further study is needed in this area. Less success has been achieved in studying the peripheral arterial circulation, and reports to date have been anecdotal. Difficulties include the need to obtain high spatial resolution over a large field of view and the presence of slow or turbulent flow in association with stenoses. Single-slice 2-0 GRE can be used to assess deep venous thrombosis [50], but MR faces stiff competition from noninvasive studies such as duplex sonognaphy. The capability for differentiating acute from chronic thrombosis and for demonstrating the presence of collateral circulation must also be developed. Application of
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Fig. 8.-A, Sequential 2-D venogram of upper abdomen in a normal subject. Scan variables for each breath-hold acquisition: 72/10/35#{176}/i (TR/ TE/flip angle/NEX), three slices per breath-hold, 5-mm slice thickness with 40-mm interslice gap, 256 x 192 acquisition matrix, and 38-cm field of view. The thickness of the projection image, created from multiple overlapping breath-hold acquisitions, is 120 mm. Presaturation slab (black stripe across top of image) above diaphragm eliminates signal from arterial blood flowing into abdomen. Inferior vena cava (v) and iliac veins, superior mesenteric vein (m) and small branches, renal veins (solid arrows), main portal vein (p) and its intrahepatic branches, and hepatic veins (arrowheads) are visualized. Splenic vein (open arrow) is not well shown because it is partially outside imaging volume. B, Sequential 2-D MA angiogram in patient with liver cirrhosis reveals massive gastric varices. Because arterial presaturation was not applied, there is overlap of aorta and portal venous system. C, Bolus tracking study of portal vein displays reversed flow. In order to eliminate vascular overlap, range of slices used for postprocessing was restricted to exclude aorta. Tagged bolus (arrow), which appears dark, is observed to move away from liver. D, Bolus tracking study of normal portal vein. Tagged bolus (arrow) is seen to move toward liver in sequential images. (Reprinted with permission from Edelman et al. [47].)
Fig. 9.-A and B, Sequential 2-D MR angiogram (A) (scan variables: 30/iO/30#{176}/i[TR/TE/ flip angle/NEX], one slice per breath-hold, 5-mm slice thickness, and i-mm overlap between sequentially acquired coronal slices) shows occlusion of left renal artery and correlates well with conventional angiogram (B). Distal portion of right renal artery is not optimally assessed in projection image because of current limitations of the technique. (Reprinted with permission from Kim et al. [49].)
MR angiography to the deep venous system is impeded by the phasic low-flow velocities, on stasis, present in these vessels. MR contrast agents such as Gd-DTPA, in conjunction with 2-D on 3-D acquisition methods and postprocessing by the MIP algorithm, might be useful in overcoming this problem, but would increase the cost and make the examination invasive.
MR angiography of the coronary arteries is, without question, the most challenging task for flow researchers, and may in fact prove to be a technical impossibility. The combination of the small size of the vessels (less than 5 mm diameter) with both cardiac and respiratory motion represents a daunting obstacle. Nonetheless, coronary arteries are occasionally visualized on standard gated SE and cine GRE studies [6,
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MR
ANGIOGRAPHY
51]. In order to produce MR angiograms of the native cononary arteries, one group has applied a technique by which two projection images are acquired, in one of which the aortic root has been preinverted [52]. In principle, the preinversion will affect only signal from blood washing into the coronary ostia, so that a subtraction image would show only the coronary arteries without signal from the ventricular cavities. To date, there have been no convincing results. Better success has been achieved in the study of coronary artery bypass grafts [53-55]. Cine GRE imaging has proved to be an accurate method for determining bypass graft patency, although the proper interpretation of these images requires considerable experience because of the complex courses of the grafts, and these tomographic images are not adequate for evaluating graft stenosis. Full acceptance of MR by cardiologists and cardiac surgeons for evaluation of bypass grafts will probably await the successful application of angiographic techniques.
Conclusions Within just a few years, the field of MR angiography has evolved from a haphazard probing of technical possibilities to a level where applications are undergoing clinical trials. At present, MR angiography should not be considered directly competitive with contrast angiognaphy because of the higher spatial resolution and more reliable depiction of vascular anatomy by the latter method. Nonetheless, MR angiography is often helpful as an adjunct to conventional MR imaging methods for improving the depiction of vascular anatomy and function. Preliminary studies suggest that MR angiography may be useful for the study of the portal venous system and other abdominal vessels, intracranial aneurysms and vascular malformations, cerebral venous and sinus thrombosis, and, in selected cases, for the evaluation of the carotid bifurcation. Further improvements will result from the implementation of shorten TEs, reconstruction schemes that can be applied to asymmetrically sampled data to improve spatial resolution [56], and optimized fast imaging techniques. With continued technical progress and the performance of carefully designed clinical studies, MR angiography will probably become a standard tool for the evaluation of vascular disorders. REFERENCES 1 . Hahn HL. Spin echoes. Phys Rev i950;80:580-594 2. Suryan G. Nuclear resonance in flowing liquids. Proc Indian Acad Sci (A] 195i;33: 107-111 3. Singer JR. NMA diffusion and flow measurements and an introduction to spin-phase graphing. J Phys [E] 1978;1 1 :281-291 4. Axel L. Blood flow effects in magnetic resonance. AJR 1984:143: 1157-1166 5. Edelman AR, Rubin JB, Buxton AR. Flow. In: Edelman AR, Hesselink JA, eds. Clinical magnetic resonance imaging. Philadelphia: Saunders, 1990 (in press) 6. Alfidi RJ, Masaryk TJ, Haacke EM, et al. MA angiography of peripheral, carotid, and coronary arteries. AJR 1987;149:1097-1109 7. Bradley WG, Waluch V, Lai K-S, et al. The appearance of rapidly flowing blood on MA images. AJR i984;143:1167-1174 8. Edelman AR, Atkinson DJ, Silver MS. FR000 pulses: a new method for elimination of motion, flow and wraparound artifact. Radiology 1988:166:231-236 9. Felmlee JP, Ehman AL. Spatial presaturation: a method for suppressing
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9. Felmlee JP, Ehman AL. Spatial presaturation: a method for suppressing flow artifacts and improving depiction of vascular anatomy in MAI. Radiology 1987;1 64:559-564 10. Frahm J, Haase A, Mattaei D. Rapid NMR imaging of dynamic processes using the FLASH technique. Magn Reson Med 1986;3:321 -327 1 1 . Singer JR. NMA diffusion and flow measurements and an introduction to spin-phase graphing. J Phys [E] i978;1 1 :281 -291 12. von Schulthess GK, Higgins CB. Blood flow imaging with MA: spin-phase phenomenon. Radiology 1985;157:687-695 1 3. Laub GA, Kaiser WA. MA angiography with gradient motion rephasing. J Comput Assist Tomogr 1988;12:377-382 1 4. Haacke EM, Lenz G. Improving MA image quality in the presence of motion by using rephasing gradients. AJR 1987:148:1251-1258 1 5. Edelman AR, Wentz KU, Mattle H, et al. Projection arteriography and venography: initial clinical results with MA. Radiology 1989:172:351-357 16. Auggieri PM, Laub GA, Masaryk TJ, Modic MT. Intracranial circulation: pulse-sequence considerations in three-dimensional (volume) MA angiography. Radiology i989;171 :785-791 17. Edelman AR, Siegel JB, Singer A, Dupuis K, Longmaid HE. Dynamic MA imaging of the liver with Gd-DTPA: initial clinical results. AJR i989;153:1213-1219 18. Wedeen VJ, Meuli RA, Edelman AR, et al. Projective imaging of pulsatile flow with magnetic resonance. Science i985;230:946-948 19. Dumoulin CL, Hart HA. MA angiography. Radiology 1986;61 :717-720 20. Dumoulin CL, Souza SP, Walker MF, Yoshitome E. Time-resolved MA angiography. Magn Reson Med i988;6:275-286 21 . Dumoulin CL, Souza SP, Walker MF, Wagle W. Three-dimensional phase contrast angiography. Magn Reson Med i989;9: 139-1 49 22. Chao PW, Goldberg H, Dumoulin CL, Wehrli FW. Comparison of time of flight versus phase contrast techniques: visualization of the intra- and extracerebral carotid artery. In: Book of abstracts: Society of Magnetic Resonance in Medicine 1989, vol. 1 . Berkeley, CA: Society of Magnetic Resonance in Medicine, i989:165 23. Dixon WT, Du LN, Faul DD, et al. Projection angiograms of blood labeled by adiabatic fast passage. Magn Reson Med 1986:3:454-462 24. Nishimura DG, Macovski A, Pauly JM. Considerations of MA angiography by selective inversion recovery. Magn Reson Med i988;7:472-484 25. Pauly J, Nishimura D, Macovski A. Line scan MA angiography. In: Book of abstracts: Society ofMagnetic Resonance in Medicine 1987, vol. 1 . Berkeley, CA: Society of Magnetic Resonance in Medicine, 1987:28 26. Pauly J, Nishimura D, Macovski A. Robust velocity selective excitation. In: Book of abstracts: Society of Magnetic Resonance in Medicine 1987, vol 1. Berkeley, CA: Society of Magnetic Resonance in Medicine, 1987:27 27. Wedeen VJ, Aosen BA, Chesler D, Brady TJ. MA velocity imaging by phase display. J Comput Assist Tomogr i985;9:530-536 28. Maier SE, Meier D, Boesiger P, Moser UT, Vieli A. Human abdominal aorta: comparative measurements of blood flow with MA imaging and multigated Doppler US. Radiology i989;1 71:487-492 29. Dinsmore RE, Wedeen VJ, Miller SW, et al. MAI of dissection of the aorta: recognition of the intimal tear and differential flow velocities. AJR i986;146: 1286-1 288 30. White EM, Edelman AA, Wedeen VJ, Brady TJ. Intravascular signal in MA imaging: use of phase display for differentiation of blood flow signal from intraluminal disease. Radiology i986;161 :245-249 31 . Wehrli FW, Shimakawa A, Gullberg GT, MacFall JR. Time-of-flight MA flow imaging: selective saturation recovery with gradient refocusing. Radiology i986;1 60:781 -785 32. Edelman AR, Mattle H, Kleefield J, Silver MS. Quantification of blood flow with dynamic MA imaging and presaturation bolus tracking. Radiology 1989:171 :551 -556 33. Masaryk TJ, Modic MT, Auggieri PM, et al. Three-dimensional (volume) gradient-echo imaging of the carotid bifurcation: preliminary clinical experience. Radiology i989;171 :801 -806 34. Keller PJ, Drayer BP, Fram EK, Williams KD, Dumoulin CL, Souza SP. MA angiography with two-dimensional acquisition and three-dimensional display: work in progress. Radiology i989;173:527-532 35. O’Leary DH, Mattle H, Potter JE. Atheromatous pseudo-occlusion of the intemal carotid artery: a review of 34 patients. Stroke i989;20: 1168-1173 36. Masaryk TJ, Modic MT. Ross JS, Auggieri P, VanDyke C, Tkach J. MR angiography of intracranial aneurysms (abstr). AJNR i989;10:893-894 37. Schmid UD, Steiger HJ, Huber P. Accuracy of high resolution computed tomography in direct diagnosis of cerebral aneurysms. Neuroradiology 1987:29:152-159
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Smith HJ, Strother CM, Kikuchi Y, et al. MA imaging in the management of supratentorial intracranial AVMs. AJNR 1988;9:225-235 Needell WM, Maravilla KR. MA flow imaging in vascular malformations using gradient recalled acquisitions. AJNR 1988:9:637-642 Edelman AR, Wentz KU, Mattle H, et al. Intracerebral arteriovenous malformations: evaluation with selective MA angiography and venography. Radiology 1989:173:831-837 Edelman AR, Mattle H, O’Reilly GV, Wentz KU, Liu C, Zhao B. Magnetic resonance imaging of flow dynamics in the circle of Willis. Stroke 1990:21 :56-65 Mattle H, Grolimund P. Huber P, Sturzenegger M, ZurbrUgg HA. Transcranial Doppler sonographic findings in middle cerebral artery disease. Arch Neurol 1988:45:289-295 Mattle H, Edelman AR, Aeis MA, Atkinson DJ. Flow quantification in the superior sagittal sinus using magnetic resonance. Neurology (in press) Rosen BA, Belliveau JW, Chien D. Perfusion imaging by nuclear magnetic resonance. Magn Reson Q i989;5:263-281 Atkinson DJ, Burstein D, Edelman AR. Evaluation of first-pass cardiac perfusion by ultrafast magnetic resonance imaging. Radiology (in press) Choyke PL, Frank JA, Girton ME, et al. Dynamic Gd-DTPA-enhanced MA imaging of the kidney: experimental results. Radiology i989;170:713-720 Edelman AR, Zhao B, Liu C, et al. Magnetic resonance angiography and flow velocity quantification in the portal venous system. AJR 1989; 153:755-760 Vock P, Terrier F, WegmUller H, Strauch E, Souza SP, Dumoulin CL. MA angiography of abdominal vessels. In: Book of abstracts: Society of Magnetic Resonance in Medicine 1989. Berkeley, CA: Society of Magnetic
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Resonance in Medicine, 1989:1012 Kim D, Edelman AR, Kent C, Porter D, SkilIman J. MA angiography renal arteries and abdominal aorta. Radiology (in press)
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Spritzer CE, Sussman 5K, Blinder AA, et al. DVT evaluation with limited flip angle gradient-refocused MAI: preliminary experience. Radiology i988;166:371-375 Paulin 5, von Schuithess GK, Fossel E, Krayenbuehl HP. MR imaging of the aortic root and proximal coronary arteries. AJR 1987;1 48: 665-670 Nishimura D, Macovski A, Pauly J. Coronary angiography by selective inversion recovery. In: Book of abstracts: Society of Magnetic Resonance in Medicine 1988. Berkeley, CA: Society of Magnetic Resonance in Medicine, 1988:726 Aubinstein Al, Askenase AD, Thickman D, et al. Magnetic resonance imaging to evaluate patency of aortocoronary bypass grafts. Circulation 1987:76:786-791 Jenkins JP, Love HG, Foster CJ, et al. Detection of coronary artery bypass graft patency as assessed by magnetic resonance imaging. Br J Radiol 1988:61:2-4 White AD, Pflugfelder PW, Upton MJ, Higgins CB. Coronary artery bypass grafts: evaluation of patency with cine MA imaging. AJR i988;1 50: 1271 -1 274 Haacke EM, Lindskog E, Un W. Half Fourier imaging: a partiallyphase constralned iterative reconstruction scheme and an evaluation of several fast reconstruction schemes (abstr). In: Book of abstracts: Society of Magnetic Resonance in Medicine 1989. Berkeley, CA: Society of Magnetic Resonance in Medicine, 1989:363
937
Review
Article
MR Angiography Robert
R. Edelman,1
Heinrich
P. Mattle,1-2
Dennis
J. Atkinson,1’3
The capability for studying blood flow noninvasively with was recognized long before the implementation of the first MR imaging systems [1-3]. MR imaging quickly proved superior to CT for assessing blood vessels. However, early studies, which relied on the conventional spin-echo (SE) pulse sequence, had significant limitations. Flowing blood may produce complex signal patterns, depending on the flow velocity, direction, and profile, and these appearances may not be evaluated unambiguously on SE images [4]. The introduction of newer techniques such as two-dimensional (2-D) and threedimensional (3-0) gradient-echo (GRE) pulse sequences, flow compensation, and RF presaturation has vastly expanded MR’s capabilities for showing vessel patency and direction of flow, and for quantifying flow velocities and flow volumes [5, 6]. These techniques became the foundation for the field of MR angiography. In this article, technical and clinical developments in the field of MR angiography will be reviewed, with an emphasis on current and future clinical applications as well as practical limitations. MR
Flow Effects Contrast
and Techniques
for Manipulating
Flow
The process of creating an MR image involves the application of RF and gradient pulses. Fresh spins first entering the imaging volume have not been recently affected by RF pulses and are unsaturated; they therefore produce an intense signal. This effect, which is most pronounced in the entrance
and
Henri
slice, is called flow-related or paradoxical enhancement. A competing effect is that caused by the washout of flowing spins from the slice during the imaging process [7]. When images are obtained with an SE pulse sequence, spins must remain in the slice sufficiently long to be exposed to both the 90#{176} and 1 80#{176} RF pulses (i.e., for a time interval of at least Y2TE). With fast flow, washout effects tend to dominate, so that flowing blood appears dark. Washout effects can be accentuated by the use of thin slices and/or long TE; this is one method for obtaining “black-blood” images. Presaturation techniques, which incorporate one or more additional RF pulses prior to the pulse sequence, are also useful to produce black-blood images [8, 9]. The basic principle is that an extra RF pulse (typically near 90#{176}) can be applied outside the imaging volume to saturate inflowing spins without altering the signal intensity of stationary tissues within the imaging volume. The inflowing, presaturated spins then appear dark when imaged with the regular pulse sequence. The technique eliminates ghost artifacts from pulsatile flow and readily distinguishes thrombus from flowing blood. Flowing blood can be made to appear bright by the combination of the GRE pulse sequence and flow compensation. In the GRE sequence, the echo is refocused without a 180#{176} RF pulse simply by a reversal of the imaging gradients, so that stationary spins have no net phase shift at the echo time (TE) [10]. The absence of the 180#{176} pulse makes washout effects negligible. However, phase shifts produced by flow across the magnetic field gradients [ii] interfere with the
Received September 14, 1989; accepted after revision November 27, 1989. Department of Aadiology. Beth Israel Hospital. 330 Brookline Ave., Boston, MA 02215. Address reprint 2Department of Aadiology. New England Deaconess Hospital, 185 Pilgrim Ad., Boston, MA 02215. 3Siemens
Medical
Systems,
D#{233}partement de Aadiologie, AJR 154:937-946,
Iselin,
NJ 08830.
H#{244}pital Cantonal,
May 1990 0361 -803X/90/1
1700 Fribourg,
545-0937
Switzerland.
© American
Roentgen
M. Hoogewoud1’4
Aay Society
requests
to A. A. Edelman.
EDELMAN
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creation of bright blood GRE images. These phase shifts result in flow-related dephasing and signal loss [1 2]. In order to make the flowing spins appear brighter, flow compensation (also called gradient motion rephasing, gradient motion nulling, or motion artifact suppression technique) is applied [13, 1 4]. The pulse sequence is modified by the addition of one or more gradient pulses, which are precisely calibrated to eliminate phase shifts from both stationary and flowing spins. At least three gradient pulses are needed to correct for firstorder (velocity) phase shifts, and more pulses are needed for higher-order effects (e.g., acceleration, jerk). Given that the additional gradient pulses needed for higher-order flow compensation prolong the TE, there is little clinical benefit in applying flow compensation of higher than first order. The efficacy of flow compensation is improved by using a very short TE. This can be achieved by shifting the center of the readout period with respect to the peak of the echo (asymmetric sampling), at the expense of some loss of spatial resolution.
MR Angiography Abnormalities involving large blood vessels, such as abdominal aortic aneurysms, are usually well evaluated by using standard 2-D SE and GRE images. However, detailed evaluation of vascular anatomy in smaller vessels, such as the renal or carotid arteries, requires the application of a more sophisticated approach. In order to overcome the restrictions inherent to tomographic images for evaluating blood vessels crossing several image slices, a variety of projection imaging techniques have been developed. Similar to a conventional angiogram, a projection image displays some, or all, blood vessels coursing through a large thickness of the body. Two general approaches have been studied for producing such MR angiograms. The first approach involves acquiring a series of contiguous, thin-slice “bright-blood” images with a 3-D or 2-D GRE pulse sequence, and then postprocessing these images. The second method involves the direct acquisition of an image encompassing the blood vessels within a large thickness of the body. MR angiography may be further categorized according to the means for generating flow contrast. Techniques that rely on the inflow of unsaturated spins into the imaging volume, in order to make blood vessels appear brighter than stationary spins, are classified as timeof-flight or magnetization recovery. Techniques that rely on the application of gradient pulses, in order to produce different phase shifts for flowing and stationary spins, are called phase contrast.
3-0
Time-of-Flight
ET AL.
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then produced by phase-encoding the excited slab along the slice-selection axis, in addition to the standard in-plane phaseencoding process. The individual slices are postprocessed by using a maximum-intensity-projection (MIP) algorithm (Fig. 1). The computer projects a line (or ray) through the slices along a user-defined viewing angle. The brightest pixel along this line is then placed into the projection image; on GRE images, this pixel usually represents flowing blood. The procedure is repeated for each pixel in the projection image. In the final projection angiogram, blood vessels appear bright and stationary tissues appear dark. An advantage of this method is that, once the images have been acquired, they may be postprocessed along any viewing angle to eliminate vascular overlap and permit optimal assessment of stenoses.
Sequential
2-0 Acquisition
The 3-D GRE acquisition has significant drawbacks for the evaluation of veins and severely diseased arteries, because blood flowing slowly within the thick imaging volume becomes saturated and flow contrast is lost. Three-dimensional acquisitions are also particularly sensitive to motion such as respiration or swallowing. The sequential 2-D acquisition method helps to overcome these limitations [1 5]. A series of contiguous or overlapping 2-D flow-compensated GRE images are acquired sequentially, spanning the region of interest. The images are then postprocessed by using the MIP algorithm to produce projection images. Unlike a 3-D acquisition, which requires several minutes, the individual 2-D acquisitions can each be completed in just a few seconds. This is fast enough that breath-holding can be used to eliminate respiratory artifacts (Fig. 2). We have found that the efficiency of the sequential 2-D study is markedly improved by acquiring multiple slices simultaneously during each breath-hold. This can be done without compromising flow contrast if thin slices are used and they are separated by a gap of several times the slice thickness. For instance, typical scan variables for each breath-hold acquisition would be 51/i 0/30#{176}/i(TR/TE/flip an-
Acquisition
Three-dimensional GRE imaging allows a series of very thin (1-2 mm), contiguous slices to be obtained, with better signal to noise and shorter TE than is available by 2-D methods. The 3-D sequence differs from a 2-D sequence in one important respect. First, a relatively thick volume or “slab” of tissue (typically 32 mm or thicker), rather than a thin slice, is excited by the RF pulse. Thin, contiguous slices, or partitions, are
Fig. 1.-Schematic of maximum-intensity-projection algorithm, as applied to sequential 2-D study of renal arteries. Brightest pixels are extracted from slices, along a ray projected through images at user-defined viewing angle. These pixels are then combined into a projection image, which overcomes limitations inherent to tomographic images for displaying tortuous blood vessels.
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AJR:154,
May 1990
Fig. 2.-Sequential 2-D angiogram of chest in a normal subject. Scan variables: 30/10/30#{176}/i (TR/TE/ flip angle/NEX), one slice per breath-hold, 5-mm slice thickness, and i-mm overlap between sequential slices.
MR
ANGIOGRAPHY
939
Fig. 3.-A, Effect of flip angle on flow contrast for 3-D time-of-flight MR angiogram. Large flip angles (e.g., 60#{176}, lower right) produce best flow contrast for inflowing spins within first few centimeters of carotid arteries. Smaller flip angles (e.g., 15#{176}, upper left) provide better visualization of vessels deep within imaging volume, such as intracranial arteries. (Courtesy of G. Laub.) B, Saturation effects are largely avoided by using an axial excitation. MR angiogram of normal carotid bifurcations, obtained with a 3-D flow-compensated gradient-echo acquisition, axial excitation, and coronal signal readout. Scan variables: 49/9/20#{176}/i (TR/TE/flip angle/NEX), 10cm-thick axial excitation volume, 64 partitions, 1.5-mm partition thickness, 256 x 192 acquisition matrix, 25-cm field of view, and 8-mm scan time. Excellent vascular detail was obtained with this method. Presaturation eliminated signal from jugular veins as well as wraparound along sliceselection direction.
gle/number of excitations [NEX]), 256 x 256 acquisition matrix, 38-cm field of view, and three slices acquired simultaneously with a slice thickness of 5 mm and 20-mm interslice gap. Compared with the 3-D method, angiograms acquired by using the sequential 2-D method consistently show better flow contrast for vessels with low or moderate flow velocities, because the thin slice thickness maximizes flow-related enhancement and minimizes in-plane saturation. Sequential 2-D acquisitions are better than 3-D acquisitions for showing abdominal and intracranial venous structures and small arteres. Conversely, rapid arterial flow in stationary body parts (e.g., in the circle of Willis) is rendered better by 3-D than 2D methods, because flow-related dephasing is reduced by the thinner slices (i.e., smaller voxel) and shorter TE available with 3-D imaging. With either 2-D or 3-D methods, the proper selection of flip angle is essential to maximize flow-related enhancement while minimizing saturation (Fig. 3A). With 2-D methods, satisfactory results are usually obtained with a TR of approximately 30 msec and a flip angle of approximately 30#{176}. With 3-0 methods, large flip angles (e.g., 60#{176}) produce the best flow contrast for inflowing spins within the first few centimeters of the imaging volume, but smaller flip angles (e.g., 20#{176}) provide better visualization of vessels deep within the imaging volume [16]. Also, thick imaging volumes (e.g., 100 mm) produce more saturation and worse flow contrast than relatively thinner volumes (e.g., 32 mm). A potential compromise is to perform sequential 3-0 acquisitions by using thin slabs and a
reduced number of partitions to preserve flow contrast while obtaining the benefits of a 3-0 sequence. Gd-DTPA enhancement can also be used to improve flow contrast, but its use entails certain drawbacks. First, tissues other than blood vessels (e.g., nasal mucosa, choroid plexus, pituitary gland) will enhance and be shown inappropriately on MR angiograms that use MIP postprocessing. Second, presaturation is rendered ineffective by the shortened Ti relaxation time of gadolinium-enhanced blood [17]. The choice of transmitter coil is also of significance. For instance, when the head coil is used as the transmitter for imaging of the carotid bifurcation, the RF excitation is limited to the head and upper neck. As a result, there is prominent flow-related enhancement within the carotid arteries. On the other hand, if the body coil is used as the transmitter for a sagittal or coronal acquisition, then the RF excitation will affect the great vessels within the chest, as well as within the neck. This results in saturation of the spins flowing into the carotid bifurcation, and loss of flow contrast. The problem may be overcome by use of an axial RF excitation through the neck, which does not affect the chest, followed by readout in the coronal or sagittal plane (Fig. 3B). Projection
Acquisition
Methods
Methods that use direct acquisition of projection images differ substantially from those already discussed in that the acquired images span a large thickness of the body. The acquisition strategy is to uniquely identify moving spins by
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940
EDELMAN
changing their appearance in the two images, while maintaining an identical appearance of stationary spins. By simply subtracting one image from the other, the signals from the background tissues are eliminated and only the blood vessels are shown. The basic principle of the technique is analogous to digital subtraction angiography; however, modifications to the pulse sequence substitute for the effect of an iodinated contrast agent. An early implementation of the projection acquisition method used cardiac gating to produce differences in vascular signal. Vascular signal is greater on SE images during slow diastolic flow than during rapid systolic flow. By subtracting a projection image gated to diastole from one gated to systole, Wedeen et al. [i 8] created MR angiograms of the peripheral arterial circulation. Better results are obtained if flow-sensitizing gradients are also used. One projection image is acquired with flow compensation to enhance vascular signal, and another with dephasing gradients to eliminate it. A limitation of this method is that it may be difficult to completely dephase very slow flow (e.g., in severely stenotic arteries), so that flow contrast may be limited. Dumoulin et al. [1 9, 20] proposed an alternative projection acquisition approach. Two projection images are acquired with bipolar flow-sensitizing gradients of opposite polarities, which produce phase shifts (0) of opposite sign for moving spins. Complex image subtraction then produces flow contrast proportional to 2 sin 0. One drawback of this phasecontrast method is aliasing: if the phase shift is more than 360#{176}, then the phase shift becomes ambiguous. For instance, rapid flow with a phase shift of 400#{176} may be interpreted identically to slower flow with a shift of 40#{176}. As a result of aliasing, there may be low signal and poor flow contrast despite brisk flow. Therefore, the flow-sensitizing gradients should be calibrated for the specific range of velocities that exists within the vessel of interest. The combination of flow-sensitizing gradients and complex image subtraction has also been incorporated into 3-D acquisitions (3-0 phase-contrast angiography) [21 ]. For small antenies and veins in stationary tissues (e.g., brain on hand), the method produces better flow contrast than the time-of-flight 3-0 methods described above [22]. However, the phasecontrast method requires 3-0 data to be acquired with multipIe permutations of the flow-sensitizing gradients, so that acquisition times are much longer than for the time-of-flight approach. Moreover, it requires much more intensive postprocessing of the data, and is sensitive to aliasing. The complex subtraction used for phase-contrast angiognaphy is also extremely sensitive to spurious phase shifts produced by gradient-induced eddy currents, so that use of properly calibrated eddy current compensation is essential. Active gradient shielding has proved helpful to achieve this. A number of other methods for MR angiognaphy have been proposed, although to date no substantial clinical results have been obtained with them. For instance, flow contrast can be produced in a pain of projection images by acquiring one image with, and one without, presatunation on preinvension [23, 24]. However, the effectiveness of presatunation for eliminating vascular signal decreases with distance from the
ET AL.
AJA:154,
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presatunation slab, so that the method is not useful for largefield-of-view applications (e.g., imaging the aorta). Other proposed methods include line-scan angiognaphy [25] and a modified driven-equilibrium sequence [26].
Flow Measurement A variety of methods are available for measuring flow velocities. These methods fall into two groups, depending on whether they assess changes in proton phase or magnetization. Phase techniques rely on the fact that constant velocity flow along a magnetic field gradient produces shifts ‘in the phase of the MR signal that are proportional to the velocity [27]. The phase information is not apparent on standard images, which are reconstructed from the signal magnitude. However, phase-sensitive images can also be reconstructed. In these images, the pixel intensity is directly proportional to phase and, therefore, velocity. Phase imaging methods have been applied to large vessels such as the aorta [28] and pulmonary arteries, for instance, permitting cardiac shunts to be quantified, to separate the true and false lumens of an aortic dissection [29], on to distinguish thrombus from slow flow [30]. Time-of-flight methods rely on specific temporal and spatial changes in longitudinal magnetization rather than phase [31]. An example is bolus tracking. If a bolus of blood is “tagged” by a thin presaturation slab, then the motion of the bolus can be imaged oven the cardiac cycle by obtaining multiple data readouts with a cine GRE pulse sequence [32]. The tagged bolus appears dark, contrasting sharply with the adjoining bright flowing blood. Velocity is quantified simply as distance traveled divided by the time between tagging and data readouts. Replay of the images in a closed movie loop permits a visual appreciation of the flow velocities and profiles. Unlike the case of arterial flow, cardiac gating is not required for flow measurements in most veins, since venous flow is relatively steady. This permits chest and abdominal flow measurements to be completed within a breath-hold.
Clinical
Results
Despite the variety of methods now available for MR angiognaphy, there has been a dearth of clinical studies. Pending the performance of well-controlled studies at multiple institutions, applying standardized techniques to large numbers of subjects, any conclusions one may draw about the clinical utility of MR angiognaphy must be considered tentative.
Extracranial
Carotid
Circulation
Atherosclerosis affecting the extracnanial carotid circulation is a significant cause of thromboembolic stroke. The gold standard to assess atherosclerotic changes is contrast angiognaphy. Duplex sonography has proved to be an accurate, inexpensive screening technique for disease affecting the extracranial carotid. However, it provides incomplete plaque characterization, patent vessels may be falsely diagnosed as occluded, and it can evaluate the intracranial cerebral cm-
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AJA:154,
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ANGIOGRAPHY
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Fig. 4.-A and B, Carotid artenogram (A) and 3-DMA angiogram (B) in a patient with moderate stenosis of proximal internal carotid artery. Scan variables: 40/8/15#{176}/i (TR/TE/flip angle/NEX), 40-mm 3-D slab thickness, and 32 partitions with 1.25-mm slice thickness. There is good correlation between the two images. However, MA angiogram exaggerates degree of stenosis. Ulceration (arrows).
A
culation only when combined with transcranial Doppler sonography. Masanyk et al. [33] have used time-of-flight 3-D acquisitions, postpnocessed by using the MIP algorithm, for studies of the carotid bifurcation (Fig. 4). MR angiognaphy correctly classified 21 of 22 stenoses and occlusions of the internal carotid artery. One problem was that lessen stenoses were sometimes ovengraded as severe stenoses. This error is produced by the presence of turbulent (i.e., chaotic) flow distal to the stenosis, which results in signal loss that is not entirely recovered by the application of flow compensation. The problem is ameliorated, but not eliminated, by the use of a very short TE (e.g., 7 msec). In addition, with the low flow velocities that can exist in severely stenotic arteries, flow contrast will be reduced by saturation effects as the blood flows within the imaging volume. Keller et al. [34] have applied sequential 2-0, rather than 3-0, acquisitions with very thin slices (e.g., nominal slice thickness of 1 mm) to reduce these saturation effects, with promising results. However, the signal-to-noise ratios of these images are poorer than those obtained by 3-D acquisitions. Both methods are also suboptimal for detecting plaque ulcerations, because the relative stasis of blood within these lesions fails to produce adequate flow contrast. Better evaluation of ulcerations might be obtamed by using more anatomic black-blood imaging methods. Because of its greater availability and lower cost, duplex sonognaphy remains the screening method of choice for carotid bifurcation disease, although MR angiognaphy may be useful for selected cases with technically inadequate or ambiguous sonography. In particular, we expect that MR will prove more accurate for differentiating a severely stenotic vessel from a thrombosed one. This distinction is important, because a stenotic vessel, unlike a thrombosed one, may be amenable to surgical treatment [35]. However, further study is needed to determine whether MR might obviate conventional angiography in this application. Intracranial
Vessels
Preliminary studies suggest a useful role in the evaluation
that MR angiography may have of a variety of cenebrovascular
B
disorders. One study of intracranial aneurysms, that used both SE imaging and MR angiography detected 17 of 19 aneurysms [36]. MR angiography increased the sensitivity for aneurysms, compared with SE images alone. However, there are several pitfalls in the use of MR angiognaphy for this diagnosis. MR angiognaphy fails to detect thrombosed aneurysms, as well as those containing very slow flow, and will underestimate the size of aneurysms containing turbulent flow. Moreover, substances having short Ti relaxation times such as extracellulan methemoglobin and proteinaceous solutions, which may be present in subarachnoid or intracerebral hemorrhages and in thrombosed vessels, can appear bright on MR angiognams, which use MIP postpnocessing. For optimal evaluation, it is therefore essential that both black-blood SE images and bright-blood angiognams be obtained (Fig. 5). In the setting of relatively modest clinical suspicion (e.g., family history of berry aneurysms involving the circle of Willis), MR may be useful for the initial imaging evaluation. However, one should note that the 89% accuracy reported in the study of Masaryk et al. [36] is inferior to the results with thin-section contrast-enhanced CT [37]. Also, MR should not, at the present stage of development, substitute for contrast angiography in patients with high clinical suspicion (e.g., evidence of subarachnoid hemorrhage). MR imaging, with conventional SE techniques, has proved to be a good means for detecting and characterizing intracranial arteniovenous malformations. Rapidly flowing blood appears dank, but may be impossible to differentiate from calcification; this differentiation is better made by MR angiognaphy [38, 39]. It has been shown that 3-0 MR angiognaphy delineates the nidus and major feeding vessels, whereas sequential 2-D MR angiognaphy better renders the draining veins (Fig. 6) [40]. Moreover, presaturation techniques allow the different vascular territories contributing to the malformation to be precisely mapped. In order to accomplish this, a presaturation slab is applied to a single feeding vessel, such as a middle cerebral artery, without affecting other major intracranial arteries. The presatunation eliminates signal only within that portion of the malformation supplied by the presaturated vessel. Thus, by using this technique of selective MR arteri-
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Fig. 5.-A, Giant aneurysm at top of basilar artery seen on sagittal 3-D angiogram. Methemoglobin or proteinaceous substances, as well as flowing spins, may appear bright on gradientecho images; therefore, clot can be mistaken for flow. B, SE MR image obtained with presaturation more accurately delineates extent of clot from open lumen of aneurysm. (Reprinted with permission from Edelman et al. [5].)
Fig. 6.-Left parietotemporal arteriovenous malformation. A, Conventional carotid angiogram. B, Axial 3-D MR angiogram. C, SE MR image with flow presaturation. Nidus is well seen
on both SE image
ography, it is not essential that the entire vascular tree be shown for functional information about the malformation to be determined. MR angiography can also be applied to the study of collatenal circulation in the cenebrovasculan system (Fig. 7) [41]. Currently, the only noninvasive means for demonstrating cross-flow through the circle of Willis is by using transcranial Doppler imaging. This technique is a useful bedside tool for the evaluation of stroke patients [42]. However, there are many possible pitfalls, especially in the assessment of the posterior circulation. On the other hand, MR angiography with time-of-flight or phase-contrast 3-D techniques shows vasculan anatomy but, as it is usually implemented, fails to provide functional information. Selective MR angiography with presaturation is an accurate means for showing origin and directionality of flow. Collateral flow on the presence of a fetal posterior circulation, which may not be apparent on standard MR angiognams, is readily shown by the selective method. MR venography of the cerebral sinuses and veins is also feasible [15]. For this purpose, sequential 2-0 MR angiography is performed with presatunation of the arterial inflow, so
and MA angiogram.
(Reprinted
with permission
from Edelman
et al. [40].)
that only veins are depicted. The effect of presatunation does not carry through to the veins, because the flowing spins nemagnetize during the few seconds of transit through the capillary circulation. This technique may prove useful for the evaluation of suspected sinus thrombosis and venous malfonmations. MR can also be applied to the measurement of intracranial venous flow, which is not possible by other noninvasive means. For instance, bolus tracking has been used to measure blood flow within the superior sagittal sinus, which might be an indicator of cortical blood flow [43]. Dynamic changes in cerebral blood flow with maneuvers such as hyperventilation are readily shown. In animals and humans, regional perfusion of the brain [44], heart [45], and kidneys [46] has also been assessed qualitatively by dynamic firstpass MR imaging with panamagnetic or superparamagnetic contrast agents, although quantitation is a more difficult task. Body
Angiography
Sequential the evaluation
breath-hold 2-0 acquisitions can be applied to of the vasculature within the chest and abdo-
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Fig. 7.-A, Conventional arteriogram in patient with occlusion of left internal carotid artery shows collateral flow from right to left internal carotid artery territory over anterior communicating artery. B, Axial 2-D gradient-echo MA image, 30/10/ 30#{176}/i(TA/TE/flip angle/NEX), shows flow in both middle cerebral arteries. Information about origin of flow is not available from this image. c, Presaturation of right carotid artery eliminated signal in left middle cerebral artery, indicating origin of flow from right side. D, Presaturation of left carotid artery does not affect signal in right middle cerebral artery. (Reprinted with permission from Edelman et al. [41].)
men (Figs. 2 and 8A) [1 5]. Venograms of the hepatic and portal venous systems are created, without overlap from arteries, by applying presaturation to the distal thoracic aorta. Esophageal, gastric, and splenic vanices are demonstrated without regard to body habitus, a significant advantage compared with sonography (Fig. 8B). Patency of the main portal vein and the flow velocity and direction are quickly determined with MR by using bolus tracking (Figs. 8C and 8D) [47]. Projection acquisition techniques such as phase-contrast angiognaphy have also been applied to the study of the abdominal vasculature [48]. Although sonognaphy may remain as the initial technique for evaluation of patients with portal hypertension, the role of MR angiography is increasing. MR may be superior to CT in depicting abdominal aortic aneurysms because of its capability for showing the entire length of the lesion in a single image. However, the interpretation of complex signal intensities in regions of slow or turbulent flow is difficult. MR may also prove useful for the initial evaluation of patients with suspected renovascular hypertension (Fig. 9). In a prospective study of 25 patients with 55 renal arteries, MR angiography with the sequential 2-D approach had a sensitivity of 100% for detecting renal artery stenoses of moderate (50%) or more severe degree [49]. MR incorrectly ovengraded the degree of renal artery stenosis in four of 55 renal arteries (specificity = 92%). MR also
correctly determined the number of renal arteries in all cases. However, MR was not adequate for evaluation of the distal portions of the renal arteries. Aortic plaque, which appears dark on GRE images, is well shown. Perhaps of even greaten potential clinical value, MR angiognaphy has been used to quantify flow volumes in the renal veins, which allows the hemodynamic significance of renal artery stenoses to be assessed. This is not possible by other noninvasive means on conventional angiognaphy. Renal vein flow is nearly equal to renal blood flow. In 1 2 healthy subjects, side-to-side differences in renal vein flow were minimal. Howeven, in five patients with unilateral renal artery stenosis, a marked reduction in blood flow was shown on the side of the stenosis (Hoogewoud HM, Edelman RR, Mattle HP, et al., unpublished data). Further study is needed in this area. Less success has been achieved in studying the peripheral arterial circulation, and reports to date have been anecdotal. Difficulties include the need to obtain high spatial resolution over a large field of view and the presence of slow or turbulent flow in association with stenoses. Single-slice 2-0 GRE can be used to assess deep venous thrombosis [50], but MR faces stiff competition from noninvasive studies such as duplex sonognaphy. The capability for differentiating acute from chronic thrombosis and for demonstrating the presence of collateral circulation must also be developed. Application of
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Fig. 8.-A, Sequential 2-D venogram of upper abdomen in a normal subject. Scan variables for each breath-hold acquisition: 72/10/35#{176}/i (TR/ TE/flip angle/NEX), three slices per breath-hold, 5-mm slice thickness with 40-mm interslice gap, 256 x 192 acquisition matrix, and 38-cm field of view. The thickness of the projection image, created from multiple overlapping breath-hold acquisitions, is 120 mm. Presaturation slab (black stripe across top of image) above diaphragm eliminates signal from arterial blood flowing into abdomen. Inferior vena cava (v) and iliac veins, superior mesenteric vein (m) and small branches, renal veins (solid arrows), main portal vein (p) and its intrahepatic branches, and hepatic veins (arrowheads) are visualized. Splenic vein (open arrow) is not well shown because it is partially outside imaging volume. B, Sequential 2-D MA angiogram in patient with liver cirrhosis reveals massive gastric varices. Because arterial presaturation was not applied, there is overlap of aorta and portal venous system. C, Bolus tracking study of portal vein displays reversed flow. In order to eliminate vascular overlap, range of slices used for postprocessing was restricted to exclude aorta. Tagged bolus (arrow), which appears dark, is observed to move away from liver. D, Bolus tracking study of normal portal vein. Tagged bolus (arrow) is seen to move toward liver in sequential images. (Reprinted with permission from Edelman et al. [47].)
Fig. 9.-A and B, Sequential 2-D MR angiogram (A) (scan variables: 30/iO/30#{176}/i[TR/TE/ flip angle/NEX], one slice per breath-hold, 5-mm slice thickness, and i-mm overlap between sequentially acquired coronal slices) shows occlusion of left renal artery and correlates well with conventional angiogram (B). Distal portion of right renal artery is not optimally assessed in projection image because of current limitations of the technique. (Reprinted with permission from Kim et al. [49].)
MR angiography to the deep venous system is impeded by the phasic low-flow velocities, on stasis, present in these vessels. MR contrast agents such as Gd-DTPA, in conjunction with 2-D on 3-D acquisition methods and postprocessing by the MIP algorithm, might be useful in overcoming this problem, but would increase the cost and make the examination invasive.
MR angiography of the coronary arteries is, without question, the most challenging task for flow researchers, and may in fact prove to be a technical impossibility. The combination of the small size of the vessels (less than 5 mm diameter) with both cardiac and respiratory motion represents a daunting obstacle. Nonetheless, coronary arteries are occasionally visualized on standard gated SE and cine GRE studies [6,
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ANGIOGRAPHY
51]. In order to produce MR angiograms of the native cononary arteries, one group has applied a technique by which two projection images are acquired, in one of which the aortic root has been preinverted [52]. In principle, the preinversion will affect only signal from blood washing into the coronary ostia, so that a subtraction image would show only the coronary arteries without signal from the ventricular cavities. To date, there have been no convincing results. Better success has been achieved in the study of coronary artery bypass grafts [53-55]. Cine GRE imaging has proved to be an accurate method for determining bypass graft patency, although the proper interpretation of these images requires considerable experience because of the complex courses of the grafts, and these tomographic images are not adequate for evaluating graft stenosis. Full acceptance of MR by cardiologists and cardiac surgeons for evaluation of bypass grafts will probably await the successful application of angiographic techniques.
Conclusions Within just a few years, the field of MR angiography has evolved from a haphazard probing of technical possibilities to a level where applications are undergoing clinical trials. At present, MR angiography should not be considered directly competitive with contrast angiognaphy because of the higher spatial resolution and more reliable depiction of vascular anatomy by the latter method. Nonetheless, MR angiography is often helpful as an adjunct to conventional MR imaging methods for improving the depiction of vascular anatomy and function. Preliminary studies suggest that MR angiography may be useful for the study of the portal venous system and other abdominal vessels, intracranial aneurysms and vascular malformations, cerebral venous and sinus thrombosis, and, in selected cases, for the evaluation of the carotid bifurcation. Further improvements will result from the implementation of shorten TEs, reconstruction schemes that can be applied to asymmetrically sampled data to improve spatial resolution [56], and optimized fast imaging techniques. With continued technical progress and the performance of carefully designed clinical studies, MR angiography will probably become a standard tool for the evaluation of vascular disorders. REFERENCES 1 . Hahn HL. Spin echoes. Phys Rev i950;80:580-594 2. Suryan G. Nuclear resonance in flowing liquids. Proc Indian Acad Sci (A] 195i;33: 107-111 3. Singer JR. NMA diffusion and flow measurements and an introduction to spin-phase graphing. J Phys [E] 1978;1 1 :281-291 4. Axel L. Blood flow effects in magnetic resonance. AJR 1984:143: 1157-1166 5. Edelman AR, Rubin JB, Buxton AR. Flow. In: Edelman AR, Hesselink JA, eds. Clinical magnetic resonance imaging. Philadelphia: Saunders, 1990 (in press) 6. Alfidi RJ, Masaryk TJ, Haacke EM, et al. MA angiography of peripheral, carotid, and coronary arteries. AJR 1987;149:1097-1109 7. Bradley WG, Waluch V, Lai K-S, et al. The appearance of rapidly flowing blood on MA images. AJR i984;143:1167-1174 8. Edelman AR, Atkinson DJ, Silver MS. FR000 pulses: a new method for elimination of motion, flow and wraparound artifact. Radiology 1988:166:231-236 9. Felmlee JP, Ehman AL. Spatial presaturation: a method for suppressing
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