1

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Review Article

MR Angiography: Present and Future

Robert R. Edelman1

MR angiography is a rapidly evolving technique for noninva- blood flows out of the plane of section in the time interval
sive vascular imaging [1J. Since 1985, when it was first shown between successive RF pulses, the result is an absence of
to be clinically feasible [2J, the imaging techniques and hard- signal, called a flow void. The flow void can be emphasized
ware used for MR angiography have greatly improved. No by using a thin section or long echo time (TE). In a fast spin-
longer is MR angiography a mere academic curiosity; it is
echo sequence, a long train of echoes is acquired by using a
already widely used to diagnose stenoses of carotid blfurca-
series of 1 800 RF pulses; as a result, washout effects are
tions and intracranial aneurysms. MR anglography supple-
ments, and In some cases supplants, duplex sonography and
even more substantial than with spin-echo techniques. Other
CT for the study of suspected venous thrombosis In the chest, methods for creating a flow void include presaturation, which
abdomen, and pelvis. With continuing technical developments, involves application of an additional RF pulse outside the
MR angiography most likely will replace conventional X-ray plane of section in order to suppress the signal intensity of
angiography In the presurgical workup of patients who are can- inflowing blood [4, 5], dephasing gradients, and preinversion
didates for carotid endarterectomy or liver transplantation. pulses to null blood signal [6, 7].
Even MR angiography of the coronary arteries, considered Data for images on which blood is bright can be acquired as
implausible just a few years ago, has become feasible with the
a series of overlapping thin sections (sequential two-dimen-
implementation of fast imaging techniques that suppress arti-
sional, 2D) or as one or more thick volumes (three-dimen-
facts from respiratory and cardiac motion. Nonetheless, sub-
sional, 3D). Each sequence has advantages, as discussed
stantial problems remain that must be overcome before the full
clinical potential of MR angiography can be realized. Despite
further on. Bright-blood techniques can be subcategorized into
the superficial similarities between MR angiograms and con- time of flight and phase contrast. With time-of-flight tech-
ventional angiograms, fundamentally different features of niques, positive flow contrast is generated by using gradient-
blood vessels are depicted. MR angiography is susceptible to a echo pulse sequences [8]. The signal intensity produced by
variety of artifacts that can exaggerate or simulate pathologic the tissue protons is proportional to their steady-state align-
changes. The patient’s cooperation Is essential. The spatial ment with the main magnetic field that existed the moment
resolution of MR angiography is inferior to its conventional before the RF pulse was applied. The rapid application of mul-
counterpart, although the gap is being narrowed. This article tiple RF pulses for gradient-echo imaging creates a steady-
reviews the basIc principles of MR angiography and flow artI-
state signal such that the tissue protons produce a lower sig-
facts and surveys existing and future clinical applications.
nal and are said to be saturated. The amount of saturation
depends on a balance of the repetition time (TR) between
excitations and the Ti relaxation time of the tissue [9]. Fully
Basic Principles of Flow Imaging
aligned protons in fresh blood that have not been previously
Flowing blood has an appearance on MR images that is excited by RF pulses continuously flow into and out of the sec-
distinct from that of stationary tissue [3]. Depending on the tion. These fully aligned protons produce an intense signal,
imaging technique used, blood may be bright or dark (Table which contrasts with the lower signals from partially saturated
1). On spin-echo images, blood vessels usually appear dark. stationary tissues, an effect called flow-related enhancement.
With spin-echo pulse sequences, a pair (900, 1800) of sec- Washout effects are absent because only a single RF pulse is
tion-selective RF pulses is used to produce an MR signal. If used in gradient-echo sequences.
Received November 18, 1992; accepted after revision February 1, 1993.

1 Department of Radiology, Beth Israel Hospital, 330 Brookline Ave., Boston, MA 02215. Address correspondence to R. R. Edelman.

AJR 1993;161:1-11 0361-803X/93/161 1-0001 © American Roentgen Ray Society

 2 EDELMAN AJR:161, July 1993

TABLE I : Appearance of Blood on MR Images Acquired by

four images must be acquired, so that scan times are longer
Using Various Techniques than for time-of-flight techniques. Advantages of phase con-
Appearance/Technique
trast include insensitivity to flow saturation, so that slow flow
is well depicted, and direct availability of functional informa-
Bright tion (flow direction and velocity) [15]. ECG-gated cine phase-
Gradient-echo pulse sequence contrast techniques permit quantification of flow over the
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Flow compensation
entire cardiac cycle [16].
Short echo time
MR angiography has been performed at a variety of field
Thin two-dimensional gradient-echo section oriented perpendicular
to direction of blood flow strengths, from 0.2 T [1 7] to 1 .5 T or higher. Ti relaxation
Gadolinium chelate to shorten Ti relaxation time of blood
times are shorter at low field strengths, necessitating use of
Spiral scan pulse sequence larger flip angles than at 1 .5 T to achieve satisfactory signal
Segmented turboFLASH pulse sequence suppression for stationary tissues. Because of the lower
Dark intrinsic signal to noise at low field strengths, use of low-
Spin-echo or fast spin-echo pulse sequence bandwidth sequences is helpful. However, the lengthened
Presaturation or preinversion TE necessitated by the use of a long, low-bandwidth readout
Dephasing gradients may make the images more sensitive to dephasing from tur-
Long echo time bulent flow.
Thin two-dimensional spin-echo or fast spin-echo section oriented
perpendicular to direction of blood flow
Superparamagnetic iron oxide or dysprosium chelate to shorten
Projection Anglography
T2 relaxation time of blood.
The heart of MA angiography is the ability to portray blood
Note-FLASH = fast low-angle shot.
vessels in a projective format similar to that of conventional
angiography. Currently, projection images are created by
Flow-related enhancement can be maximized by using a postprocessing images acquired by a 2D or 3D gradient-
thin section oriented perpendicular to the direction of flow; echo sequence. Although image processing can be post-
this maneuver reduces the residence time of blood within the poned until after the patient has left the MR suite, it is best
section and thereby the likelihood that flowing blood will be done while the patient is still within the magnet so that addi-
saturated by multiple RF pulse repetitions. Other maneuvers tional scans can be obtained if needed. Most commonly, the
that improve flow-related enhancement include flow com- images are processed by using a maximum-intensity-projec-
pensation, in which an additional gradient pulse is used to tion algorithm [18]. With this algorithm, the brightest pixels
eliminate flow-related phase shifts [10, ii], use of a para- along a user-defined direction are extracted to create a pro-
magnetic contrast agent such as a gadolinium chelate [12], jection image. A series of such projections can then be cre-
and an appropriate balance between TR and flip angle. For ated to aid the 3D visualization of vessel anatomy, especially
instance, with a small flip angle, saturation of flowing blood in regions of vessel overlap or tortuosity. Despite its wide-
is minimized, but an undesirable increase in the relative sig- spread use, the maximum intensity projection has substan-
nal intensity of stationary tissue occurs; conversely, with a tial drawbacks. Areas with poor flow contrast, including the
large flip angle, the signal intensities of both stationary tissue edges of blood vessels and small vessels with slow flow,
and flowing blood are suppressed. A good compromise is to may be obscured by overlap with brighter stationary tissue.
use a moderate flip angle (e.g., 3O600) in conjunction with a As a result, the apparent vessel lumen may be falsely nar-
short TA (e.g., 30-60 msec) for through-plane flow and a rowed and stenoses exaggerated. It is helpful to view the
somewhat longer TA and smaller flip angle for in-plane flow. individual sections to determine the true diameter of the
The flow of blood along a magnetic field gradient causes a lumen. The results are improved by restricting the volume of
shift in the phase of the MR signal; this is the basis for tissue included for processing, a technique called targeted
another class of MR angiographic techniques called phase maximum intensity projection. Other algorithms such as con-
contrast [13, 14]. With phase contrast, pairs of images are nectivity [1 9, 20] potentially offer superior features, such as
acquired that have different sensitivities to flow. For instance, better background suppression or depth cuing.
for one image of each pair, a gradient of positive polarity By reducing the pixel size and suppressing stationary sig-
might be used to induce positive flow-related phase shifts, nal intensity, the quality of intracranial MA angiograms can
and for the other image, a negative polarity gradient might be be improved substantially. The reduction in pixel size is
used to induce negative phase shifts. Image subtraction accomplished by using a large (e.g., 256 x 51 2) acquisition
deletes stationary tissues, so that only blood vessels are matrix; background suppression is accomplished by using
shown. Phase-contrast sequences must be calibrated for a magnetization transfer pulses. Magnetization transfer is a
specific peak velocity, so that flow-related phase shifts are phenomenon that depends on the existence of two pools of
kept near ±180#{176}.
This peak velocity should be kept less than protons: (1) a mobile pool, which predominates in fluids, and
the maximum anticipated flow velocity in order to avoid alias- (2) a restricted pool, which exists in tissues having an abun-
ing. For instance, a phase shift of +220#{176}
would be aliased to dance of macromolecules (e.g., proteins) [21]. The signal
_1400, so that the apparent flow direction and velocity would intensity of the restricted pool is not directly observable
be wrong. To allow for this limit, the smallest peak velocity because these protons have ultrashort T2 relaxation times. A
that does not cause aliasing should be selected to maximize consequence of the short T2 is that the restricted protons
flow contrast. To encode flow in all three directions, at least resonate over a large frequency range, on the order of tens
 AJR:161, July 1993 MR ANGIOGRAPHY 3

of kilohertz. An intense off-resonance RF pulse (i.e., one pIe sequence repetitions) [27], and flow displacement errors
applied at a frequency that is different from the Larmor fre- relating to the time delay between RF excitation and fre-
quency) saturates the restricted pool but only minimally quency encoding or between phase and frequency encoding.
affects the mobile pool. Exchange of magnetization between These effects tend to falsely exaggerate the severity of a
the restricted (saturated) and mobile (unsaturated) pools stenosis [28], and are worst with 2D MR angiography. A short
then causes an observable decrease in the signal intensity TE minimizes flow displacement and phase dispersion arti-
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of the mobile pool. White matter contains both restricted and facts; phase dispersion is further decreased by minimizing
unrestricted pools, so that magnetization transfer pulses the voxel size (e.g., by using thin sections). Small voxels and
markedly suppress its signal intensity. On the other hand, short TEs are most easily obtained with 3D time-of-flight
flowing blood, which consists mostly of unrestricted protons, methods [29]. The biggest drawback of the thick volumes
is only minimally affected. Flow contrast, and thus vessel used with 3D is that slow or recirculating flow can become
conspicuity, is greatly improved [22, 23] (Fig. 1). saturated.
The advantages of both 2D and 3D techniques are gained
with a series of thin-slab 3D acquisitions. The sequential 3D
Flow Artifacts
(or multiple overlapping thin slab acquisition, MOTSA) tech-
A variety of artifacts, caused by phase or magnitude varia- nique [30, 31] gives better flow enhancement than single-slab
tions in the MR signal, afflict MA angiography [24, 25]. The 3D techniques and less dephasing than 2D techniques. The
importance of understanding and gaining experience with method has some drawbacks as well. For instance, the non-
flow artifacts before embarking on extensive clinical use of rectangular profile ofthe 3D slabs necessitates the use of sub-
MR angiography cannot be overemphasized; otherwise, seri- stantial overlap (up to 50%) of adjacent slabs, so that total
ous diagnostic errors are inevitable. Within a voxel, blood scan time is longer than with single-slab 3D techniques. More-
protons flowing at different velocities accumulate a range or over, signal intensity variations within the individual slabs due
dispersion of phase shifts. Complex flow can produce signal to saturation effects cause an annoying ‘Venetian blind” arti-
loss due to intraview phase dispersion (i.e., it occurs during fact. With sequential 2D or 3D acquisitions, slight motion of
each repetition of the pulse sequence) [26], ghost artifacts patients can generate discontinuities in the vessel contour that
from view-to-view signal variations (i.e., occurring over multi- can be mistaken for stenosis or fibromuscular dysplasia [32].

Fig. 1-Examples of magnetization transfer

effect.
A and B, Axial 3D gradient-echo MR images
without (A) and with (B) magnetization transfer
pulse show selective background suppression
with magnetization transfer.
Cand D, 3D MR angiograms in a different sub-
ject without (C) and with (D) magnetization
transfer pulse obtained with a 256 x 512 acquisi-
tIon matrix and a 19 x 25cm field of view. Conspi-
cuity of small vessels has improved markedly
with magnetization transfer. (Reprinted with per-
mission from Edeiman at al. [23j.)
 4 EDELMAN AJR:161, July 1993

Stenoses can be mimicked by signal loss due to surgical From a technical standpoint, MR angiography of the
clips at anastomotic sites or intravascular stents or filters. A carotid bifurcation is aided by the paucity of motion artifacts
traveling saturation pulse, commonly used in conjunction and the availability of surface coils for the neck. Dedicated
with the 2D time-of-flight technique, can cause artifactual head and neck MA angiography coils are becoming available
signal loss if a vessel loops down and then up again through that permit efficient imaging of the aortic arch through the cir-
the presaturated region. Mixing effects at venous conflu- cle of Willis without the need for multiple coil placements [37].
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ences can also cause signal loss. Moving ascitic fluid may Most studies to date have shown excellent sensitivity but van-
appear bright and simulate blood flow in the abdomen [33]. able specificity for detection of disease of the carotid bifunca-
Because of the short Ti relaxation time of methemoglobin, tion with MR angiography, depending on the equipment and
subacute hemorrhage or thrombus can appear brighter than pulse sequence used [38-40]. Two recent studies [41 42], in ,

stationary tissue and thus simulate a vascular structure on which 3D sequences with short TEs were used to evaluate
maximum-intensity-projection images [34]. This artifact is not extracranial carotid stenoses, found highly significant correla-
encountered on phase-contrast images, because signals tions (r values ranging from .94 to .97) for diameters of
from stationary tissues are deleted. stenoses measured by using MR angiography and conven-
tional angiography. Ultimately, 2D and 3D time-of-flight tech-
niques (e.g., 30/9/600 [TR/TE/flip angle]) are both necessary
Neurovascular Applications for optimal evaluation. Because 3D techniques are less sen-
sitive to turbulence than 2D techniques are, the grading of
MA angiography is best established for the diagnosis of carotid stenoses based on findings on 3D time-of-flight
extracranial carotid bifurcation disease. A major incentive for sequences correlates better with findings on conventional
developing a noninvasive means for evaluating the carotid angiography (Fig. 2). Three-dimensional phase-contrast MR
bifurcation came from the North American Symptomatic angiography can be made sensitive to low-velocity flow by
Carotid Endarterectomy Trial [35], which showed that carotid using a small VENC, but the acquisition is time-consuming.
endarterectomy significantly reduces the prevalence of stroke As a result, 2D time offlight is more commonly used to depict
in symptomatic patients with stenosis in which the diameter of slow flow, particularly in the differentiation of an occlusion
the affected vessel is narrowed 70% or more. The prevalence from a critical stenosis. Evidence is mounting that this differ-
of major morbidity associated with conventional angiography entiation can be reliably made by using MR angiography (Fig.
is 0.5-3.0% [36]. Duplex sonography is accurate but operator 3), although no large studies specifically addressing this
dependent, and few surgeons are willing to operate solely on problem have yet been published. In our experience, imaging
the basis of a sonographic study. Occlusions cannot always of both the intra- and extracranial carotid circulations should
be differentiated from critical stenoses. Moreover, tandem be done to help solve this problem. Carotid and vertebral dis-
intracranial stenoses, which may preclude endarterectomy, sections can be shown [43], although at present conventional
are not accessible without the additional use of transcranial angiography remains the technique of choice because of its
Doppler sonography or other noninvasive tests. better spatial resolution and proven ability to show subtle

Fig. 2.-Severe proximal stenoses of internal and external carotid arteries.

A, Digital subtraction anglogram.
B, MR angiogram from sequential 2D acquisition (30/9/60#{176},
first-order flow compensation, 55 sections, 3-mm section thickness, 1-mm overlap, 160
256 matrix, 17 x 23 cm field of view) shows exaggeration of lesions.
C, MR angiogram from sequential 3D acquisition (29/6/20#{176},
first-order flow compensation, two slabs, 52-mm slab thickness, 0.8-mm partition thick-
ness, 64 partitions, 192 x 256 matrix, 15 x 20 cm field of view) shows stenoses more precisely, at least in part because smaller voxels and shorter TE
minimize signal ioss from turbulence-induced dephasing.
 AJR:161, July 1993 MR ANGIOGRAPHY 5
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Fig. 3.-Severe stenosis of internal carotid artery with string sign.

A and B, Digital subtraction angiograms of right carotid bifurcation and siphon show string sign (arrow).
C, Coronal maximum-intensity-projection MR angiogram from sequential 3D acquisition (29/6/20#{176})
shows string sign well; usually, sequential 2D MR
angiograms would be preferred because of their greater sensitivity to slow flow.

lesions. Similar to conventional angiography, in MR angiogra- Willis, but is less reliable for evaluating small, distal vessels.
phy the dissected vessel typically appears tapered; however, Spatial resolution is not adequate for the diagnosis of small-
shine-through from paramagnetic methemoglobin can create vessel vasculitis. Collateral flow patterns can be determined
an artifactual widening of the lumen on maximum-intensity- by using judiciously placed presaturation pulses [49]; these
projection images. Because intramural blood appears bright pulses suppress signal within the vascular territory supplied
but flow appears dark on spin-echo images, the addition of a by the presaturated vessel. MR angiography is useful for
spin-echo sequence resolves any confusion [44]. grading vertebrobasilar stenoses, thereby influencing strate-
When findings on sonography and MR angiography agree, gies for anticoagulation. However, care must be taken to
100% concordance with findings on conventional angiogra- interpret properly anatomic variations, such as termination of
phy has been reported [39, 42]. It thus appears increasingly a vertebral artery at the posterior inferior cerebellar artery,
likely that the combination of noninvasive MR angiography and to apply appropriately techniques sensitive to slow flow
and duplex sonography will replace conventional angiogra- for showing hypoplastic or stenotic vessels.
phy in most patients with disease of the carotid bifurcation; The use of MR angiography to screen asymptomatic
however, this degree of accuracy assumes use of state-of- patients for intracranial aneurysms remains controversial
the-art equipment and radiologists experienced in interpret- [50]. In one series [51], the accuracy of detection was 95%,
ing MR angiograms. As yet, the accuracy of MR angiography but some small (<5 mm) aneurysms were missed. The com-
for evaluating the carotid and vertebral origins off the aortic plication rate from such small aneurysms is low. Whether
arch is not known. this sensitivity is acceptable will depend on the institution-
Three-dimensional methods have been most effective for dependent biases of the referring clinicians, and must be
imaging the intracranial arteries [45-48]. MR angiography balanced against the potential morbidity associated with
can show stenoses of the primary branches of the circle of conventional angiography. High-resolution imaging with tar-

Fig. 4.-5-mm aneurysm of carotid siphon.

A, Lateral projection, digital subtraction an-
giogram.
B, Lateral projection, targeted maximum-in-
tensity-projection MR angiogram from sequen-
tial 3D acquisition. Aneurysm could not be seen
on any other views.
 6 EDELMAN AJR:161, July 1993

Fig. 5.-Arteriovenous malformation of right tempo-

ral lobe.
A, Digital subtraction angiogram.
B, 3D time-of-flight MR angiogram shows malforma-
tion, but a hematoma along medial aspect partly ob-
scures medial nidus and P2 segment of right posterior
cerebral artery.
C and D, Magnitude display of 3D phase-contrast
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MR anglogram before (C) and after (D) administration

of 0.3 mmol/kg of contrast material (Prohance; Squibb
Diagnostics, Princeton, NJ) with VENC of 20 cm/sec.
Hematoma is not seen.
E and F, Magnitude display of 3D phase-contrast MR
angiogram before (E) and after (F) administration of
0.3 mmol/kg of Prohance with VENC of 80 cm/sec. Rap-
ld flow in middle cerebral arteries is better depicted
with higher VENC.
G and H, Phase display of 2D phase-contrast MR an-
giograms with anteroposterior flow encoding shows
reversed flow in right posterior communicating artery.
(Reprinted with permission from Potchen et al. [55].)
 AJR:161, July 1993 MR ANGIOGRAPHY 7

geted maximum intensity projections of critical regions such Duplex sonography is the initial choice for studying the por-
as the middle cerebral bifurcations, basilar tip, and carotid tal and hepatic veins. If overlying gas or surgical dressings
siphons is essential to maintain accuracy (Fig. 4). MA preclude adequate evaluation, then 2D time-of-flight MA
angiography is not an acceptable substitute for conventional angiography is an accurate alternative [64]. A presaturation
angiography in patients with subarachnoid hemorrhage, band placed through the lower chest suppresses arterial sig-
although it may be a helpful adjunct to define the bleeding nal intensity. Because of its large, unimpeded field of view,
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site. MR angiography is sensitive for intracranial vascular MR angiography is better than duplex sonography for deter-
malformations [52-55] (Fig. 5) and can be used to determine mining patency of the portal vein and for depicting collateral
the volume of persistent nidus after radiosurgery [56], but it vessels; this information can be especially critical in the pre-
cannot substitute for conventional angiography in defining surgical examination of candidates for liver transplants [65]
feeder vessels and shunting. Administration of a paramag- (Fig. 6), as an occluded portal vein may preclude transplanta-
netic contrast agent is sometimes useful for giving better tion, and awareness of the locations of enlarged collateral
definition of the nidus. vessels can help avoid accidental vascular injury. MR angiog-
MR angiography of the intracranial veins can be done by raphy also has been used to map hepatic and portal venous
several means, including 2D time of flight with arterial pre- anatomy for percutaneous transjugular intrahepatic portosys-
saturation [57], contrast-enhanced 3D time of flight [76], and temic shunting procedures, with a consequent reduction in
phase contrast [48]. MR angiography has largely supplanted procedure time and complication rate (Finn JP, personal com-
conventional angiography for detecting thrombosis involving munication). Although CT is the preferred technique for stag-
the major venous sinuses, and for showing tumor encase- ing of renal cell carcinoma, MR angiography can better show
ment of major venous structures [58, 59]. the extent of tumor thrombus in the renal vein and inferior
vena cava and, most importantly, involvement of the hepatic
veins or extension through the diaphragm. MA angiography
Body Applications
can show the patency of veins in the lower extremities [66],
Because the technical obstacles are more severe, appli- although duplex sonography would be the first test because
cations of MR angiography in the body are generally less of its lower cost. MA angiography is more useful for the pelvic
well developed and tested than those for the head and neck veins, where sonography may be technically limited.
[60]. As is the case for the intracranial veins, the venous sys- Transesophageal echocardiography, because of its portabil-
tems of the chest [61], abdomen [62, 63], and pelvis are par- ity and clear depiction of the aortic root structures, is the tech-
ticularly amenable to study with MR angiography. MR nique of choice for evaluating acute aortic dissections. MR is
angiography can be used in place of contrast-enhanced superior in accuracy to contrast-enhanced CT for evaluating
phlebography in the chest, depicting occlusions of the supe- stable aortic dissections and aneurysms [67], although care
rior vena cava and subclavian and jugular veins. Axial pre- must be taken with MR to differentiate mural thrombus from
saturation of the left ventricle suppresses the signal intensity persistent intravascular signal caused by slow flow. ECG-
of the aorta and branch arteries. A combination of 2D time- gated cine imaging is helpful in this regard because the intralu-
of-flight gradient-echo axial, sagittal, and sometimes coronal minal signal intensity of slow flow will vary over the cardiac
scans suffices for complete evaluation. cycle, whereas the signal intensity of thrombus is constant.

Fig. 6.-Candidate for liver transplantation.

A, Spienoportogram shows dilated splenic vein but does not show proximal portion of portal vein. Portal vein could not be seen with duplex sonog-
raphy either.
B, Coronal maximum-intensity-projection MR angiogram created from breath-hold sequential coronal 2D gradient-echo acquisition (30/8/30#{176},
5-mm
sections, 1-mm overlap, 38 x 38 cm field of view, 192 x 256 matrix) shows a patent portal vein (arrow) and splenic varices.
C, MR angiogram with bolus tracking of main portal vein, done by placing a thin presaturation stripe perpendicular to long axis of vessel. Displace-
ment of dark stripe (arrow) is away from liver, indicating hepatofugal flow.
 8 EDELMAN AJR:161, July 1993

Stenosis of the renal artery afflicts a small percentage of using different coils and repositioning the patient several
patients with systemic hypertension. Neither duplex sonogra- times makes it difficult to screen the pelvis and lower extrem-
phy nor radionuclide renography has been entirely satisfac- ties in a reasonable time. Best results are obtained when
tory as a screening test, so digital subtraction angiography the MA angiographic examination is focused on a restricted
remains the gold standard. Several MR angiographic tech- volume. Using an axial 2D time-of-flight method with a track-
niques, including 2D [68] and 3D time-of-flight and phase- ing venous presaturation pulse, Owen et al. [72] showed that
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contrast techniques [69], have shown promise for the evalua- significantly more distal run-off vessels can be shown with
tion of renal artery stenosis (Fig. 7). Our current approach is MR angiography than with conventional angiography (Fig.
to use a 2D time-of-flight sequence with a reduced band- 8); the finding of a patent run-off vessel may alter the choice
width to improve the signal-to-noise ratio. Breath-holding 2D between surgical revascularization and amputation. As a
sections are acquired in coronal and axial orientations, with general screening method for peripheral artery disease, MR
oblique presaturation pulses applied over both kidneys to angiography is compromised by the tendency of stenoses to
suppress the renal veins. Additional oblique images oriented be exaggerated and by limited spatial resolution, particularly
along the long axis of each renal artery can be helpful. Also, when a body coil is used.
fat-suppressed 2D time-of-flight MA angiography done Additional problems that affect MR angiography of the
immediately after administration of an MR contrast agent lower extremities are the phasic nature of arterial blood flow
can, in our early experience, improve vessel delineation. and the bright signal intensity of bone marrow and subcuta-
Care must be taken to recognize early vessel bifurcations; neous fat. The latter problem is solved by using a chemical
also, differentiation of slow flow due to medical renal disease shift-selective fat saturation pulse [73]. With respect to the
from a vessel occlusion may be difficult because the renal first problem, most of the data with standard 2D time-of-flight
artery may be inapparent in both conditions. Currently, MA sequences are acquired during diastole, when little or no
angiography is most useful in older patients with suspected flow contrast exists. Gating the central phase-encoding lines
atherosclerotic disease affecting the proximal renal arteries, (which determine image contrast) to the period of maximal
and less useful for suspected fibromuscular dysplasia in systolic flow can markedly improve vessel conspicuity [74].
young patients with more distal disease. It cannot yet In conjunction with this technique, scan time is reduced by
replace conventional angiography for screening potential using an oblique coronal plane of section so that fewer sec-
renal donors because it is not accurate in depicting small tions are needed to span the region of interest. Promising
accessory vessels. Further development of pulse sequences results are also being obtained with a modified ECG-gated
and testing is needed before MR angiography can be touted cine 2D phase-contrast technique that uses a variable veloc-
for widespread use as a screening test for stenosis of the ity sensitivity; the peak velocity for a phase-contrast
renal artery. Because of its speed and insensitivity to flow sequence that does not cause aliasing is matched to the
artifacts, contrast-enhanced spiral CT promises to provide peak velocity for each phase of the cardiac cycle, thus opti-
stiff competition in this area, at least in patients without mizing flow contrast [75]. The images are then summed to
impaired renal function. create a projection angiogram. Flow contrast also can be
Although the peripheral arteries were the first vascular improved by using gadolinium chelates [76-78], but then dif-
system in which the feasibility of MR angiography was dem- ferentiating arteries from veins is difficult.
onstrated [70], only recently has the initial promise of MR Pulmonary MR angiography could prove useful for the
angiography in this area become a clinical reality [71]. One evaluation of suspected thromboembolism. Breath-holding
technical impediment has been the lack of a suitable surface 2D time-of-flight [79] and 3D time-of-flight [80] techniques
coil that could encompass a sufficiently large field of view. can show distal branches of the pulmonary arteries in
Typically, a body coil is used for the pelvic and thigh arteries, healthy subjects. Ultrashort TEs are needed to overcome
and an extremity coil for the calves and ankles. The need for susceptibility artifacts from air in the lungs. Unfortunately,

Fig. 7.-30-year-old woman with uncontrol-

lable hypertension.
A, Axial maximum-intensity-projection MR
angiogram from sequential axial 3D gradient-
echo acquisition (29/6/20#{176},
48-mm siab, 1.5-
mm partition thickness, 32 x 32 cm field of
view, 128 x 256 matrix) with venous presatura-
tion shows a beaded appearance of right renal
artery.
B, Conventional aortogram shows fibro-
muscular dysplasia affecting right renal artery.
 AJR:161, July 1993 MR ANGIOGRAPHY 9

patients with pulmonary embolism may be too unstable for a dients are oscillated in tandem, so that k-space (a descrip-
prolonged MR study, and hyperventilation can degrade tiort of the data in terms of spatial frequencies) is traversed
image quality. in a spiral rather than as a series of straight lines. For high-
Although considered implausible just a few years ago, resolution imaging, a series of breath-holding ECG-gated
rapid progress is being made in the application of MR spirals is acquired over several heart beats; the spirals are
angiography to the coronary arteries. Formidable technical then combined before reconstructing the image. Although
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obstacles have impeded this application of MR angiography, sensitive to magnetic field inhomogeneities, spiral MR
including respiratory and cardiac motion, the small size of angiography has great potential for coronary artery imaging.
the coronary arteries, lack of a suitable surface coil, and low My colleagues and I have used a fast gradient-echo
flow velocities. Several approaches have been proposed, sequence in which the data are acquired during multiple
including 3D gradient-echo imaging [81], tagging of flow in heart beats as groups of phase-encoding steps, called seg-
the aortic root with a projection readout [7], echoplanar 2D ments. By keeping the duration of each segment short (e.g.,
spiral scanning [82], and 2D segmented turbo-FLASH (fast 50-100 msec) and by imaging during diastole, we can mini-
low-angle shot) [83]. To date, the majority of clinical experi- mize blurring from cardiac motion. The patient is positioned
ence has been accumulated with the last two methods. prone over a surface coil, and an incremented flip angle
Echoplanar is the fastest method for producing an MR series [86] is used to maximize the signal-to-noise ratio; fat
image [84]. With echoplanar imaging techniques, the read- saturation improves contrast between the coronary arteries
out gradient is rapidly oscillated to quickly produce a series and epicardial fat [87] (Fig. 9). In a series of 38 patients with
of separately phase-encoded gradient echoes. Image acqui- angiographic correlation, 90% positive and 88% negative
sition is completed in as little as 30 msec. However, spatial predictive values for coronary artery disease were obtained
resolution is not yet adequate for evaluating the coronary [89]. Further improvements in accuracy are expected with
arteries, and flow artifacts with echoplanar imaging can be the introduction of faster gradient systems and better sur-
substantial [85]. Spiral scanning is conceptually similar to face coils. With a phase-contrast modification of segmented
echoplanar imaging, but has better flow properties. Two gra- turbo-FLASH, the feasibility of measuring flow velocities in

Fig. 8.-Patient with claudicatlon and steno-

515 of superficial femoral artery (not shown).
A, Delayed film from conventional run-off
angiogram of calf shows calf arteries poorly.
B, Sagittal maximum-intensity-projection
MR angiogram from sequential axial 2D acqui-
sition obtained with tracking venous presatura-
tion shows patency of run-off vessels more
clearly.

Fig. 9.-Severe stenosis of right coronary

artery.
A, Conventional angiogram after selective
injection of right coronary ostium shows le-
sion.
B, Maximum-intensity-projection MR anglo-
gram created from breath-hold sequential 2D
ECG-gated turbo-FLASH acquisition (13/8/In-
cremental flip angle of 10-40#{176}, 5-mm section
thickness, 2-mm overlap, 160 x 256 acquisition
matrix, 23 x 23 cm field of view) also shows
stenosis. (Reprinted with permission from
Edelman et al. [88].)
 10 EDELMAN AJR:161, July 1993

coronary arteries at rest and after augmentation with phar- 5. Edelman AR, Atkinson DJ, Silver MS, Loaiza FL Warren WS. FR000
pulse sequences: a new means of eliminating motion, flow, and wrap-
macologic stimulation has been shown [90]. This technique
around artifacts. Radiology 1988;166:231-236
might be useful for determining the physiologic significance 6. Mayo JR, Cuiham JA, Mackay AL Aikins DG. Blood MR signal suppres-
of a stenotic coronary artery and for monitoring the efficacy don by preexcitation with inverting pulses. Radiology 1989:173:269-271
of mechanical or pharmacologic interventions. These meth- 7. Nishimura DG, Macovski A, Pauly JM. Considerations of magnetic reso-
ods can also be applied to coronary artery bypass grafts, but nance angiography by selective inversion recovery. Magn Reson Med
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1988;7:472-484
susceptibility artifacts from sternal wires and surgical clips
8. Haase A, Frahm J, Matthaei D, Hanicke W, Merboldt KD. FLASH imaging:
are impediments. rapid NMR imaging using low flip-angle pulses. J Magn Reson 1986;67:
Additional works in progress for MR angiography include 256-266
intravascular contrast agents and enhanced gradient sys- 9. Wehrli FW. Time-of-flight effects in MA imaging of flow. Magn Reson Med
tems. Available gadolinium chelates can provide effective 1990;14:187-193
10. Laub GA, Kaiser WA. MA angiography with gradient motion refocusing. J
enhancement of blood vessels, which is often useful in dis- ComputAssist Tomogr 1988:12:377-382
tinguishing signal loss caused by thrombus from saturation 11 . Haacke E, Lenz G. Improving MR image quality in the presence of motion
effects caused by slow flow. However, preliminary data sug- by using rephasing gradients. MR 1987;148:1251-1258
gest that the best results are obtained with double or triple 12. Un W, Haacke EM, Smith AS, Clampitt ME. Gadolinium-enhanced high-
resolution MR angiography with adaptive vessel tracking: preliminary
doses (e.g., 0.2 or 0.3 mmol/kg), and imaging should be per-
results in the intracranial circulation. JMRI 1992;2:277-284
formed during, or in the first few minutes after, infusion of the 13. Dumoulin C, Souza 5, Walker M, Wagle W. Three-dimensional phase
contrast agent. Although an intravascular contrast agent is contrast angiography. Magn Reson Med 1989;9:139-.149
years away from approval by the Food and Drug Administra- 14. Dumoulin CL, Yucel EK, Vock P. et al. Two- and three-dimensional phase
tion, such an agent could be of enormous value for MR contrast MR angiography of the abdomen. J Comput Assist Tomogr
1990;14:779-764
angiography. Intravascular contrast agents such as gadolin- 15. Permicone JR, Siebert JE, Laird TA, Aosenbaum TL, Potchen EJ. Deter-
ium polylysine persist for hours in the blood with little mination of blood flow direction using velocity-phase image display with 3-
enhancement of soft tissues [91]. As a result, flow contrast! D phase-contrast MR angiography.AJNR 1992;13:1439-1 438
noise and depiction of slowly flowing blood would be 16. Mostbeck GH, Caputo GA, Higgins CB. MA measurement of blood flow in
the cardiovascular system. AJR 1992;1 59:453-461
improved. Another upcoming development is faster, stronger
17. Pavone P. Marsili L Catalano C, et al. Carotid arteries: evaluation with
gradient systems. Using a new whole-body echoplanar gra- low-field-strength MA angiography. Radiology 1992;184:401-404
dient system, my colleagues and I have been able to imple- 18. Laub G. Displays for MA angiography. Magn Reson Med 1990;14:222-229
ment TEs as short as 1 msec and small fields of view. With 19. Saloner D, Hanson W, Tsuruda J, Tyen A, Anderson C, Lee A. The appli-

such short TEs, flow-related dephasing becomes insignifi- cation of a connected voxel algorithm to magnetic resonance angio-
graphic data. JMRI 1991;1 :423-430
cant. However, very short TEs have a major drawback, 20. Cline HE, Dumoulin CL. Lorensen WE, Souza SP, Adams WJ. Volume
which is that the necessarily short readout times result in a rendering and connectivity algorithms for MA angiography. Magn Reson
high-signal bandwidth. The high bandwidth adversely affects Med 1991;18:384-394
signal to noise. 21 . Wolff SD, Balaban AS. Magnetization transfer contrast (MTC) and tissue
water proton relaxation in vivo. Magn Reson Med 1988; 10:135-144
22. Balaban AS, Chesnick 5, Hedges K, Samaha F, Heinman FW. Magneti-
zation transfer contrast in MA imaging of the heart. Radiology 1991:180:
Conclusions
671-675
Multiinstitutional prospective trials are needed to deter- 23. Edelman AR, Ahn 5, Chien D, et al. Improved time-of-flight MR angiogra-
mine the cost-effectiveness of MR angiography. These trials phy of the brain using magnetization transfer contrast. Radiology 1992;
184:395-399
may be required to qualify MR angiography for reimburse- 24. Anderson CM, Saloner D, Tsuruda JS, Shapeero LG, Lee RE. Artifacts in
ment by private and governmental insurers. Such studies maximum-intensity-projection display of MR angiograms. AJR 1990;154:
have daunting obstacles, such as the rapid pace of techno- 623-629
logic advancement and diversity of software and hardware. 25. Tsuruda J, Saloner D, Norman D. Artifacts associated with MA neuroan-
giography.AJNR 1992;13:1411-1 422
Nonetheless, the field of MA angiography has progressed to
26. Gao JH, Gore JC. Turbulent flow effects on NMR imaging: measurement
a stage at which several clinical applications are of obvious of turbulent intensity. Med Phys 1991;18:1045-1051
value, including the diagnosis of venous disorders and dis- 27. Wolf AL Richardson DB, LaPlante CC, Huston JI, Riederer SJ, Ehman
ease of the carotid bifurcation. With further technical im- AL Blood flow imaging through detection of temporal variations in mag-

provements, it seems likely that important applications of MR netization. Radiology 1992;185:559-567

28. Podolak MJ, Hedlund LW, Evans AJ, Herfkens AJ. Evaluation of flow
angiography will also be found in the diagnosis of peripheral through simulated vascular stenoses with gradient echo magnetic reso-
artery disease, stenosis of the renal artery, and ischemic nance imaging. Invest Radiol 1989:24:184-189
heart disease. 29. Schmalbrock P, Yuan C, Chakeres DW, Kohli J, PeIc NJ. Volume MR
angiography: methods to achieve very short echo times. Radiology 1990;
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