MR Angiography
Author:
William G. Bradley, MD, PhD, FACR
Objectives: Upon the completion of this CME article, the reader will be able to
1.
Discuss Time-of-Flight (TOF) MR angiography and the different aspects of 2DTOF, 3D-TOF, and multiple overlapping thin slab acquisition (MOTSA) and
describe the clinical settings for which each may be of use.
2.
Describe Phase Contrast MR angiography, its limitations, and the clinical settings in
which it may be used.
3.
Explain Contrast Enhanced MR angiography, its benefits in the clinical setting and
its potential limitations.
Introduction
MR angiography (MRA) is a noninvasive technique based on magnetic resonance
imaging (MRI), which can produce images of blood vessels similar to those produced by the
more invasive catheter angiogram. MRA can be performed with or without injecting
intravenous gadolinium (the MR contrast agent) anywhere in the body. The purpose of this
paper is to describe the different techniques used for MR angiography. The article is
organized according to the MR technique used rather than by the specific blood vessel being
imaged. These techniques include time of flight MRA, phase-contrast MRA, and contrastenhanced MRA.
Time-of-Flight MRA
Time-of-flight (TOF) MRA is based on the phenomenon of “flow related
enhancement” or “inflow phenomenon”. When fully magnetized spins in blood vessels first
enter an imaging volume, they produce high signal. On conventional MR images, this can
lead to flow artifacts. On MR angiograms, the effect is harnessed to produce images of the
vessel, like an angiogram. In most cases, the clinical question will only involve arteries or
veins but not both. In such cases, a 90 pulse is applied above or below the imaging volume
to “saturate” (or eliminate) the signal from spins entering in the unwanted venous or arterial
vessels. This 90 pulse is referred to as a “spatial saturation pulse” or simply a “SatPulse”.
TOF MRA can be performed as a 2D or 3D technique. Two-dimensional TOF
MRA consists of single slice gradient echoes, sequentially acquired in the direction
countercurrent to flowing blood (so the slices are always meeting fresh, unsaturated, fully
magnetized spins, head on). Thus, to image the carotid arteries, you would want to start
from the top and go down so that the scan is meeting the up-flowing arterial blood head on
(figure 1). If you were interested in imaging the jugular veins, on the other hand, you would
start at the bottom and go up to meet the fresh, down-flowing spins, head on. Using this
technique will also allow you to image blood that is flowing in the opposite direction from its
normal flow, for example, down flowing blood in the vertebral artery in subclavian steal
syndrome.
The slice thickness in 2D-TOF techniques is generally on the order of 2 to 4 mm
depending on the application (thinner slices being used for the carotids and thicker slices
being used for flow in the portal vein or aorta). The saturation pulse in a 2D-TOF MRA
technique typically travels behind the imaging slice to eliminate unwanted arterial or venous
blood.
In 3D-TOF MRA, signal is acquired from a 3 to 6 cm thick slab. This both increases
the signal-to-noise (S/N) ratio (compared to the 2 to 4 mm thick slice of 2D-TOF) and
decreases the effective slice thickness, improving spatial resolution. Because the slab in a
3D-TOF technique is thicker than the slices used for 2D-TOF MRA, the spins may be
exposed to more than one RF pulse as they traverse the slab. This may lead to loss of
magnetization and saturation, eliminating signal from the vessel (figure 2). Saturation effects
are more pronounced with larger flip angles (which release more magnetization per RF
excitation) and shorter repetition times (TR) (which expose the spins to more RF exposures
per unit time) in the gradient echo acquisition. There are several ways to decrease saturation
effects:
1. Decrease the flip angle (which decreases the signal elicited per RF exposure)
2. Increase the TR (which increases the acquisition time)
3 Decrease the slab thickness (which decreases the coverage)
4. Give gadolinium (which shortens the T1 – see contrast-enhanced MRA below).
MOTSA (Multiple Overlapping Thin Slab Acquisition) is a third TOF MRA
technique that consists of multiple 2 to 3 cm thick 3D-TOF slabs covering the anatomy of
interest. MOTSA combines the best features of 2D- and 3D-TOF MRA, because it has the
unlimited coverage of 2D-TOF and the high spatial resolution of 3D-TOF (figure 3).
Occasionally, minor saturation effects will remain, producing low intensity bands at the
junctions between the slabs known as “Venetian blind artifacts”. To minimize these
artifacts, the outer portion of the slab (where saturation effects are greatest) is discarded.
Since the discarded portion may be 10% to 50% of the slab thickness, MOTSA is less
efficient than 3D-TOF MRA. Typically, the smaller the portion of the slab discarded, the
greater the venetian blind artifact.
When limited coverage is needed (for example, an evaluation of the circle of Willis in
an acute cerebral infarct), a single 3D-TOF slab can be used. When greater coverage is
required (for example, an evaluation of carotid artery stenosis or to screen the entire brain
for an aneurysm – figures 4 & 5) MOTSA is used. While 2D-TOF MRA can be used to
screen the carotids, MOTSA typically has higher spatial resolution and is more accurate at
sizing stenoses than 2D-TOF MRA – although neither is as accurate as contrast-enhanced
MRA (see below).
Once a series of 2D or 3D slices has been acquired, they can be viewed directly (as
64 or so separate images), scrolled consecutively on a workstation, or displayed in
angiographic format. For the last option, a maximum intensity projection (MIP) algorithm is
generally used. The MIP algorithm basically tells the computer to connect the bright dots of
inflowing blood on the 64 source images looking from a particular angle or projection. We
typically rotate the data about a horizontal and or vertical axis, acquiring 12 images every 15
degrees for a total of 180 degrees. (The back 180 degrees is the mirror image of the front
180 degrees so it is not necessary to repeat it.) When rotating vertically, we typically cut the
data set in half so the right and left sides do not overlap. This is called a “targeted MIP”.
With increasing gradient strength and advanced image processing, shorter repetition
times are possible, making 10242 MRA technically feasible. Intracranial vessels appear much
larger with 300 µm pixels than they do at lower resolution. This partially reflects the capture
of pixels at the periphery of the artery, where the greatest phase dispersion occurs during
laminar flow. With larger pixels, this intravoxel dephasing results in nonvisualization. With
higher resolution (smaller pixels), the phase differences from one edge of the pixel to the
other are smaller, leading to less phase cancellation. Such improved visualization of true
arterial diameter at 250 µm spatial resolution will increase the applications of MR
angiography to include vasculitis, spasm following subarachnoid hemorrhage, and detection
of even smaller aneurysms.
One of the potential problems with the maximum intensity projection algorithm is
that it includes anything that is bright on the T1-weighted source images, including subacute
hemorrhage (figures 6, 7, & 8), fat, or anything enhancing with gadolinium. It is therefore
important to examine both MRA images and conventional images (figure 6) to determine if
something is showing up on the MIP images that doesn’t represent flowing blood (figure 7).
In such cases, it may be desirable to acquire a phase contrast MRA that subtracts out high
intensity saturation structures (figure 8) (see below).
The MIP algorithm has an S/N ratio threshold for what is included in the image, so
very small vessels or the residual lumen of tight stenoses may not be visualized. For this
reason, it is important to review the individual source images before diagnosing a complete
stenosis or absence of a vessel from the MIP images.
The source images are also useful for diagnosing the small lenticulostriate collaterals
in moyamoya disease. Moyamoya disease is a poorly understood disease that involves the
occlusion of arteries (such as the internal carotid and the middle cerebral arteries). This
results in the development of collaterals around the occlusion that on angiography gives the
appearance of a puff of smoke or moyamoya.
Phase Contrast MRA
In phase contrast (PC) MRA, signal is based on the phase gained (or lost) as the
spins move through a magnetic field gradient. This phase is subtracted from the background
phase to determine the portion of the phase that is only due to motion. Background
stationary tissue, which is not moving, subtracts out – as does subacute hemorrhage and any
other bright signal that would normally be included in a time-of-flight image (figure 8). The
amount of phase gain (or loss) has to be less than 180 degrees (or –180 degrees) or “velocity
aliasing” occurs (which means that the spins appear to be moving at maximum velocity in
one direction in one pixel and then, in the next pixel, they appear to be moving at maximum
velocity in the opposite direction). The strength of the phase encoding gradient is
determined by setting a parameter called the “encoding velocity” or “Venc”. Since phase
sensitization has to be performed along the x, y, and z gradients and then each is subtracted
from a baseline image (without gradient activation), this sequence typically takes 4 times
longer than a TOF technique with the same TR and matrix. For this reason, it is rarely used
except when it is necessary to subtract out subacute hemorrhage or fat (for example, from a
ruptured dermoid).
Contrast Enhanced MRA
Contrast enhanced (CE) MRA has become the preferred technique for imaging
arteries everywhere in the body except for the brain. With modern echo planar imaging
(EPI) capable MRI systems, the stronger, faster gradients allow an image to be acquired
during the brief time that gadolinium is in the arterial phase before it gets to the veins. CE
MRA is essentially a time-of-flight technique without saturation effects. To image the
carotids, for example, a coronal 3D-TOF slab is set up to maximize the field-of-view (FOV),
covering from the carotid origins through the siphon. Typically, a mask image is acquired
and then contrast is injected. In standard k-space acquisition mode, a series of several 10 sec
acquisitions are acquired following injection of gadolinium, one of which is bound to be in
the arterial phase. The advantage of this technique is that the exact time of arrival of the
gadolinium bolus does not need to be known. When the timing is known (by injecting a 2 cc
bolus of gadolinium and noting the time it takes to reach the carotid bulb), a more
sophisticated acquisition technique allows a higher resolution image to be acquired in
approximately 30 to 60 seconds (figure 9). This technique is known as “elliptical-centric”
MRA and refers to the pattern of k-space acquisition in the 3D-TOF technique.
Some MR manufacturers also have automated bolus detection software to determine
when the gadolinium bolus arrives at the anatomic level of interest. (For example, GE calls
this SmartPrep and Siemens calls it CareBolus.) This works particularly well for
abdominal and runoff angiography (figure 10) but not as well for carotid MRA. Peripheral
MRA is also facilitated by the use of a stepping table which first acquires a mask image at
three stations moving from inferior to superior and then, after the gadolinium injection, the
table chases the bolus from superior to inferior during image acquisition. While this
technique works in the vast majority of cases, it is sometimes necessary to perform a 2DTOF acquisition from inferior to superior through the leg, should there be proximal stenoses
and asymmetric delivery of the contrast to the legs (particularly in diabetic patients).
Figures:
1
2D-TOF Carotid MRA. LAO projection demonstrates normal carotid and vertebral
arteries.
2
Saturation Diagram. As spins traverse a 3D-TOF slab, they lose magnetization in
proportion to the flip angle (FA). During time TR they recover magnetization
according to the equation 1-exp(-TR/T1). The shorter the TR, the larger the flip angle,
and the longer the T1, the sooner saturation (loss of signal) occurs.
3
MOTSA through a normal Circle of Willis.
4
MRA of an Intracranial Aneurysm. A MOTSA demonstrates a cavernous carotid
aneurysm.
5
MRA of an Intracranial Aneurysm. For comparison, a lateral projection from a catheter
angiogram.
6
Subacute Subdural Hemorrhage. A T1-weighted image shows subacute subdural
hematoma with high signal methemoglobin.
7
Subacute Subdural Hemorrhage. A 3D-TOF MRA is degraded by the bright subacute
subdural hematoma.
8
Phase Contrast MRA with Subacute Hemorrhage. A PC MRA subtracts out the high
signal stationary subdural hematoma.
9
CE MRA of Carotid and Vertebral Arteries. Elliptical-centric k-space acquisition shows
right carotid stenosis.
10
CE MRA of the aorto-iliac system demonstrates normal renal arteries and left iliac
artery occlusion.
References or Suggested Reading:
1.
Bradley WG, Waluch V. “Blood flow: magnetic resonance imaging” Radiology 154:443450, 1985.
2.
Bradley WG. Chapter 11. “Flow Phenomena” in Stark DD, Bradley WG (eds)
Magnetic Resonance Imaging 3rd ed (Mosby, St. Louis) 1999;pp 231-256.
3.
Masaryk TJ, Perl J II, Dagirmanjian A, Tkach JA, Laub G. Chapter 56. “Magnetic
Resonance Angiography: Neuroradiological Applications” in Stark DD, Bradley WG
(eds) Magnetic Resonance Imaging 3rd ed (Mosby, St. Louis) 1999;pp 1277-1316.
4.
Blatter DD, Parker, Ahn SS, et al. “Cerebral MR Angiography with multiple
overlapping thin slab acquisition II. Early clinical experience” Radiology 1992;183:379.
5.
Erly WK, Zaetta J, Borders GT, Ozgur H, et al. “Gadopentetate dimeglumine as a
contrast agent in common carotid arteriography” AJNR 2000;2(5):964-967.
6.
Fain SB, Riederer SJ, Bernstein MA, Huston J 3rd. “Theoretical limits of spatial
resolution in elliptical-centric contrast-enhanced 3D-MRA” Magn Reson Med
1999;42(6):1106-1116.
7.
Prince MR. Renal MR Angiography: a comprehensive approach: JMRI 1998;5:511-516.
8.
Grist TM. “MRA of the abdominal aorta and lower extremities” JMRI 2000;11:32-43.
9.
Dumoulin CL, Souza SP, Walker MF, et al. “Three-dimensional phase contrast
angiography” Magn Reson Med 1989;9:139.
About the Author:
Dr. William Bradley currently is the director of the Magnetic Resonance Imaging
Center at Long Beach Memorial Medical Center, in Long Beach, California. He is also a
Professor of Radiology at the University of California, Irvine. He actively teaches Magnetic
Resonance Imaging to medical students, Radiology residents and fellows in Radiology.
Dr. Bradley has over 100 publications in peer-review journals and is actively involved
in research in the field of Magnetic Resonance Imaging. He has presented his research and
has given lectures on MRI topics at major conferences around the country as well as
internationally, including Europe, Japan, and India.
Examination:
1.
In most clinical cases, the question will only involve arteries or veins but not both.
In TOF MRA, a 90 pulse, which is called a ________ is applied above or below the
imaging volume to eliminate the signal from spins entering in the unwanted venous
or arterial vessels.
A.
SatPulse
B.
MIP
C.
Venc
D.
Venetian blind
E.
Targeted MIP
2.
Two-dimensional TOF MRA consists of
A.
a signal that is based on the phase gained (or lost) as the spins move through
a magnetic field gradient.
B.
a signal that is acquired from a 3 to 6 cm thick slab.
C.
multiple 2 to 3 cm thick slabs covering the anatomy of interest.
D.
single slice gradient echoes, sequentially acquired in the direction
countercurrent to flowing blood.
E.
a series of acquisitions that are acquired following injection of gadolinium
3.
To image the jugular veins by 2D-TOF,
A.
you would want to start from the top and go down.
B.
you would start at the bottom and go up.
C.
you would acquire a 3 to 6 cm thick slab of the neck area.
D.
you would obtain a series of acquisitions following the injection of
gadolinium.
E.
you would obtain multiple 2 to 3 cm thick slabs that cover the neck area.
4.
The slice thickness in 2D-TOF techniques is generally on the order of ________
depending on the application.
A.
0.5 to 1 mm
B.
1 to 2 mm
C.
2 to 4 mm
D.
5 to 7 mm
E.
7 to 9 mm
5.
In 3D-TOF MRA,
A.
signal is acquired from multiple 2 to 3 cm thick slabs.
B.
the thinner slab increases the signal-to-noise (S/N) ratio compared to 2DTOF).
C.
the thinner slab improves spatial resolution.
D.
because the slab is thinner than the slices used for 2D-TOF MRA, the spins
may be exposed to more than one RF pulse.
E.
because the spins may be exposed to more than one RF pulse, this may lead
to loss of magnetization and saturation, eliminating signal from the vessel.
6.
In the gradient echo acquisition of 3D-TOF MRA, saturation effects are more
pronounced
A.
with smaller flip angles and shorter repetition times (TR).
B.
with smaller flip angles and longer repetition times (TR).
C.
with larger flip angles and longer repetition times (TR).
D.
with larger flip angles and shorter repetition times (TR).
E.
when the flip angles equal the repetition times (TR).
7.
In the gradient echo acquisition of 3D-TOF MRA, one of the ways to decrease the
saturation effects includes
A.
decreasing the flip angle.
B.
decreasing the TR.
C.
increasing the slab thickness.
D.
avoiding the use of gadolinium.
E.
the use of targeted MIP’s.
8.
MOTSA (Multiple Overlapping Thin Slab Acquisition)
A.
consists of a 3 to 6 cm thick slab covering the anatomy of interest.
B.
has the unlimited coverage of 2D-TOF.
C.
has the low spatial resolution of 3D-TOF.
D.
E.
is more efficient than 3D-TOF MRA.
will occasionally have minor saturation effects that remain, producing low
intensity bands at the junctions between the slabs known as “SatPulse’s”.
9.
When limited coverage is needed (for example, an evaluation of the circle of Willis in
an acute cerebral infarct),
A.
MOTSA is used.
B.
2D-TOF is used.
C.
2D-TOF followed by MOTSA is used.
D.
Phase contrast MRA is used.
E.
a single 3D-TOF slab is used.
10.
When greater coverage is required (for example, an evaluation of carotid artery
stenosis or to screen the entire brain for an aneurysm)
A.
a single 3D-TOF slab is used.
B.
multiple 3D-TOF slabs are used.
C.
MOTSA is used.
D.
Phase contrast MRA is used.
E.
Phase contrast MRA followed by 2D-TOF is used.
11.
Once a series of 2D or 3D slices has been acquired, to be displayed in angiographic
format,
A.
they are viewed directly as 64 separate images.
B.
they are scrolled consecutively on a workstation.
C.
a maximum intensity projection algorithm is generally used.
D.
Venetian blind artifacts must be produced.
E.
the Venc parameter must be set.
12.
One of the potential problems with the maximum intensity projection algorithm is
that it includes anything that is
A.
bright on the T1-weighted source images, including subacute hemorrhage
and fat.
B.
dark on the T1-weighted source images, including chronic hemorrhage and
cysts.
C.
bright on the T2-weighted source images, including hyperacute hemorrhage
and fibrous tissue.
D.
dark on the T1-weighted source images, except those entities that enhance
with gadolinium.
E.
bright on the T1-weighted source images, including bone and fibrous tissue.
13.
To determine if something is showing up on the MIP images that doesn’t represent
flowing blood,
A.
it may be desirable to acquire a phase contrast MRA.
B.
it may be desirable to acquire a 2D-TOF MRA.
C.
it may be desirable to acquire a 3D-TOF MRA.
D.
it may be desirable to acquire a MOTSA.
E.
it may be desirable to acquire an MRA that uses gadolinium.
14.
Which of the following statements is (are) true?
A.
The MIP algorithm has an S/N ratio threshold for what is included in the
image, so very large vessels and the residual lumen of tight stenoses may not
be visualized.
B.
Because the MIP algorithm may not visualize tight stenoses, it is important to
review the individual source images before diagnosing a complete stenosis.
C.
The source images are not useful in diagnosing the small lenticulostriate
collaterals in moyamoya disease.
D.
A & B above are true.
E.
B & C above are true.
15.
The phenomenon where the spins appear to be moving at maximum velocity in one
direction in one pixel and then, in the next pixel, they appear to be moving at
maximum velocity in the opposite direction, is called
A.
the Venc
B.
encoding velocity
C.
velocity aliasing
D.
the Satpulse
E.
Venetian blind artifacts.
16.
In PC MRA, the strength of the phase encoding gradient is determined by setting a
parameter called the
A.
Satpulse
B.
slab thickness
C.
MIP
D.
xyz gradient
E.
Venc
17.
Phase contrast MRA typically takes 4 times longer than a TOF technique with the
same TR and matrix, and for this reason, it is rarely used. In which clinical setting
listed below, might PC MRA be of use?
A.
A stenotic internal carotid artery
B.
Identifying the collaterals in moyamoya disease
C.
Identifying the vessels leading to a meningioma
D.
A ruptured dermoid
E.
A chronic subdural hematoma
18.
Contrast enhanced MRA has become the preferred technique for imaging arteries
everywhere in the body except for the
A.
kidney
B.
neck
C.
liver
D.
brain
E.
lower extremities
19.
Which of the following statements is (are) true regarding CE MRA?
A.
B.
C.
D.
E.
20.
With modern echo planar imaging capable MRI systems, the stronger, faster
gradients allow an image to be acquired during the brief time that gadolinium
is in the venous phase before it gets to the arteries.
CE MRA is essentially a time-of-flight technique without saturation effects.
In the standard k-space acquisition mode, the exact time of arrival of the
gadolinium bolus needs to be known.
When the exact time of arrival of the gadolinium bolus is known, an
“elliptical-centric” MRA technique (which is less sophisticated) allows a
lower resolution image to be acquired.
A & D above are true.
Some MR manufacturers also have automated bolus detection software to determine
when the gadolinium bolus arrives at the anatomic level of interest. This works
particularly well for
A.
carotid MRA
B.
circle of Willis MRA
C.
collateral detection in moyamoya disease
D.
collateral detection around a meningioma
E.
abdominal and runoff angiography