CME

JOURNAL OF MAGNETIC RESONANCE IMAGING 35:1274–1289 (2012)

Review: MR Physics for Clinicians

Gradient Echo Imaging

Michael Markl, PhD,1,2* and Jochen Leupold, PhD3

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1
Department of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA.
2
Department of Biomedical Engineering, McCormick School of Engineering, Northwestern University, Evanston, Illinois, USA.
3
Department of Radiology, Medical Physics, University Medical Center Freiburg, Freiburg, Germany.
*Address reprint requests to: M.M., Departments of Radiology and Biomedical Engineering, Northwestern University, 737 N. Michigan Ave.,
Ste. 1600, Chicago, IL 60611. E-mail: [email protected]
Received August 31, 2011; Accepted February 15, 2012.
DOI 10.1002/jmri.23638
View this article online at wileyonlinelibrary.com.

V
C 2012 Wiley Periodicals, Inc. 1274
Gradient Echo Imaging 1275

state free precession (bSSFP), unbalanced GRE, and

Magnetic resonance imaging (MRI) based on gradient ech-
oes is used in a wide variety of imaging techniques and RF spoiled gradient echo imaging. In addition, the
clinical applications. Gradient echo sequences form the effects of contrast agent, flow, magnetic susceptibility,
basis for an essential group of imaging methods that find and chemical shift are briefly reviewed and examples
widespread use in clinical practice, particularly when fast of the clinical application of different GRE techniques
imaging is important, as for example in cardiac MRI or are provided. For further details, the reader may con-
contrast-enhanced MR angiography. However, the term sult textbooks on MRI (20–22).
‘‘gradient echo sequence’’ is somewhat unspecific, as even
images acquired with the most common sequences
employing the gradient echo for data acquisition can sig- MR Spin Magnetization Dynamics
nificantly differ in signal, contrast, artifact behavior, and
sensitivity to, eg, flow. This is due to the different use of The MR signal is created by the nuclear proton spin
sequence timing and basic sequence building blocks such magnetization of 1H hydrogen atoms (23). Inside an
as spoiler gradients or specific radiofrequency (RF) pulse MR system the strong magnetic field B0 along the
phase patterns. In this article the basic principles of gra- z-axis of the scanner (direction of the magnet bore)
dient echo formation compared to spin echo imaging are will result in the alignment of a certain fraction of the
reviewed and the properties of gradient echo imaging in spin magnetization along the direction of B0. As a
its simplest form (TR  T2) are described. Further, the result, a net ‘‘thermal equilibrium’’ magnetization M
most common three variants of fast gradient echo sequen- directed along B0 is generated (Figure 2, left). The z-
ces (TR < T2), namely, unbalanced gradient echo, RF
component of M characterizes the magnetization that
spoiled gradient echo, and balanced steady state free pre-
cession; are discussed. For each gradient echo sequence
is available for signal generation, which can be con-
type, examples of applications exploiting the specific verted into transverse magnetization by RF excitation.
properties of the individual technique are presented. The application of RF excitation with a flip angle a
tips the available magnetization M toward the trans-
Key Words: gradient echo; balanced SSFP; steady state verse plane by the angle a (Figure 2, mid). The
free precession; RF-spoiling
J. Magn. Reson. Imaging 2012;35:1274–1289.
V
C 2012 Wiley Periodicals, Inc.

PRINCIPLES AND CONCEPTS of gradient echo (also

‘‘gradient recalled echo’’ [GRE]) imaging are the basis
of many applications on modern magnetic resonance
imaging (MRI) systems. Technically, the difference
between spin echo (1–3) and gradient echo imaging is
related to the pulse sequence elements that are used
to generate an MR signal (Figure 1). While two radio-
frequency (RF) pulses (90 and 180 ) are used for spin
refocusing and spin echo generation, GRE imaging is
based on only a single RF pulse, typically <90 , in
combination with readout gradient reversal (4–7). As a
result, shorter repetition times (TR) and therefore
faster imaging is feasible. Although signal formation
is also more sensitive to magnetic field inhomogeneity
caused by hardware-related imperfections of the main
magnetic field (shim) or properties of tissue (magnetic
susceptibility) (8–10), today’s advanced hardware,
particularly improved shim and gradient performance,
permits the successful application of GRE imaging
with reliable and reproducible image quality. Many
GRE-based applications such as dynamic (CINE) car-
diac imaging (11), MR angiography (12), assessment
of tissue perfusion or viability (13–16), or body or
musculoskeletal imaging (17,18) are an integral part Figure 1. Simplified spin echo (top) and gradient echo (bot-
of MR protocols used in routine clinical settings. tom) pulse sequence diagrams. The basic difference between
The purpose of this review is to provide an overview gradient echo and spin echo imaging is related to the fact
of the fundamental properties of GRE imaging and to that echo formation is a result of a single RF pulse and gra-
dient reversal while spin echo imaging uses two RF pulses,
describe the influence of the selection of imaging
ie, a second 180 pulse, for echo generation. As a result, the
parameters on signal, contrast, and typical artifacts.
gradient echo signal intensity is determined by T2 -decay
Next to the fundamental properties of gradient echo and, contrary to the spin echo T2-weighted signal intensity,
formation and their consequences regarding signal field inhomogeneity effects are not refocused at the time of
and contrast of basic GRE imaging (TR  T2), the signal formation. DAQ reflects the period of data acquisition.
three most common fast GRE techniques (TR < T2) See section Relaxation Effects for a more detailed description
(19) are discussed in this review: balanced steady of T2 and T2 -decay.
1276 Markl and Leupold

Figure 2. Spin magnetization

during thermal equilibrium
(a), after RF excitation (b), and
following the dephasing of the
transverse magnetization Mxy
(c).

resulting magnetization vector can be characterized the net detectable transverse magnetization Mxy is
by its remaining longitudinal component Mz along the reduced by this dephasing effect (the vector addition
direction of the main magnetic field and a transverse of the individual magnetization components with dif-
component Mxy in the plane orthogonal to the main ferent amount of rotation results in a reduced net
magnetic field B0. Once tipped in the transverse plane, transverse magnetization which determines the
Mxy continuously rotates around the main magnetic detectable signal for each voxel).
field with the Larmor frequency vL and induces a The dephasing of the transverse magnetization is
detectable MR signal, the so-called free induction decay governed by two independent processes. The decay
(FID) in a receive coil surrounding the object under time T 2* is composed of spin dephasing caused by
investigation. The speed of the rotation of Mxy (preces- static (time-invariant) dephasing effects (T20 -decay)
sion frequency vL) is directly determined by the local and nonconstant (time-variant) field fluctuations (T2-
magnetic field, ie, changes in the local magnetic field decay) as described by the following relationship:
due to tissue properties (regional differences in mag- 1 1 1
netic susceptibility, eg, at air–tissue interfaces) or hard- ¼ 0þ ½1
T2 T2 T2
ware imperfections (quality of the main magnetic field,
shim) will result in locally different rotation frequencies. T20 -decay reflects the dephasing due to temporally
unchanged magnetic field inhomogeneity. These origi-
nate from, eg, local differences of the magnetic prop-
Relaxation Effects
erties (described by the so-called susceptibility) of
The MR signal will persist as long as Mxy has a non- tissues, fluids, contrast agents, etc., or from hard-
zero component. Two different relaxation effects (T1- ware-related magnetic field imperfections (eg, shim).
recovery and T 2*-decay) will affect the amplitude of the In contrast, T2-decay is caused by stochastic and
signal. T1-recovery characterizes restoration of the temporal varying interactions between the magnetic
longitudinal magnetization Mz, ie, the magnetization moments of neighboring spins. Due to the stochastic
returns to its equilibrium magnetization M directed nature of this process, the dephasing effects associ-
along B0 by exchanging energy with its environment. ated with T2-decay cannot be reversed with a spin
Typically, T1 relaxation values are field strength- echo sequence. In contrast, dephasing caused by
dependent (longer T1 times at higher fields) and can deterministic T20 can be fully time-reversed with the
vary between 250 msec (fat at 1.5 T), 700–800 msec spin-echo.
(brain tissue at 1.5T), 1200 msec (blood at 1.5 T), and
up to 3–4 sec (cerebrospinal fluid at 1.5 T). Spin and Gradient Echo Formation
T1 relaxation can thus reduce the transverse mag-
netization Mxy. More important, however, local mag- For a spin echo experiment (Figs. 1, 3, top), two RF
netic field fluctuations and associated T 2*-effects will pulses (90 and 180 ) are used for echo generation.
result in dephasing of the transverse magnetization During the time between the 90 and 180 pulses, the
Mxy and a rapid signal decay on a much shorter time transverse magnetization Mxy starts to dephase
scale, within milliseconds to seconds (Figure 2, right). according to T20 and T2 effects. The second RF pulse
Based on local variations of the magnetic field due to with a flip angle of 180 , called a refocusing pulse, is
a variety of effects (susceptibility differences at air– used to flip over (invert) the magnetization which
tissue interfaces, imperfect shim, interactions reverses the rotation direction of all transverse mag-
between magnetic moments of neighboring spins) the netization components Mxy. Dephasing that has
transverse magnetization Mxy experiences different occurred as result of static (T20 ) effects, such as sus-
magnetic fields locally. As a result, the transverse ceptibility or field imperfections (9), is reversed. This
magnetization rotates at locally different frequencies process leads to the formation of a spin echo at echo
and, in a given amount of time, magnetization at dif- time TE when the T20 -dephasing has effectively been
ferent locations acquires different amounts of rotation nullified. Spin echo imaging thus compensates for
in the transverse plane (dephasing, Figure 3, right). static magnetic field effects and the signal strength is
The differences in amount of rotation occur on a small governed by the remaining T2-induced dephasing and
scale such that within each voxel of an MR image signal decay.
Gradient Echo Imaging 1277

Figure 3. Signal formation for spin echo (top) and gradient echo (bottom) imaging. Top: The 180 refocusing pulse for spin
echo imaging flips over magnetization and reverses the rotation direction of the transverse magnetization and results in a
compensation of dephasing caused by the T20 effect resulting in the rephasing of the magnetization at echo time TE. The col-
ored arrows represent exemplary magnetization vectors. Bottom: For gradient echo imaging, the dephasing is not reversed.
Signal and contrast are determined by both T20 and T2 effects. Note that shorter echo times are necessary for detectable gra-
dient echo signal intensity.

The situation is different for GRE imaging (Figs. 1, influence the signal and contrast. Note that T 2*
3, bottom), which uses a single RF pulse in combina- includes both T2 and static T20 -field effects (Figure 3)
tion with readout gradient reversal such that the net and is typically much shorter than T2 alone. As a
gradient area is zero at echo time TE. The gradient result, GRE signal intensity decays much faster and
echo sequence omits the formation of a spin echo and echo times have to be shorter than for spin echo
directly uses the signal from the free induction decay imaging in order to yield sufficient signal intensity.
following the RF excitation pulse. Mechanisms such In short, while spin echoes are RF-refocused and pro-
as field inhomogeneity or susceptibility are not refo- vide T2-dependent signal strength, GRE imaging is gra-
cused with the gradient echo at echo time TE and will dient refocused and has echo amplitudes determined
1278 Markl and Leupold

Figure 4. Steady state formation for basic GRE imaging (TR  T2). Repeated RF excitation results in a reduction of the longi-
tudinal magnetization (Mz) for consecutive repetition times (TR) until the steady state magnetization (MSS) is reached. Mxy
fully decays prior to each RF-excitation pulse and does not contribute to the steady state formation. The steady state magnet-
ization (MSS) which defines the signal intensity for basic GRE imaging is determined by T1, TR, and the flip angle a.

by T*2-decay (Figure 3). Note that the formation of a which determines the signal intensity for basic GRE
(gradient) echo instead of a pure FID leads to better imaging. Basic GRE images are thus T1-weighted and
quality of the magnitude image. The symmetric shape the signal intensity is determined by the ratio TR/T1
of the echo is beneficial to the Fourier transform.
Recording a pure FID (exponential decay) with a read-
out gradient only and without a preceding dephasing
gradient would be detrimental to image quality (24).

Basic GRE Imaging (TR  T2)

MRI typically consists of several repetitions of a basic
pulse sequence module with given repetition and echo
times TR and TE until all data for a complete 2D or
3D dataset are collected, as illustrated in Figure 4. As
a consequence, the timing of the acquisition, ie, TE
and TR relative to signal recovery (T1) and decay (T2,
T 2*), will determine signal intensity and contrast. A
gradient echo sequence acts as a pure progressive
saturation sequence on longitudinal magnetization
Mz, such that a so-called steady state will build up af-
ter several RF excitations.
To illustrate such a steady state formation, Figure 4
shows the temporal evolution of the magnetization
components Mz and Mxy over several pulse sequence
repetitions for basic GRE imaging with repetition
times TR much greater than T2. Due to the long TR,
the transverse magnetization Mxy (dashed lines) com-
pletely decays prior to each new RF excitation. How-
ever, since TR is typically shorter than, or on the
order of T1, the longitudinal magnetization (solid lines)
will not fully recover to its initial amplitude M0.
Instead, after several repetitions a new longitudinal
equilibrium magnetization MSS is reached, the
‘‘steady state.’’ The signal intensity in the MR image
is determined by the available longitudinal magnet-
ization MSS in the steady state that can be converted
into detectable MR signal. The steady state value MSS
can be calculated according to the so-called ‘‘Ernst
equation’’ (25):
Figure 5. Cranial images acquired with basic GRE imaging
TR=T1
(TR ¼ 500 msec, TE ¼ 4 msec, TR  T2) demonstrate signal
1e
MSS ¼ M0 ½2 and contrast behavior as a function of flip angle. PD, proton
1  e TR=T1 cos a density.
Gradient Echo Imaging 1279

Figure 6. Comparison of the three variants of fast gradient echo (GRE) imaging. Note that all three images were acquired
with short TE and TR. Unbalanced GRE (left) shows mixed T2/T1 contrast and cerebrospinal fluid (CSF) flow artifacts (signal
void, black arrows) due to its sensitivity to flow. In addition, CSF is clearly attenuated in the spinal cannel compared to
bSSFP. CSF flow acts in a similar way as RF spoiling and thus results in T1-weighted dark CSF signal. Pure T1 contrast can
be restored in RF-spoiled GRE (mid) accompanied by a loss in SNR. Balanced SSFP (right) provides high SNR and good fluid-
tissue contrast but banding artifacts (yellow arrows) demonstrate its sensitivity to local field inhomogeneity. [Color figure can
be viewed in the online issue, which is available at wileyonlinelibrary.com.]

and the flip angle a. Signal intensity can be maximized Practically, basic GRE imaging is often not very
for a given TR and T1 (ie, tissue) using an optimal flip favorable because the need for a long TR leads to long
angle a ¼ arccos[exp(-TR/T1)], also known as the acquisition times. However, the application of RF spoil-
‘‘Ernst angle.’’ In many imaging applications, optimiz- ing (see next section) offers the possibility of making
ing the signal from one tissue is not the major con- the Ernst equation valid for short repetition times TR.
cern. More important is optimizing the contrast
between two tissues (eg, lesion and healthy tissue). It
should be noted that even though the signal inten- Fast GRE Imaging (TR < T2)
sities may be optimal for certain Ernst angles, contrast
between tissues with different T1 is typically maxi- Fast GRE imaging refers to the situation where TR is
mized at higher flip angles (26,27). assumed to be short (TR  T1 and < T2), such that a
The steady state formation and relationship steady state of the magnetization has built up during
between T1, TR, and flip angle described above is the image acquisition (28–30). Since repetition times TR
reason why flip angles much smaller than 90 are typ- are short (<T2), the transverse magnetization Mxy does
ically chosen for GRE imaging as compared to spin not fully decay prior to each new RF pulse and there-
echo imaging for which maximum signal intensity is fore contributes to the steady state formation. In con-
provide by 90 –180 RF pulse pairs. trast to basic GRE imaging, both the longitudinal (Mz)
Figure 5 summarizes the signal and contrast behav- and the transverse (Mxy) magnetization determine the
ior for GRE imaging in the Ernst regime. Any T2 con- final steady state signal intensity. As for basic GRE,
tributions are minimized and images are predomi- signal intensities demonstrate strong flip angle de-
nantly T1-weighted. The highest signal intensities pendence but also more complex contrast behavior,
are typically found at low flip angles (between 40 depending not only on T1 TR, and but also T2 (29).
and 50 ). Tissue contrast, however, is optimized for For this review, three different types of fast GRE
larger flip angles (for example, gray and white mat- sequences are distinguished, depending on how the
ter contrast is maximized using flip angles between transverse magnetization is used during the sequence
60 and 80 ). TR, as illustrated in Figure 6.
1280 Markl and Leupold

Figure 7. Contrast-enhanced (CE) MR angiography (MRA) and assessment of myocardial perfusion using fast RF-spoiled GRE
imaging. a: Intravenous Injection of a Gd-based contrast agent results in T1-shortening in blood during the passage of the con-
trast agent bolus. b,c: The combination of appropriate synchronization of the measurement with the arrival of the arterial contrast
permits the acquisition of the contrast agent bolus passage with high arterial signal and contrast. RF-spoiled 3D GRE is ideally
suited for CE-MRA due to the possibility for rapid data acquisition with pure T1 contrast. CE-MRA can be applied in all vascular
regions throughout the body as illustrated for cervical and cranial arteries (left), the thoracic aorta (mid), and hand (right). d: The
first-pass arterial passage of contrast agent through myocardial tissue can monitored using ECG gated saturation recovery (SR)
fast 2D RF spoiled GRE. In typical clinical applications, 3–5 short axis slices are acquired per RR-interval permitting the measure-
ment of myocardial signal changes during contrast agent passage with a temporal update rate of one heartbeat. Prior to data ac-
quisition for each slice, a 90 SR pulse is used to enhance contrast between enhancing and nonenhancing tissue. The two short
axis images demonstrate an endocardial perfusion defect (arrows) during early (left) and late (right) arterial phases. [Color figure
can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Unbalanced GRE As for unbalanced GRE, a spoiler gradient is neces-

sary as well.
After the readout process, additional ‘‘spoiler’’ gra-
dients are used to effectively average over different
Balanced SSFP (bSSFP)
dephasing states of the transverse magnetization.
The net gradient area is nonzero but constant within The gradients are arranged such that the net gradient
each TR. area over one repetition time TR is zero along each
axis. This results in an efficient ‘‘recycling’’ of all avail-
able magnetization for MR signal generation but with
RF Spoiled GRE the undesirable result of increased sensitivity to field
inhomogeneities.
The phase of the RF pulses is systematically incre-
mented, leading to a steady state that is approxi- A more generic name for the whole family of fast
mately T1-weighted according to the Ernst equation. GRE sequences that is often used is ‘‘SSFP’’ (steady-
Gradient Echo Imaging 1281

tions. Nevertheless, the method represents an impor-

tant basis for fast GRE imaging. To address the
shortcoming of unbalanced GRE, two different fast
GRE variants have been developed: RF spoiled GRE
and balanced SSFP.

RF spoiled GRE. One of the key features of clinically

used fast GRE has been the ability to provide well-
defined T1 contrast while maintaining high imaging
speed. To enhance T1 contrast while maintaining the
short repetition times, TR, necessary for fast imaging,
a solution is provided by the so-called RF spoiling
technique (28,34–38). As shown in Figure 6 (mid), the
method is based on quadratically incrementing the
phase of the RF pulse from TR to TR, eg, resulting in
a phase f(n) of the n-th RF-pulse of f(n) ¼ n(n-1)v/2,
with a constant number v. The phase of an RF pulse
refers to the ‘‘tipping direction’’ when the magnetiza-
Figure 8. Time-resolved ECG-gated cardiac imaging with tion is flipped from the longitudinal direction to the
bSSFP and RF spoiled GRE. Improved image quality and
transverse plane and determines the orientation of
enhanced blood–tissue contrast for bSSFP are clearly visible.
the magnetization after the pulse in the transversal
Note the appearance of SSFP banding artifacts (arrows) visi-
ble as signal void in regions of increased field inhomogeneity. (x-y-) plane. It can be shown that for certain RF phase
LV, left ventricle; RV, right ventricle. increments (eg, v ¼ 117 or 50 ) the T2 contributions
from transverse magnetization can effectively be elimi-
nated. As a result, RF spoiled fast GRE sequences are
state free precession) (31). This term refers to magnet- predominantly T1-weighted. The signal intensity in RF
ization precessing freely (ie, without being exposed to spoiled GRE images effectively obeys the Ernst equa-
RF) between consecutive RF excitation pulses. In this tion in the same way as for the basic GRE sequence.
context, some confusion can result from nomencla- Note that RF spoiling does not destroy magnetization
ture of these sequences, as there are different acro- in the strict sense. Instead, RF spoiling manipulates
nyms used in the literature and by different vendors magnetization such that the vector addition of all
for one and the same sequence. Moreover, some acro- transverse magnetization components results in a
nyms have changed their meaning over the years (eg, zero net magnetization at the end of every sequence
the acronym FISP (32)). The only advice that can be interval.
given is to read publications thoroughly and to not Figure 6 shows a side-by-side comparison of RF
rely on the meaning of acronyms. An overview of fast spoiled GRE and an unbalanced GRE acquisition. It is
GRE techniques and most common vendor-specific evident that RF spoiling can successfully be used to
acronyms typically used for the different sequence eliminate T2 contributions and enhance T1 contrast
types is also provided in the review article by Elster while maintaining short TR. It should be noted, how-
(33) and in Figure 10. ever, that RF spoiled GRE carries an SNR penalty
since the transverse magnetization does not contrib-
Unbalanced GRE. The simplest form of fast GRE ute to the total MR signal.
imaging, unbalanced GRE, corresponds to the basic RF spoiled GRE sequences are a common work-
GRE pulse sequence with short TR (<T2) and ‘‘spoiler horse in the clinical routine and find a wide variety of
gradients’’ to provide sufficient dephasing of the trans- applications for which the availability of T1-contrast
verse magnetization. In the example in Figure 6 (left), in combination with short scan times is essential (eg,
spoiling is simply accomplished by lengthening the rapid imaging for large volumetric coverage). Impor-
readout gradient prior to application of the next RF tant applications include tissue perfusion imaging
excitation. Despite the spoiler effect, the transverse (15,16) or infarct imaging with delayed enhancement
magnetization does not fully decay before the execu- (13,14). In cardiovascular MRI, frequently employed
tion of the next RF pulse such that unbalance GRE clinical applications include first-pass myocardial
provides high signal-to-noise ratio (SNR) due to coher- perfusion imaging and contrast-enhanced MR angiog-
ent use of magnetization but offers complex T2/T1- raphy (39), which rely on the T1 shortening of contrast
contrast (as opposed to pure T1 contrast for basic agents in combination with fast imaging to capture
GRE with TR  T2) that may make image interpreta- the passage of an intravenous bolus injection (Figure
tion difficult. In addition, the complex interaction of 7). Historically, RF spoiling made fast T1-weighted
nondecayed transverse magnetization over several TR imaging possible and opened the door to numerous
intervals can result in flow-induced artifacts, as contrast-enhanced clinical applications.
shown in Figure 6 (left, black arrows). A remark on the term ‘‘gradient spoiling’’: Cancella-
The mixed T2/T1-contrast and sensitivity to flow tion of transversal magnetization components can
and motion artifacts are often problematic for clinical also be established by spoiler gradients varying along
applications. As a result, unbalanced GRE does not the slice-selection direction from TR to TR (40). How-
play an important role in routine clinical applica- ever, this ‘‘gradient spoiling’’ technique is less robust
1282 Markl and Leupold

Figure 9. Simulation of signal (left column) and gray matter/white matter contrast (right column) for various GRE
sequences.

than RF spoiling; therefore, it is rarely used in recent contrast (41,42). Compared to other GRE variants,
clinical GRE imaging methods (21,34). Gradient spoil- gradients are fully balanced (ie, gradient areas sum to
ing is conceptually different from the use of a constant zero over TR, see Figure 6, right), resulting in a more
spoiler gradient, which is used for both RF spoiled and efficient refocusing of the steady state magnetization
unbalanced GRE. Note that in unbalanced GRE and thus increased signal.
sequences, flow can also lead to T1-weighting, as it can However, bSSFP also exhibits a strong sensitivity to
act in a similar way as RF spoiling (eg, attenuation of local field offsets such as variations of the external
flowing CFS in Figure 6 in the spinal canal, left). field or regional susceptibility differences (off-reso-
nance sensitivity) (43). Signal and contrast for bSSFP
Balanced SSFP (bSSFP). A third fast GRE variant is imaging are a function of the local magnetic field. If
known as bSSFP imaging (17) and has gained the magnetic field is nonuniform, there can be regions
increased importance in a number of applications due in the image where the signal almost completely van-
to its superior SNR and in particular blood–tissue ishes (banding artifacts, see Figs. 6, 8).
Gradient Echo Imaging 1283

used until the late 1990s (17), when the necessary

gradient performance became available. Balanced
SSFP sequences are mostly used for, but not limited
to, body and cardiovascular MRI (17,42).
In addition to local field inhomogeneities, bSSFP is
sensitive to any disruption of the steady state, ie, by
interruption of the regularly spaced train of RF pulses.
For applications that rely on repetitive magnetization
preparation or added functionality, such as fat satura-
tion, tagging preparation, or navigator gating, the
steady state must be interrupted to include an appro-
priate preparation sequence. In order to avoid severe
disruption of the steady state magnetization, the RF
pulses and gradients necessary for the preparation are
typically embedded into a steady state storage scheme
(‘‘a/2 technique’’) as presented by Scheffler et al (44).
Figure 10. Fast gradient echo imaging variants, fundamen- Both RF spoiled GRE and balance SSFP are used for
tal signal and contrast properties and corresponding vendor- dynamic cardiac imaging. If data acquisition is gated
specific acronyms. or synchronized with the cardiac RR interval, time-
resolved (CINE) anatomical images can be collected to
In addition to the local field, the repetition time TR depict the dynamics of left and right ventricular func-
can substantially influence the spatial bSSFP signal tion during the cardiac cycle (45). For short TR, the
homogeneity. As TR is increased, image quality superior signal amplitude and improved blood-tissue
degrades and banding artifacts in areas of high local contrast of bSSFP is obvious from Figure 8. However,
field offsets become more and more prominent. A sensitivity of bSSFP to field inhomogeneities may result
combination of good field homogeneity (the so-called in signal variations and artifacts. The effects become
‘‘shim’’) and short repetition times is therefore crucial more prominent at higher fields (3 T and higher) such
for artifact-free bSSFP imaging. The short repetition that cardiac imaging with balanced SSFP has become
times needed by bSSFP can only be achieved with suf- the method of choice at 1.5 T, while RF spoiled GRE,
ficiently fast switching and strong gradients. This is which is less sensitive to local field variations, is often
the reason why bSSFP imaging did not become widely used at 3 T. Figure 8 shows results from an

Figure 11. T2 -effects in GRE imaging illustrated for basic multislice 2D GRE (TR  T2) for two images at different axial loca-
tion in the head. The GRE images are compared to spin echo (SE) images at identical anatomical locations using the same
echo and repetition times. For short TE ¼ 4.1 msec, both GRE and SE images are predominantly proton density (PD)-
weighted, show similar contrast, and no or only minor artifacts. Increasing echo time to TE ¼ 30 msec, GRE images show
overall signal reduction and marked signal loss in regions which have high susceptibility variations (air–tissue interfaces,
white arrows). In contrast, spin echo imaging is insensitive to these effects. Note that long echo times result in T2 contrast for
SE images while GRE images are T2 -weighted. All images were acquired at 1.5T.
1284 Markl and Leupold

Figure 12. Examples of the application of T2 -weighted gradient echo imaging. a: Cranial 2D GRE with long echo times reveal
hemosiderin deposits as a result of microbleeds (white arrows) after stroke. b: Functional MRI used GRE with long echo times
to detect changes in regional blood T2 based on to changes in local blood oxygenations levels related to neuronal activity
(BOLD effect).

electrocardiogram (ECG)-gated dynamic study of car- plex T2/T1-contrast and is sensitive to flow and motion
diac motion in the four-chamber view. Note the high artifacts. T1 contrast is enhanced by the application of
SNR and also blood–tissue contrast of bSSFP (bottom RF spoiling but overall signal intensity is considerably
row) as compared to RF spoiled gradient echo imaging reduced. Balanced SSFP imaging can offer the highest
(top row). signal but suffers from strong sensitivity to local field
changes and also provides mixed T2/T1 contrast (43).
Comparison of Fast GRE Techniques
T *2 and Off-Resonance Effects
Figure 9 provides an overview of the signal and con-
trast characteristics for all three fast GRE techniques One of the fundamental differences between GRE and
and basic GRE as a function of the flip angle used for spin echo imaging is related to the fact that phase
RF excitation. Simulations based on Bloch equations shifts from local magnetic field inhomogeneities are
have been employed to calculate signal and contrast not refocused in GRE imaging and lead to signal
of brain white matter (WM) and gray matter (GM). decay governed by T 2*.
Relaxation times at 1.5 T (20) are: WM: T1 ¼ 600 In general, GRE images are thus more sensitive to
msec, T2 ¼ 80 msec; and GM: T1 ¼ 950 msec, T2 ¼ artifacts due to changes in magnetic susceptibility
100 msec. Three different repetition times were simu- (46). For long echo times, signal loss can be severe, as
lated: TR ¼ 6 msec ( T2); TR ¼ 60 msec (T2); TR ¼ shown by the GRE images in Figure 11, where it is
180 msec (>T2, <T1). Contrast is simply the difference demonstrated that a longer TE leads to an overall
in signal amplitudes between WM and GM. decline in signal intensity and almost complete signal
RF spoiled GRE shows signal behavior according to dropout in the frontal region with increased field
the Ernst equation, with maximum GRE signal at the inhomogeneity resulting from high susceptibility dif-
Ernst angle. The maximum shifts to lower flip angles ferences. For comparison, spin echo imaging is inde-
with shorter TR. Note that at the Ernst angle all three pendent of these effects.
sequence variants exhibit the same signal intensity. However, T 2*-sensitivity of GRE imaging can also be
For longer TR, the signal curves become more and beneficial and used to generate new diagnostic infor-
more similar, with maximum signal intensity shifting mation, as shown in Figure 12. For example, T 2*-con-
closer to 90 . Contrast increases with longer TR, and trast is used in functional MRI (fMRI) where changes
is highest for RF spoiled GRE for intermediate and in blood oxygenation that lead to alterations in T 2* are
long TR. Simulations confirm the finding from Figure used to analyze brain activation (Figure 12b) (47,48).
5, contrast of RF spoiled GRE is maximized for flip Another widely used application involves the detection
angles higher than the Ernst angle (26,27). of bleeding in stroke patients. Microbleeds in such
The basic properties and commonly used acronyms patients lead to local field alterations and therefore
of the three most widely used fast GRE techniques T *2-changes that can be visualized as signal drop-
are summarized in Figure 10. Unbalanced GRE outs using GRE techniques (49) with long echo
demonstrates high signal but rather low and com- times (Figure 12b). Since such bleeds are very small
Gradient Echo Imaging 1285

Figure 13. a: Principe of fat water imaging based on in-phase and out-of-phase images for GRE imaging with different echo
times TE. Fat and water images calculated for the in-phase/out-of-phase data. b: Cardiac fat-water imaging in four-chamber
orientation clearly showed intraarterial lipomatous signal as visible in the fat image and absent in the water image (white
arrows). Fat-water imaging permitted an improved characterization of this lesion compared to standard GRE imaging (left).

and hardly detectable with any other imaging mo- which depends on the echo time TE. Of special impor-
dality, T *2-GRE imaging is often part of the clinical tance are the in-phase (fat and water magnetization
routine workup of stroke patients. Furthermore, T *2 are aligned and add) and the out-of-phase (fat and
differences are also exploited in susceptibility- water magnetization are opposed and cancel) condi-
weighted imaging (SWI) (50). Additional applications tions. For a 1.5 T magnet, images can be produced
include the analysis of the T *2-dynamics in contrast that provide contrast generated by opposed (TE ¼ 2.2
agent studies (51) that can be used to generate brain msec, 6.6 msec,. . .) and aligned fat and water spins
perfusion maps (52,53) such as regional cerebral (TE ¼ 4.4 msec, 8.8 msec,. . .).
blood volume and flow. Figure 13a shows an example of in-phase/out-of-
A second important effect acting on the observed phase images, which can be used to analyze fat and
signal intensity of gradient echo sequences is the water content in different tissues (54). Since fat and
chemical shift. Due to the frequency difference of water signal add in the in-phase image, signal inten-
water and fat (220 Hz at 1.5 T, 440 Hz at 3 T), their sities are typically higher than in the out-of-phase
magnetization vectors exhibit a phase difference, images. Note the occurrence of dark rims at the
1286 Markl and Leupold

Figure 14. In-flow enhancement in GRE imaging results in bright signal of blood entering the imaging slice. In combination
with saturation of static tissue this effect can be exploited to provide high blood-tissue contrast as in TOF MR angiography.
[Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

interface between fatty and aqueous tissues when TE (steady state formation), resulting in saturated and
is chosen to correspond to the out-of-phase condition. consequently reduced signal intensities. Then signal
The signal void represents partial volume effects in behaves according to the steady state simulations for
pixels with roughly equal fat and water content which which typical examples have been shown in Figure 9.
cancel and lead to signal void. Furthermore, the infor- In contrast, blood that flows into an imaging slice has
mation in both images can be combined and proc- not experienced a sufficient number of previous RF
essed for effective fat–water separation (55–57), eg, for excitations to build up a steady state. This will lead to
imaging of joints for cartilage analysis (58), diagnosis signal enhancement, ie, in-flow of unsaturated mag-
of fatty liver disease (59), or lesion characterization as netization results in bright signal of blood as typically
shown in Figure 13b. observed in fast GRE imaging.
This manifestation of the chemical shift must not Such inflow enhancement can be beneficial and
be confused with the so-called ‘‘chemical shift misre- used to acquire additional diagnostic information as,
gistration’’ artifact (22), which occurs in GRE as well for example, shown in Figure 14 for time-of-flight
as in SE sequences. In this context, chemical shift (TOF) techniques (60,61). The in-flow enhancement is
can cause a spatial misregistration of fat versus used to separate arterial or venous signal from static
water tissue depending on the bandwidth of the tissue or background signal to generate angiograms.
pulse sequence. Here the optimal flip angle for high blood/tissue con-
trast is usually higher than for static tissues such as
the example of gray and white matter shown in Figure
5. Additionally, background (static tissue) suppres-
Flow Effects
sion techniques such as magnetization transfer pulses
Since signal intensity in GRE imaging is determined can be employed (62).
by repeated RF excitation, any static tissue will typi- In-flow can also lead to image artifacts such as mis-
cally not fully recover prior to the next excitation registration and ghosting (22) that arises if laminar or
Gradient Echo Imaging 1287

Figure 15. Left: Magnetization preparation by inversion recovery (IR) for enhanced T1 contrast as in delayed enhancement
cardiac MRI. To improve contrast between tissue with and without contrast agent uptake, the inversion time (TI) can be
selected to null nonenhancing myocardial tissue (long T1). Contrast agent that accumulates in infarcted tissue results in
shorter T1 and high GRE signal. Right: Delayed enhancement images of the left ventricle (LV) in a patient with myocardial in-
farction. Bright areas (arrows) mark regions with contrast agent accumulation in irreversibly damaged myocardial tissue.
[Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

pulsatile flow leads to amplitude or phase inconsis- clinically important example of an inversion recovery
tencies. A solution to this problems is offered by flow application is the ‘‘delayed hyper-enhancement’’ tech-
compensation techniques (63), which can eliminate nique (65), which is used to identify infarcted and
artifacts but lead to an increase in echo and repetition nonviable tissue in patients with coronary artery dis-
times TE and TR. ease. Here, the inversion time TI is selected such that
the myocardial signal is nulled and only contrast
agent that accumulates in infarcted tissue—and has
Magnetization Preparation
much shorter T1—appears bright in the GRE images
The intrinsic contrast of GRE imaging techniques may (Figure 15).
not be sufficient, for example, when using short TRs.
In this case, as can be seen from Figure 9, signal and
contrast are rather poor for unbalanced and RF DISCUSSION
spoiled GRE. A potential solution is offered by mag-
netization preparation methods, which are used to In this review the basic principles of GRE imaging and
imprint T1 or T2 contrast onto the longitudinal mag- the most commonly used techniques for fast GRE
netization Mz and enhance the desired contrast and data acquisition have been presented. A brief sum-
signal amplitude. A frequently used technique is mary of GRE properties is provided in Figure 16.
shown in Figure 15, which illustrates enhanced T1 Noticeably, the signal of a gradient echo sequence is
weighting by inversion recovery imaging (64). Before sensitive to various T 2*-effects, which—contrary to
the actual start of GRE imaging, a 180 inversion spin echo acquisition—are not refocused at the time
pulse is applied preceding data acquisition by the of signal detection.
time-interval or inversion time TI. Depending on T1 of Signal and contrast for basic GRE imaging (TR 
the tissue and the TI time, certain T1 species can be T2) depend on the formation of a steady state that is
enhanced, suppressed, or even nulled. For cranial governed by the Ernst equation. T2-contribution can
imaging, magnetization prepared rapid gradient echo be ignored, resulting in relatively simple contrast
(MP-RAGE) is often used clinically for anatomical behavior depending on TR, T1, and the flip angle.
imaging of the entire head with T1-contrast. Another Due to the long TRs (on the order of several 100
1288 Markl and Leupold

tions. Second, the broad variety of contrast behavior

and sensitivity to other influences such as flow makes
it possible in a large number of cases to find a suita-
ble gradient echo sequence as the matter of choice.
Third, due to their robust and reliable image quality,
GRE sequences can be used as acquisition modules
in combination with various magnetization prepara-
tion modules.

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