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Magnetic Resonance in Medicine 51:243–247 (2004)
Fat and Water Separation in Balanced Steady-State Free
Precession Using the Dixon Method
Teng-Yi Huang,1–2 Hsiao-Wen Chung,1,2* Fu-Nien Wang,1 Cheng-Wen Ko,1,3 and
Cheng-Yu Chen2
In this work the feasibility of separating fat and water signals
using the balanced steady-state free precession (SSFP) technique is demonstrated. The technique is based on the observation (Scheffler and Hennig, Magnetic Resonance in Medicine
2003;49:395–397) that at the nominal values of TE ⴝ TR/2 in
SSFP imaging, phase coherence can be achieved at essentially
only two orientations (0° and 180°) relative to the RF pulses in
the rotating frame, under the assumption of TR << T2, and
independently of the SSFP angle. This property allows in-phase
and out-of-phase SSFP images to be obtained by proper
choices of the center frequency offset, and thus allows the
Dixon subtraction method to be utilized for effective fat–water
separation. The TR and frequency offset for optimal fat–water
separation are derived from theories. Experimental results from
healthy subjects, using a 3.0 Tesla system, show that nearly
complete fat suppression can be accomplished. Magn Reson
Med 51:243–247, 2004. © 2004 Wiley-Liss, Inc.
Key words: fat–water separation; Dixon method; in-phase and
out-of-phase images; steady-state free precession; frequency
offset
The advantage of increased signal-to-noise ratio (SNR) efficiency in balanced steady-state free precession (SSFP)
imaging (also denoted as true fast imaging in steady-state
precession (TrueFISP), balanced fast field-echo (FFE), or
fast imaging employing steady-state acquisition (FIESTA)
by various manufacturers) has made this technique attractive for clinical applications. Examples of such applications include (but certainly are not limited to) cardiac
imaging (1,2), angiography (3,4), gastrointestinal imaging
(5,6), and fetal imaging (7). In certain situations, the signal
from fat protons is a major source of interference that
hinders our ability to interpret the image unambiguously.
This is understood because fat has a higher T2/T1 value
compared to parenchymal tissues, which corresponds to
bright steady-state signals on SSFP images (8). Therefore,
1
Department of Electrical Engineering, National Taiwan University, Taipei,
Taiwan, R.O.C.
2
Department of Radiology, Tri-Service General Hospital, Taipei, Taiwan,
R.O.C.
3
Department of Computer Science and Engineering, National Sun Yat-Sen
University, Kaohsiung, Taiwan, R.O.C.
Grant sponsor: National Science Council; Grant number: NSC-91-2213-E002-078; Grant sponsor: National Center for Research Resource; Grant number: P41RR14075; Grant sponsors: Mental Illness and Neuroscience Discovery (MIND) Institute; Ministry of Education; National Science Council.
T.-Y. Huang and F.-N. Wang are now at the Massachusetts General Hospital,
MGH/MIT/HMS Athinoula A. Martinos Center for Biomedical Imaging,
Charlestown, Massachusetts.
*Correspondence to: Hsiao-Wen Chung, Ph.D., Department of Electrical Engineering, National Taiwan University, Rm. 238, No. 1, Sec. 4, Roosevelt
Road, Taipei, Taiwan 10764, R.O.C. E-mail: [email protected]
Received 28 April 2003; revised 26 June 2003; accepted 26 September 2003.
DOI 10.1002/mrm.10686
Published online in Wiley InterScience (www.interscience.wiley.com).
© 2004 Wiley-Liss, Inc.
for SSFP imaging applications intended to highlight fluids
with large T2/T1 values, such as angiography, myelography, and MR cholangiopancreatography (MRCP), it is essential to eliminate the fat signals.
Fat suppression in SSFP imaging can be accomplished
by using frequency-selective RF pulses in every TR, similarly to the conventional approach used in spin-echo imaging (5). This method increases TRs that are ordinarily
short in generic SSFP sequences, and thus increases total
scan time by a noticeable factor. Alternatively, magnetization preparation during the steady state, which refers to
the addition of one fat-suppression pulse every several
TRs, has also been shown to be effective (9). The latter
method is advantageous in that the scan time is not significantly increased, which is beneficial for 3D examinations.
Other methods, such as linear combination SSFP (10) and
fluctuating equilibrium MR (11), have been proposed that
make use of the SSFP spectral profiles manipulated by
different RF phase schemes to selectively reconstruct different spectral species. For 2D imaging, the use of a single
fat-suppression RF pulse followed by a centric-ordered
SSFP readout should serve the same purpose well, with
the exception that the resulting image contrast is inevitably altered to proton-density weighting due to the transient-state signal behavior (12).
In a recent work, it was shown that SSFP images exhibit
spin-echo-like behavior, such that spin isochromats at
similar resonant frequencies show phase coherence at either 0° or 180° relative to the RF pulses at the time TR/2,
the nominal TE in SSFP imaging (13). For off-resonance
species, such as fat relative to water, the SSFP angle (i.e.,
the precession phase angle for the spin isochromats within
one TR in the rotating frame) can be manipulated by adjusting the center reference frequency, which in turn determines the directional location for phase coherence in
the rotating frame (13). This property leads naturally to the
use of in-phase and out-of-phase images for Dixon addition/subtraction to achieve fat–water separation in SSFP
imaging (14). In this study, we demonstrate the feasibility
of separating fat and water signals in SSFP imaging using
the Dixon method in vivo at a high magnetic field (3.0
Tesla). We note that certain cautions should be used with
this approach, and describe optimal off-resonance ranges
using both theories and experimental results.
METHODS AND MATERIALS
Theories
The current technique is based on the observation that at
the nominal values of TE ⫽ TR/2, SSFP images show
spin-echo-like phase coherence at only two orientations,
under the assumption of TR ⬍⬍ T2 (13). The steady-state
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transverse magnetization immediately after the RF pulse,
Mx⫹ and My⫹, can be expressed as a function of TR, T1, T2,
flip angle ␣, and the SSFP angle ␪ within one TR, given by
(8):
M x⫹ ⫽ M 0共1 ⫺ E 1兲共E 2 sin␣sin␪)/D
[1]
M y⫹ ⫽ M 0共1 ⫺ E 1兲关共1 ⫺ E 2 cos␪)sin␣]/D
[2]
with
D ⫽ 共1 ⫺ E 1cos␣)(1⫺E2 cos␪)
⫺(E1 ⫺ cos␣)(E2 ⫺ cos␪)E2
[3]
E 1 ⫽ e ⫺TR/T 1
[4]
E 2 ⫽ e ⫺TR/T 2,
[5]
where M0 is the magnetization at thermal equilibrium, and
␪ includes the effects of chemical shift and RF phasing. It
can be shown that the transverse magnetization at TE ⫽
TR/2 shows phase coherence at 0° relative to the RF pulses
for 4n␲ ⬍ ␪ ⬍ (4n ⫹ 2)␲ in the rotating frame, or at 180°
relative to the RF pulses for (4n – 2)␲ ⬍ ␪ ⬍ 4n␲, where n
is an arbitrary integer. Figure 1 shows the signal intensity
and the phase angle relative to the RF pulses, plotted as a
function of the off-resonance frequency for muscle (water)
and fat protons, respectively, assuming 180° phase alternations for the RF excitation pulses (13). The calculations
were performed for TR ⫽ 3.4 ms at 3.0 Tesla (the rationale
for choosing TR ⫽ 3.4 ms is explained below). It is seen
from Fig. 1 that in-phase and out-of-phase images at the
chosen TR are both obtainable by appropriately adjusting
the center frequency offset, if shimming can be performed
satisfactorily (13). For example, an off-resonance of 0 to
–120 Hz would lead to out-of-phase images, whereas an
off-resonance of 20 –130 Hz would result in in-phase images. This property justifies the use of the Dixon method
for fat–water separation using SSFP at otherwise identical
scanning parameters.
However, one should note that not all TRs are eligible
for the proposed Dixon method. In particular, at TR equal
to the inverse of the chemical shift (2.24 ms at 3.0 Tesla),
it has been shown that the water and fat protons would
always be out of phase in an SSFP image (15). In other
words, in-phase images would not be obtainable. This is
understood because a TR of 2.24 ms introduces a difference of 2␲ in the SSFP angles for water and fat. By the
same token, at TR equal to an even multiple of 2.24 ms, the
water and fat protons would always be in phase. On the
other hand, if one selected a zero frequency offset for water
at TR ⫽ 3.4 ms at 3.0 Tesla, the fat signal would be close to
its minimum intensity, as shown in Fig. 1a. In this situation, since the exact “null point” for fat is very sensitive to
the local magnetic field strength, the difficulty of obtaining
homogeneous intensity for fat at this frequency offset
would lead to imperfections in signal cancellation from
in-phase and out-of-phase images. Fat–water separation
would thus be nonideal. To address the issues of TR se-
FIG. 1. Signal intensity (a) and the phase angle relative to the RF
pulses (b) in the steady state plotted as a function of center frequency adjustment in units of Hertz for muscle (water) and fat
protons, respectively, assuming 180° phase alternations for the RF
excitation pulses. The calculations were performed with TR ⫽
3.4 ms and TE ⫽ TR/2 at 3.0 Tesla, at a flip angle of 24° (the same
parameters as used in the experiments). It can be seen that inphase images (regions showing overlapped curves in b) and outof-phase images (regions showing 180° separation in b) are both
obtainable by carefully adjusting the off-resonance frequency, even
using the same TE and TR values. This illustrates the feasibility of
using the Dixon method for fat–water separation.
lection and heterogeneity in signal intensity, we performed the following analysis:
Equations [1]–[5] were used to calculate the signal intensity and phase angle for muscle (water) and fat at 3.0
Tesla as a function of center frequency offset from –200 Hz
and ⫹200 Hz. A 180° phase alternation for the RF pulses
was assumed, since that is often used in SSFP imaging.
The ranges of frequency offset that yielded low signal
intensity for either water or fat were marked out as “not
recommended for SSFP Dixon imaging” because signal
heterogeneity would likely cause imperfect signal cancellation in the Dixon method. “Low signal intensity” was
defined as ⬍70% of the SSFP signal at ␪ ⫽ 180° (e.g., the
Fat–Water Separation With SSFP Dixon Imaging
245
flat regions in Fig. 1a). For the remaining frequency offsets
that provided fairly uniform signals for both water and fat,
the phase angles of the two species were examined. The
above process was repeated for TR ⫽ 2.0 –7.0 ms. Thus, a
graph was generated that showed the in-phase or out-ofphase behavior as a function of TR and frequency offset.
The TR value showing equally wide ranges of frequency
offset for both in-phase and out-of-phase behavior was
regarded as the optimum TR for SSFP Dixon imaging, and
was therefore chosen for the experiments. The middle
frequency values in the offset ranges for in-phase and
out-of-phase images were regarded as the optimal center
frequency offsets because they were far from the null signal regions for both fat and water.
Image Acquisition
Abdominal imaging was performed on eight healthy adults
(seven males and one female, 23–38 years old) who volunteered to participate in this study. Experiments were
performed on a 3.0 Tesla MRI system (Siemens Trio, Erlangen, Germany). Transaxial SSFP images at about the
kidney level were acquired using a 2D TrueFISP sequence
with TR/TE ⫽ 3.4/1.7 (TR chosen according to results
obtained from the theoretical analysis), flip angle ⫽ 24°,
field of view (FOV) ⫽ 340 mm, matrix ⫽ 256 ⫻ 256, slice
thickness ⫽ 5 mm, and four signal averages. The halfangle-half-TR preparation scheme was used before RF excitation, along with a linear phase-encoding order (16).
Note that at the matrix size chosen in this study, the image
contrast can be regarded as being largely dominated by the
steady-state signal response (12). The body coil was used
for signal receiving. Scan time was ⬍1 s per slice for each
signal average. Three-dimensional shimming was performed before the SSFP data were acquired in all cases to
ensure maximum field homogeneity. Off-resonance was
achieved by adjusting the RF center frequency from
–100 Hz to ⫹100 Hz (corresponding to a ⫾0.68␲ change in
␪ at the chosen TR) at a 20-Hz step. The RF specific absorption rate was estimated with the use of the manufacturer-supplied software, and the FDA-recommended limitations were not exceeded. During imaging and shimming,
the subjects were asked to hold their breath at end expiration to ensure consistent acquisition locations. The image
raw data (before the absolute magnitude was taken) were
digitally transferred to a personal computer for calculation. Summation of the in-phase and out-of-phase images
yielded the water-only image, whereas subtraction gave
the fat-only image.
RESULTS
Figure 2 shows the phase behavior for muscle and fat at 3.0
Tesla as a function of TR and center frequency offset. The
stripe-like regions correspond to those that are not recommended for use in Dixon imaging because the signals from
either muscle or fat (or both) are close to zero, and hence
are likely to cause imperfect signal cancellation or shimming difficulties. From Fig. 2 it can be seen that at TRs
equal to odd multiples of 2.24 ms (i.e., the inverse of the
chemical shift frequency), the SSFP images would always
show out-of-phase behavior, consistent with results from a
FIG. 2. Graph showing the phase behavior for muscle and fat in
SSFP images at 3.0 Tesla (flip angle ⫽ 24°, 180° phase alternations
for the excitation RF pulses) as a function of TR and center reference frequency offset. The abbreviations “ip” and “op” represent
in-phase and out-of-phase behavior for muscle and fat, respectively. The stripe-like regions correspond to those that are not
recommended for use in Dixon imaging because the signals from
muscle or fat (or both) are close to zero, and hence are likely to
cause imperfect signal cancellation or shimming difficulties. At TR
equal to odd multiples of 2.24 ms (i.e., the inverse of the chemical
shift frequency difference), the SSFP images would always show
out-of-phase behavior, whereas at TR equal to even multiples of
2.24 ms, muscle and fat would always be in phase. The vertical
dashed line corresponds to the experimental condition (TR ⫽
3.4 ms, about halfway between 2.24 ms and 4.48 ms) used in this
work. The different center frequency offsets yield half in-phase and
half out-of-phase SSFP images, and thus are optimal for Dixon
imaging.
previous report (15). In contrast, at TRs equal to even
multiples of 2.24 ms, muscle and fat would always be in
phase. Thus it becomes clear that the choice of TR ⫽
3.4 ms (about halfway between 2.24 ms and 4.48 ms) is
close to the situation where equal ranges of center frequency offset can be used to obtain both in-phase and
out-of-phase images (vertical dashed line in Fig. 2). Therefore, a TR of 3.4 ms was selected for all experiments
performed in this study. Furthermore, at TR ⫽ 3.4 ms, the
frequency offsets of ⫹80 Hz and – 80 Hz are optimal for
in-phase and out-of-phase imaging, respectively, because
the obtained images are relatively immune to intensity
heterogeneity near the null signal points.
Figure 3a– e show the series of abdominal images from
one male subject (27 years old) at different RF off-resonance frequencies (– 80 Hz, – 40 Hz, 0 Hz, ⫹40 Hz, and
⫹80 Hz). As the off-resonance frequency changes from
– 80 Hz to ⫹80 Hz, one can observe from the boundaries of
the kidneys that the images change from out-of-phase to
in-phase in appearance. Of note, in the ⫹40 Hz image (Fig.
3d), the right kidney demonstrates out-of-phase characteristics (long arrow), whereas the left kidney shows in-phase
characteristics (short arrow). This is obviously due to
shimming imperfections resulting in different effective offresonance frequencies across a large FOV. In addition, a
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Huang et al.
FIG. 3. Abdominal SSFP images acquired at different off-resonance frequencies: (a) – 80 Hz, (b) – 40 Hz, (c)
0 Hz, (d) ⫹40 Hz, and (e) ⫹80 Hz. As the
off-resonance frequency changes from
– 80 Hz to ⫹80 Hz, one can observe from
the boundaries of the kidneys that the
images change from out-of-phase to inphase in appearance. In image d in particular, the right kidney demonstrates
out-of-phase characteristics (long arrow), whereas the left kidney shows inphase characteristics (short arrow). A
dark band in the fat region can be seen
between the two kidneys (open arrow),
consistent with the theoretical prediction
shown in Fig. 2. The on-resonance image (c) also shows an obvious dark band
within the left-side subcutaneous fat.
dark band in the fat region can be seen between the two
kidneys (open arrow), showing the presence of the null
point for fat protons, consistent with the theoretical prediction shown in Fig. 1. The on-resonance image in Fig. 3c
also shows an obvious dark band within the left-side subcutaneous fat. These images both represent situations in
which fat protons are near the null points in Fig. 1 (␪ ⬃
2n␲, where n is an arbitrary integer).
Figure 4a and b show the water-only and fat-only images, respectively, obtained from the ⫹80 Hz in-phase and
the – 80 Hz out-of-phase images in Fig. 3. Nearly complete
fat suppression can be seen in Fig. 4a. Note that although
the on-resonance image in Fig. 3c is also out-of-phase in
characteristics, the presence of banding would result in
incomplete fat cancellations if Fig. 3c were used along
with Fig. 3e to form the water-only image (result not
shown). This is in good agreement with our theoretical
prediction from Fig. 2. Figure 4c shows a fat-suppressed
image on the same slice location, acquired via one single
fat-suppression RF pulse followed by a 2D SSFP readout
with centric phase encoding (i.e., the manufacturer-supplied fat-suppression TrueFISP sequence). Note in particular the change of image contrast in Fig. 4c to protondensity weighted, compared with the T2/T1 weighting in
Fig. 4a, which provides much better contrast between the
muscle and kidneys.
DISCUSSIONS AND CONCLUSIONS
We have presented a Dixon-based method for fat–water
separation using in-phase and out-of-phase SSFP imaging.
We analyzed the in-phase/out-of-phase behavior as a function of TR and center frequency offset at 3.0 Tesla, and also
derived the optimum TR and offset values for SSFP Dixon
imaging. Unlike the Dixon method used in conventional
gradient-echo imaging (14), SSFP Dixon imaging employs
the concept of spin-echo-like phase coherence at TE ⫽
TR/2 (13). This phase coherence is dependent on the SSFP
angle, which is tunable via adjustments of the center reference frequency. One notices that for a wide range of
SSFP angles, there are essentially only two orientations in
which phase coherence occurs (i.e., 0° and 180°) relative to
the RF pulses (Fig. 1). Consequently, the exact value of the
off-resonance frequency chosen to form in-phase or out-ofphase images is not critically important, as long as the
low-signal region can be effectively avoided (Fig. 2). This
idea is supported by our experimental results, which indicate that nearly complete fat–water separation was
achievable at ⫾80 Hz off-resonance. These off-resonance
frequencies corresponded (Figs. 1 and 2) to situations in
which both fat and water signal phases were relatively
insensitive to slight changes in the SSFP angle due to
shimming imperfections.
FIG. 4. (a) Water-only and (b) fat-only SSFP images obtained using the Dixon method from the ⫹80 Hz in-phase and the – 80 Hz
out-of-phase images in Fig. 3. Shown in part c for comparison is a fat-suppressed image on the same slice location, acquired via one single
fat-suppression RF pulse followed by a 2D SSFP readout with centric phase encoding (manufacturer-supplied fat-suppression TrueFISP
sequence). Note that the image contrast in c is basically proton-density weighted (transient-state contrast), as opposed to the better
contrast (e.g., between muscle and kidney) provided by the steady-state T2/T1 weighting in a.
Fat–Water Separation With SSFP Dixon Imaging
Fat suppression in SSFP imaging can be accomplished
by several other approaches (5,9,15). The use of a frequency-selective RF pulse to achieve either fat suppression or
water excitation (5) appears to be a straightforward technique for that purpose. However, since frequency-selective
RF pulses generally have a long duration, on the order of
several milliseconds (i.e., the inverse of the fat–water
chemical shift), the employment of these RF pulses in
every TR inevitably increases the minimum TR values
substantially, from about 4⬃5 ms to 6⬃8 ms. The resulting
increase in the total scan time is already on the same order
(i.e., a factor of 2 increase) as that in SSFP Dixon imaging.
In addition, increases of TR in SSFP imaging may hurt
image quality by introducing banding artifacts, particularly at higher magnetic fields (e.g., 3.0 Tesla). At such
fields, shimming is more difficult to perform than at lower
fields because of strong susceptibility effects.
Hargreaves et al. (15) recently described a closely related
approach that makes use of the out-of-phase nature for fat
and water at a TR equal to the inverse of the chemical shift.
With the background phase corrected, this method
achieves fat–water separation in a single scan. A minor
drawback of this approach is that the single-shot method
can not perform separation in voxels that contain a partial
volume mixture of different spectral species. In contrast,
with the use of complex subtraction in SSFP Dixon imaging, as described in this study, one can achieve fat–water
separation even in the presence of partial volume effects,
at the expense of twice the scan time.
Compared with SSFP fat suppression using the algorithm proposed by Scheffler et al. (9), the Dixon-based
method has the disadvantage of requiring a longer scan
time (by a factor of 2) to obtain in-phase and out-of-phase
images. Subject motion between successive scans could
lead to imperfect fat cancellation due to image misregistration. Nevertheless, since the scan time is ⬍1 s per slice,
involuntary motion is expected to be minimal. The insensitivity of the technique to the exact value of the offresonance frequency in obtaining in-phase or out-of-phase
images also makes this method easy to use. In clinical
applications where quantification of fat content is of diagnostic value (17,18), SSFP Dixon imaging may be an effective alternative for achieving fat–water separation relatively quickly.
In situations where more than two frequency components are present, such as imaging in breasts with silicone
implants (19), it should be possible, by carefully selecting
the off-resonance frequency, to obtain images that show,
for example, in-phase behavior for water and silicone gel,
and out-of-phase characteristics for fat/water and fat/silicone gel. Under such circumstances, the SSFP Dixon
method may be useful for selectively isolating one frequency component (e.g., silicone gel) using only two acquisitions.
In conclusion, we have successfully demonstrated the
feasibility of separating fat and water signals in SSFP
imaging based on the Dixon approach. We analyzed the
in-phase and out-of-phase behavior as a function of TR and
center frequency offset. This method is directly applicable
to systems equipped with a generic SSFP imaging se-
247
quence, with no need for advanced pulse programming,
and potentially allows for the quantification of fat/water
content even in the presence of partial volume effects. An
investigation of this approach in terms of clinical applications is currently under way.
ACKNOWLEDGMENTS
The authors are indebted to Dr. Kenneth K. Kwong for his
assistance in the experiments and helpful discussions.
T.Y.H. and F.N.W. receive support from the Ministry of
Education and the National Science Council, respectively,
under the International Student Exchange program.
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