Rapid phase-modulated water-excitation steady-state free precession for fat-suppressed cine cardiovascular MR
© Lin et al; licensee BioMed Central Ltd. 2008
Received: 15 November 2007
Accepted: 13 May 2008
Published: 13 May 2008
The purpose of this article is to describe a steady-state free precession (SSFP) sequence for fat-suppressed cine cardiovascular magnetic resonance (CMR). A rapid phase-modulated binomial water-excitation (WE) pulse is utilized to minimize repetition time and acquisition time.
Three different water-excitation pulses were combined with cine-SSFP for evaluation. The frequency response of each sequence was simulated and examined in phantom imaging studies. The ratio of fat to water signal amplitude was measured in phantoms to evaluate the fat-suppression capabilities of each method. Six volunteers underwent CMR of the heart at 1.5T to compare retrospectively-gated cine-SSFP with and without water-excitation. The ratio of fat to myocardium signal amplitude was measured for conventional cine-SSFP and phase-modulated WE-SSFP. The proposed WE-SSFP method was tested in one patient referred for CMR to characterize a cardiac mass.
Results and discussion
The measured frequency response in a phantom corresponded to the numerical Bloch equation simulation demonstrating the widened stop-band around the fat resonant frequency for all water-excitation pulses tested. In vivo measurements demonstrated that a rapid, phase-modulated water-excitation pulse significantly reduced the signal amplitude ratio of fat to myocardium from 6.92 ± 2.9 to 0.8 ± 0.13 (mean ± SD) without inducing any perceptible artifacts in SSFP cine CMR.
fat-suppression can be achieved in SSFP cine CMR while maintaining steady-state equilibrium using rapid, phase modulated, binomial water-excitation pulses.
Suppression of bright fat signal is important in a variety of cardiovascular magnetic resonance (CMR) applications to characterize lesions, suppress chemical shift and motion artifacts, and distinguish fluid or tumor from adipose tissue. Numerous techniques such as chemical shift selective pre-saturation (CHESS) [1, 2], short tau inversion recovery (STIR) [3, 4], and the multi-point Dixon method  have been developed to provide suppression of signal from normal adipose tissue. These techniques all have limited success when applied to steady-state free precession (SSFP) imaging as they disturb the steady-state equilibrium and/or prolong repetition time (TR) and acquisition time. A number of recent articles describe fat-suppression methods designed to maintain the magnetization steady-state in SSFP imaging [6–14]. Scheffler  first proposed a method of interleaving spectral fat saturation pulses within the SSFP acquisition, utilizing an α/2 flip-back pulse to store the established steady-state magnetization prior to each fat-suppression pulse. While successful, this method is incompatible with cine CMR that requires continuous data acquisition without interruption. Reeder  proposed a water-fat separation method using an "iterative decomposition of water and fat with echo asymmetry and least squares estimation" (IDEAL) which decomposes cine-SSFP images into separate water and fat images. IDEAL requires acquisition of three complete datasets and a longer TR, nearly tripling image acquisition time and increasing sensitivity to off-resonance artifacts. Hardy  proposed a method of maintaining an uninterrupted, fat-suppressed steady-state by cycling the SSFP RF-excitation pulse amplitude through a repeating binomial pattern. This approach utilizes the principle of binomial water-excitation , modulating the excitation pulse amplitudes to create a broad band of signal suppression centered on the fat frequency. However, Hardy's technique required additional TR's and a significant increase in total acquisition time. The method of alternating-TR (ATR-SSFP) proposed by Leupold  arrives at a similar pulse sequence design to that which we propose, but with differences in concept and in sequence design constraints that will be discussed.
A simple, practical method for spectrally and spatially selective water-excitation (WE) based on binomial pulse design  has been used in combination with spoiled gradient echo imaging for several years. Binomial water-excitation has been applied to abdominal and orthopedic MRI [16–18], and more recently to CMR  providing advantages of no disruption of the steady-state and uniform fat suppression. More recently, binomial water-excitation has been combined with 3D SSFP for orthopedic imaging . In this work, we combine a rapid phase-modulated binomial water-excitation pulse with SSFP for fat-suppressed cardiac cine imaging. Our hypothesis is that sufficient fat signal suppression can be achieved with minimal impact on TR, sensitivity to flow artifact, total scan time, and cine-SSFP image quality using rapid binomial water-excitation RF pulses. While the combination of binomial water-excitation with SSFP has similarities with the methods proposed by both Hardy  and Leupold , our design strategy removes the necessity for any additional data acquisition or constraints on the relationship between the TR and the water-excitation pulse timing. Numerical simulation, phantom and healthy volunteer imaging trials were performed to provide experimental validation of the fundamental concepts and performance of WE-SSFP, and images in one patient are shown to demonstrate a potential clinical application.
Summary of imaging parameters for phantom and in vivo studies*
Interpulse Phase Evolution (°)
Interpulse Delay (ms)
Total Pulse Duration (ms)
TR for Phantom Studies (ms)
TR for in vivo Studies (ms)
Component Pulse Flip Angles (°)
Resultant Flip Angle (°)
17.7 – 35.4 – 17.7
35.4 – 35.4
56.4 – 56.4
Simulations were run to predict the variation of steady-state transverse magnetization with chemical shift for the SSFP sequence in combination with the four different excitation pulses. All simulations were performed with the following simulation parameters: TR = 9.68 ms, TE = 4.8 ms, Flip angle = 70° for the conventional SSFP and all WE-SSFP sequences; relaxation time constants of simulated water-based tissue (T1 = 578 ms, T2 = 263 ms) and fat (T1 = 252 ms, T2 = 81 ms) were chosen to match the phantom compartments. The TR was chosen to match that used in the phantom study of pulse sequence frequency response. The frequency response of the 1-(90°)-1 pulse was also simulated at shorter TR's (8.9 ms, 5.9 ms, and 4.45 ms) to investigate any impact of TR on the fat-suppression frequency band. Analytic expressions for the resulting rotation matrices and magnetization distributions were generated using Mathematica (Wolfram Research, Inc., Champaign, IL.).
Pulse sequence implementation
WE-SSFP cine sequences using each of the four pulse designs were implemented on a 32-channel, 1.5 Tesla MR system (MAGNETOM Avanto, Siemens Healthcare, Erlangen, Germany) with 45 mT/m gradient amplitude and 200 mT/m/ms maximum slew rate. Phantom and human imaging studies were performed using twelve array coil elements.
Table 1 shows the CMR imaging parameters used for phantom and human volunteer studies. A 2D SSFP cine with retrospective ECG-gating was used with an effective 70° total flip angle, 5-mm section thickness, a 256 × 192 acquisition matrix, and 350 × 262 mm FOV, one signal average, and parallel acquisition acceleration rate of 2 using "Generalized Autocalibrating Partially Parallel Acquisitions" (GRAPPA). These imaging parameters were held constant throughout all phantom and human imaging experiments. In phantom studies designed to demonstrate the frequency response, the TR was set long enough (9.68 ms) to allow for the longest (1-2-1) RF pulse and keep the spacing of band artifacts the same among the four sequences. In fat/water phantom and human imaging experiments, the TR was set to the minimum permitted by each sequence in order to illustrate the benefits of minimizing the RF pulse duration. The shortest water-excitation pulse, 1-(90°)-1, was also tested at longer TR values in phantoms and in vivo to demonstrate the independence of fat-suppression to choice of TR, and the loss of image quality and increased flow sensitivity as a result of longer TR.
Phantom imaging studies
The first phantom study was performed on a uniform spherical water phantom doped with 1.25 g NiSO4 + 6 H2O and 5 g NaCl per 1000 g water. This phantom was imaged with an applied constant gradient offset of 0.0723 mT/m in the x-direction (left-right) to demonstrate the effect of each of the four excitation pulses on the frequency response of the cine-SSFP sequence. Images were acquired using all four pulse designs and signal profiles were measured in the direction of the applied field inhomogeneity to illustrate the frequency response and compare to the simulation results. TR was kept constant at 9.68 ms across the four sequences to maintain spacing of banding artifacts for comparative purposes.
The second phantom experiment was performed using water and mineral oil phantoms (T1/T2 of water = 578/263 ms and T1/T2 of oil = 252/81 ms) to measure the ratio of fat to water signal amplitude for each pulse and compare to that expected based on simulation results. The regions of interest (ROI) measured in the phantom images were the maximum size permissible within the boundaries of the object. The SSFP sequence was tested using the shortest TR allowed by each excitation pulse scheme. Additionally, the shortest phase modulated 1-(90°)-1 pulse was tested at longer TR's (5.0 ms and 5.6 ms) to demonstrate the independence of fat-suppression from the choice of TR.
Human subject imaging studies
Conventional cine-SSFP and three different WE-SSFP sequences were evaluated in six healthy volunteers (1 women; aged 46 years, and 5 men; aged 22-57 years, with a mean age of 43.25 ± 13.72) and with no history of common cardiovascular disease. Vertical and horizontal long-axis views were acquired in each subject using each of the four sequences. The phase modulated 1-1 WE-SSFP sequence was also tested in one 42 year-old male patient referred for CMR to characterize a cardiac mass seen on echocardiography. All images were acquired using electrocardiographic (ECG) signal gating and breath-holding. No patient-specific or volume-localized shimming was performed. The default shim values based on field homogeneity in a uniform spherical phantom were used for all in vivo studies. All subjects gave written informed consent to participate in this Institutional Review Board-approved protocol.
One individual (HYL) measured the signal amplitude in the myocardium and fat in all cine series acquired in normal subjects. Measurements were made in a single, end-diastolic frame from each of the cine series acquired in the two different views using each of the four sequences. Circular ROI's were placed within the left ventricular myocardium and surrounding fat to measure average signal amplitudes (SA). For consistency, similar anatomical regions were selected in all images. The signal amplitude ratio between fat and myocardium was calculated to evaluate the effect of fat-suppression.
Numerical simulations and phantom imaging studies
Signal amplitude ratio between fat and water in phantom studies
Sequences for Fat/water Studies
Interpulse Phase Evolution (°)
Interpulse Delay (ms)
781 ± 27.1
1036 ± 32.6
721 ± 24.3
36 ± 10.8
723 ± 25.7
40 ± 11.2
736 ± 25.2
35 ± 9.8
737 ± 21.3
32 ± 8.7
726 ± 20.8
39 ± 10.4
Human subject imaging studies
We have shown that the simple combination of a phase-modulated 1-(90°)-1 water-excitation pulse together with cine-SSFP results in a fat-suppressed steady-state with only minimal increase in TR and overall scan time. This technique utilizes the frequency offset between fat and water spins and a binomial pulse design to effectively suppress the normally bright fat signal in cine-SSFP. As shown by Thomasson et al. , the component pulse spacing in binomial water-excitation need not be restricted to the time necessary to allow 180 degrees of phase evolution between fat and water. By appropriate RF phase modulation, component pulse spacing can be shortened while maintaining fat suppression. The resultant rapid water-excitation pulses incur only a minimal increase in TR, critical in cine-SSFP to avoid off-resonance banding and blood flow artifacts. Results in phantoms showed that the fat-suppression achieved is similar to that predicted by Bloch equation simulations (Figures 2, 3 and 4), and in vivo results showed that this technique can significantly reduce bright fat signal while maintaining SSFP image quality (Figures 5, 6, 7, and 8). Furthermore, Figures 2d, h and 2l show a single-sided stop-band for the 1-(90°)-1 pulse at -220 Hz (i.e. the fat frequency) instead of the double-sided stop bands at ± 220 Hz (Figures 2b, f, j and 2c, g, k) demonstrated by the other WE pulses. The single-sided stop band may be an advantage as it is less likely to lead to suppression of water signal in case of field inhomogeneity. The frequency response profiles in Figure 3 demonstrated that the stopband frequency of the 1-(90°)-1 binomal pulse is independent on the choice of TR. Moreover, the 1-(90°)-1 pulse demonstrated consistent fat-suppression at different TR's in water and mineral oil phantoms (Figure 4d–f). Phantom and in vivo signal measurements showed consistent fat signal attenuation was achieved without restriction of TR.
Existing fat-suppression methods that have been described for SSFP applications [7–10, 12, 13] are generally of limited use in breath-hold SSFP cine imaging because they entail prolonged acquisition time, increased TR, or disruption of the steady-state. WE-SSFP has significant similarities with the fat-suppressed alternating repetition time (FS-ATR) technique described by Leupold et al. . The difference between the techniques is primarily conceptual, and both show that fat-suppression can be achieved while maintaining the steady-state with only a minimal (~30%) increase in TR. Leupold describes frequency response and fat-suppression in terms of a new steady-state defined by the alternation of TR between excitation pulses, and places certain restrictions on the relationship between the two TR's. Specifically, Leupold states that a TR = 4.3 ms is necessary for fat-suppression at 1.5T. However, he goes on to show that fat-suppression can still be achieved to some degree while allowing TR to vary. Our approach instead recognizes that the water-excitation pulse can be defined as a phase-modulated 1-(90°)-1 binomial pulse pair independent of other imaging sequence parameters. Based on this, we provide a simplified description of the method, and avoid unnecessary restrictions on the sequence design. The WE-SSFP technique described here imposes no specific restrictions on TR other than the usual SSFP requirement that TR<<T2, and no fixed relationship between TR and binomial pulse spacing. While TR must be increased to accommodate the binomial pulse length, the flexibility of choice in binomial WE pulse design and selection of imaging TR was demonstrated in the phantom and in vivo results. Three different configurations of WE pulses and TR values ranging from 4.0 ms to 8.9 ms were shown. The time between the component pulses of the binomial pulse series can be flexibly chosen based on slice profile and gradient constraints, with the understanding that lengthening the overall TR can have adverse effects on SSFP image quality. Any increase in TR in SSFP increases sensitivity to field inhomogeneity and flow.
One important limitation of this phase-modulated 1-(90°)-1 WE method is that field inhomogeneities can cause non-uniform fat suppression. However, this is true of any frequency-selective fat-suppression scheme, and initial results in human subjects show sufficient homogeneity that these effects are not severe at 1.5T. The variability in fat-suppression throughout the field-of-view observed in the in vivo images acquired with different pulses may be due to a variety of factors. As shown in Figure 2 and Figure 3, the frequency response pattern varies from pulse to pulse, and also with TR. Since these are breath-hold images of a beating heart, there can be variation in position causing variation in local homogeneity from one scan to the next. These factors may all contribute to the observed differences.
In conclusion, our results show fat-suppression is feasible by the combination of phase modulated binomial water-excitation with SSFP cine CMR. It was found that a phase-modulated RF slice-selective pulse with phase evolution equal to 90° (1.1 ms interpulse delay) is sufficient to null fat signal while maintaining steady-state equilibrium for high SNR, insensitivity to off-resonance artifacts, and time-efficiency. Further testing is warranted to evaluate the effectiveness of this technique in clinical imaging.
OPS and SVR receive research support from Siemens Healthcare, Inc., and Y–CC is an employee of Siemens Healthcare, Inc.
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