DANTE-EPI for CSF Suppression in Cervical Spinal Cord BOLD fMRI at 7T
Alan Charles Seifert1,2, Hadrien Dyvorne1,2, Joo-won Kim1,2, Bei Zhang3, and Junqian Xu1,2,4

1Translational and Molecular Imaging Institute, Icahn School of Medicine at Mount Sinai, New York, NY, United States, 2Department of Radiology, Icahn School of Medicine at Mount Sinai, New York, NY, United States, 3Department of Radiology, NYU Langone Medical Center, New York, NY, United States, 4Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, NY, United States

Synopsis

A major challenge in spinal cord fMRI is physiological noise due to pulsating CSF, which confounds detection of BOLD signal. In this work, we adapt DANTE to reduce CSF signal contamination in spinal cord BOLD fMRI at 7T. Absolute signal intensity, temporal SNR, and temporal cross-correlation between left and right spinal cord gray matter were measured in DANTE-EPI images at multiple pulse-train lengths and flip angles. Aggressive DANTE preparation suppresses CSF signal, but also significantly reduces spinal cord signal. More conservative DANTE preparation yields an optimal tradeoff between adequate CSF attenuation and preservation of spinal cord signal.

Introduction

Spinal cord blood oxygenation level-dependent (BOLD) fMRI studies [1] have begun to demonstrate convincing activation in the spinal cord gray matter for sensory and pain signals [2] and during resting state [3]. Among many challenges in spinal cord fMRI, physiological noise due to pulsating cerebrospinal fluid (CSF) surrounding the spinal cord is arguably the most detrimental to BOLD signal detection in the spinal cord. Most current spinal cord fMRI studies address the CSF signal contamination issue with image post-processing methods (e.g. regressing out CSF signal, or physiological cardiac recording). In this work, we adapt a CSF signal suppression strategy, delay alternating with nutation for tailored excitation (DANTE), to reduce CSF signal contamination in spinal cord BOLD fMRI at 7T.

DANTE

In the original DANTE method [4], a series of evenly-spaced low-flip-angle RF pulses was used to exert a cumulative effect on a narrow band of frequencies on-resonance. Off-resonance spins accumulate phase between pulses, interrupting the cumulative effect of the pulse train. Li et al. [5] recently introduced a motion-sensitive preparation technique based on DANTE, in which a train of low-flip angle RF pulses interleaved with gradient pulses suppresses moving spins. This method has been proven to attenuate CSF signal in the spine at 3T [6]. In this work, DANTE is combined with an echo-planar imaging (EPI) sequence and applied to the cervical spinal cord at 7T.

Methods

Axial gradient echo EPI was performed on a 7T whole-body scanner (Siemens) with a 4-channel Tx, 22-channel Rx array coil [7] at the C4 spinal level of one healthy adult volunteer in resting condition. TR=2100 ms, TE=23 ms, flip angle=65°, RF pulse duration=2560 µs, 100 frames, 1563 Hz/pixel, echo spacing=0.37 ms, 240 mm x 240 mm FOV, one anterior saturation band, 1.2 mm x 1.2 mm in-plane resolution, 5 mm slice thickness, GRAPPA=2, and ETL=50 (18.5 ms). A DANTE preparation block, consisting of a train of non-selective RF pulses (100 µs duration; number of pulses Np=250, 150, 75, 40, 25, or 0 (DANTEoff); flip angle $$$\alpha$$$=5°, 10°, or 15°; phase cycle f=0°, 180°) interleaved with z-gradient pulses (Gz=20 mT/m, duration=1 ms, ramp time=200 µs), was applied before each EPI acquisition. Images within each EPI series were registered in plane using FSL/FLIRT [8] with two degrees of freedom. From each series, voxel-wise temporal SNR (tSNR = s/m) maps were calculated, and signal time-courses were extracted from regions of interest (ROIs) in the left and right spinal cord gray matter medial to the lateral horns (Fig. 1) and anterior CSF. Pearson’s correlation coefficients (r) were calculated for temporal cross-correlations between left and right gray matter and between total gray matter and CSF.

Results

Images and tSNR maps at all tested Np and $$$\alpha$$$ are shown in Fig. 2. Surface plots of signal intensity in the spinal cord gray matter and CSF (Fig. 3) show that DANTE with 250 pulses at 15° achieves 95% suppression of CSF signal, while more conservative 150x15° and 150x10° yield 92% and 80% suppression, respectively. These three DANTE conditions, however, result in attenuation of signal in the spinal cord by 42%, 34%, and 26%, respectively. Similar decreases in gray matter tSNR (Fig. 4) were observed, although these measured decreases do not distinguish between BOLD signal and other non-BOLD contributions. Despite the moderately decreased signal intensity in the static spinal cord, the temporal cross-correlation of resting-state signal in the bilateral spinal cord gray matter (Fig. 5) improves from r=0.25 (without DANTE) to r=0.80-0.90 (with DANTE). In addition, application of DANTE (250x15°) reduces the temporal correlation of CSF versus gray matter signal significantly (from r=0.54 to r=0.08), suggesting that signal fluctuation related to the pulsating CSF was attenuated and/or removed from the gray matter by DANTE.

Discussion

The present results show that motion-sensitive DANTE preparation strongly suppresses signal from pulsating CSF in the cervical spine at 7T. Because DANTE also causes attenuation of signal in static tissues proportional to Np and $$$\alpha^2$$$ [5], these parameters must be selected carefully to balance CSF suppression with preservation of spinal cord signal. The strongest DANTE preparation applied in this work, 250x15°, suppressed CSF most strongly, but at an increased cost to spinal cord signal intensity and tSNR. A more moderate preparation, 150x10°, maintains effective CSF suppression (see Fig. 1), but attenuates spinal cord signal less heavily, and preserves a stronger bi-lateral correlation in gray matter signal than 250x15° (r=0.90 vs. r=0.80, respectively). In conclusion, DANTE prepared EPI with CSF-attenuation/suppression is a promising spinal cord BOLD fMRI acquisition technique at ultra-high field.

Acknowledgements

This study was supported by Radiological Society of North America (RSNA) research scholar grant RSCH1328 (JX), National Multiple Sclerosis Society (NMSS) - International Progressive MS Alliance (IPMSA) infrastructure award PA0097 (JX), and the National Institute of Health (NIH) under award numbers U01 EY025500 (ACS, JK, and JX) and R00 NS070821 (HD).

References

[1] Yoshizawa T, Nose T, Moore GJ, Sillerud LO. Functional magnetic resonance imaging of motor activation in the human cervical spinal cord. Neuroimage 1996;4:174–182

[2] Eippert F, Bingel U, Schoell ED, Yacubian J, Klinger R, Lorenz J, Büchel C. Activation of the opioidergic descending pain control system underlies placebo analgesia. Neuron 2009;63(4):533-543

[3] Kong Y, Eippert F, Beckmann CF, Andersson J, Finsterbusch J, Büchel C, Tracey I, Brooks JC. Intrinsically organized resting state networks in the human spinal cord. PNAS 2014;111(50):18067-18072

[4] Morris GA, Freeman R. Selective excitation in Fourier transform nuclear magnetic resonance. JMR 1978;29:433-462

[5] Li L, Miller KL, Jezzard P. DANTE-prepared pulse trains: a novel approach to motion-sensitized and motion-suppressed quantitative magnetic resonance imaging. MRM 2012;68(5):1423-1438

[6] Li L, Kong Y, Zaitsu Y, Matthews L, Palace J, Jezzard P. Structural imaging of the cervical spinal cord with suppressed CSF using DANTE pulse trains. MRM 2015;74(4):971-977

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Figures

a) Axial 7T multi-echo GRE image at C4 spinal level in a healthy adult volunteer (0.3 mm x 0.3 mm x 3 mm, TR=300 ms, TE=3.3/14.3/18.7/23 ms, flip angle=20°, BW=260 Hz/px, 6 averages). Borders of gray and white matter are outlined in yellow. b) EPI image without DANTE flow suppression, overlaid with approximate borders of gray and white matter in yellow, and actual locations of ROIs used for quantification of gray matter and CSF signal.

Montage of mean absolute signal intensity (grayscale) and temporal SNR (color) for 15 combinations of DANTE pulse train lengths and flip angles and one with no DANTE preparation applied (parameters inset within each frame). In images with strong DANTE preparation (e.g., 250x15°), no signal is visible from CSF, although signal intensity and temporal SNR in the spinal cord are moderately reduced.

Surface plots of the mean absolute signal intensity within the gray matter (mesh edges solid) and CSF (mesh edges dashed) ROIs. As the number of DANTE pulses is increased (i.e., as the DANTE pulse train is lengthened), and as the DANTE RF pulse flip angle is increased, signal from the moving CSF spins is strongly suppressed, while signal from the stationary spinal cord is only moderately attenuated.

Surface plots of the temporal SNR within the gray matter (mesh edges solid) and CSF (mesh edges dashed) ROIs. As the number of DANTE pulses or the DANTE flip angle is increased (i.e., as stronger DANTE preparation is applied), temporal SNR in both the gray matter and CSF is reduced, although tSNR in the gray matter remains higher than in CSF for all parameter sets.

Surface plot of the temporal correlation coefficient, r, for signal in ROIs in the left versus right gray matter (note reversal of x and y axis limits vs. Figures 2 and 3). As signal from CSF is more strongly suppressed, signal in the left and right gray matter during resting-state scans becomes more strongly correlated. This suggests the suppression of nuisance signal contributions from the pulsating CSF spins, while the underlying resting-state BOLD signal in the gray matter is preserved.



Proc. Intl. Soc. Mag. Reson. Med. 24 (2016)
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