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Quantitative Susceptibility Mapping Using 2D Simultaneous Multi-slice Gradient-echo Imaging at 7T
Wei Bian1, Adam Bruce Kerr2, Kongrong Zhu2, Paymon Rezaii1, Maged Goubran1, Christopher Lock3, May Han3, Yi Wang4, Zhe Liu4, Sherveen Parivash1, Brian Rutt1, and Michael Zeineh1

1Department of Radiology, Stanford University, Stanford, CA, United States, 2Department of Electrical Engineering, Stanford University, Stanford, CA, United States, 3Department of Neurology and Neurological Sciences, Stanford University, Stanford, CA, United States, 4Department of Radiology, Weill Cornell Medical College, New York, NY

Synopsis

A 2D multi-echo simultaneous multi-slice (SMS) gradient-echo imaging sequence was implemented for simultaneous anatomical imaging, R2* mapping and quantitative susceptibility mapping (QSM). Imaging acceleration in the slice direction speeds up the sequence to clinical scan times while using a longer TR and larger flip angle compared to 3D imaging. Evaluation from both healthy and multiple sclerosis subjects showed that, using the same acquisition time and imaging resolution as a 3D sequence, the proposed sequence improved tissue susceptibility contrast, suggesting 2D SMS GRE imaging may be a viable alternative for clinical applications of susceptibility-based imaging.

Introduction

Quantitative susceptibility mapping (QSM) is a useful tool for tissue susceptibility measurement. Its superior sensitivity to myelin and iron makes it useful in the evaluation of brain diseases such as multiple sclerosis (MS)1. Although QSM is often performed with 3D imaging to achieve small pixel size with high signal to noise ratio (SNR) while accelerating in the slice direction, 2D imaging also produces excellent gray-white contrast on magnitude and QSM images2. This is because that interleaved multi-planar acquisition in 2D imaging allows a much longer TR and flip angle than 3D imaging. With the advent of simultaneous multi-slice (SMS) imaging, 2D imaging can be accelerated through slice as well by exciting multiple slices simultaneously. The purpose of this study is to implement a 2D multi-echo SMS gradient-echo sequence to perform high-resolution magnitude imaging, R2* mapping, and QSM, and compare it to a 3D sequence.

Methods

Subjects: Eight healthy volunteers (age 30.6±4.8) and one MS patient (age 29) were scanned in accordance with IRB and HIPAA.

MR Imaging: a VERSE RF pulse was phase modulated and combined to excite multiple slices simultaneously for 2D SMS imaging3. The sampling scheme of the sequence is shown in Figure 1. For the 3D comparison, a product multi-echo 3D gradient-echo sequence was used. All imaging was performed on a GE 7T scanner with a 32-channel coil. Both the 2D SMS and 3D imaging were axially acquired using the same following parameters: FOV=22cm, resolution=0.5x0.5x1.5mm3, slice number=72, bandwidth=41.7KHz, and echo number=4. The TEs, TR and flip angle of the 2D imaging were 8.2/15.5/22.7/30ms, 1000ms, and 60°, while those of 3D were 5.9/12.9/19.9/26.9ms, 32ms, and 15°. Three slices were simultaneously excited in the SMS imaging with in-plane GRAPPA acceleration factor of 2. The 3D imaging was accelerated by in-plane ASSET factor of 2.75 and 70% partial Fourier through slice. The total acquisition time was 4.5 minutes for both 2D and 3D imaging.

Image processing: SMS images were reconstructed using a Slice-GRAPPA algorithm4. The raw phase images from each coil were Laplacian unwrapped and then background removed using PDF5, finally combining by magnitude weighting for each echo. For 3D imaging, the raw phase images from each coil were combined by the scanner console, and unwrapped and background removed as above. The phase images from all echoes were averaged (weighted by TE) for QSM reconstruction using MEDI6. R2* maps were generated by linearly fitting magnitude image signal from each echo after log transformation. The magnitude images were combined from all echoes using root mean square.

Data Analysis: The regions of interest (ROI) were manually defined for all volunteers on phase images (Figure 3). The CNRs of the Globus Pallidus/Putamen to Internal Capsule and the cortical gray to white matter (along the superior frontal sulcus) were calculated by dividing the difference in mean values between the two ROIs by the standard deviation of the latter. CNRs between the 2D and 3D were compared by a paired t-test.

Results

Overall the 2D SMS imaging achieved better image quality than the 3D imaging (Figure 2). Paired t-tests also showed significantly improved CNR on both phase and QSM images from healthy volunteers using the 2D imaging (Figure 3). Visual inspection of images yielded the same conclusion as the quantitative analysis (Figure 4). The improved CNR was also applied to lesions in a MS patient (Figure 5), revealing one cortical and two white matter lesions with altered susceptibility and R2*.

Discussion

With the same imaging resolution and coverage, our 2D SMS gradient-echo sequence could perform QSM as fast as optimized-product 3D with improved contrast of QSM images. Although in theory the susceptibility contrast should not depend on TR and flip angle, in practice discretized imaging results in different MR signal properties in voxels having multiple microscopic compartments7, making the contrast TR and flip angle dependent. Thus, the improved CNR may be due to the dramatically different TR and flip angle in 2D imaging. With SMS imaging, this advantage of 2D imaging can be maintained and utilized without a cost in imaging time. Accelerated 2D QSM imaging is also possible using EPI, but it results in image distortions and low imaging resolution that compromise the ability to contrast small structures. The ability of our sequence to contrast small tissues such as cortical gray and white matter could be very useful in characterizing MS cortical lesions, which have different pathology and higher impact on patient disability8.

Conclusion

2D SMS imaging is a viable method to perform fast high-resolution simultaneous imaging for magnitude, R2*, and QSM in clinical applications.

Acknowledgements

The authors acknowledge research support from the NIH (P41 EB015891, 1 S10 RR026351-01A1) and GE Healthcare.

References

1. Wang Y and Liu T. Quantitative susceptibility mapping (QSM): Decoding MRI data for a tissue magnetic biomarker. Magn Reson Med. 2015;73:82-101

2. Bian W, Tranvinh E, and Tourdias T, et al. In Vivo 7T MR Quantitative Susceptibility Mapping Reveals Opposite Susceptibility Contrast between Cortical and White Matter Lesions in Multiple Sclerosis. AJNR AM J Neuroradiol 2016;17:1808-15

3. Kerr AB, Zhu K, and Middione M, et al. Delay-Insensitive Variable-Rate Selective Excitation (DIVERSE). Proc Intl Soc Mag Reson Med. 2015; 23: 921.

4. Setsompop K, Gagoski BA, Polimeni J, et al. Blipped-Controlled Aliasing in Parallel Imaging (blipped-CAIPI) for simultaneous multi-slice EPI with reduced g-factor penalty. Magn. Reson. Med. 2012;67:1210–24.

5. Liu T, Khalidov I, de Rochefort L, et al. A novel background field removal method for MRI using projection onto dipole fields (PDF). NMR Biomed. 2011;24:1129–36.

6. Liu J, Liu T, de Rochefort L, et al. Morphology enabled dipole inversion for quantitative susceptibility mapping using structural consistency between the magnitude image and the susceptibility map. Neuroimage. 2012; 59: 2560-8.

7. Li W, Han H, and Guidon A, et al. Dependence of gradient echo phase contrast on the differential signal decay in subcellular compartments. Proc Intl Soc Mag Reson Med. 2013; 21: 161.

8. Calabrese M, Filippi M and Gallo P. Cortical lesions in multiple sclerosis. Nat Rev Neurol. 2010; 6: 438-44.

Figures

Figure 1. An illustration of the sampling scheme of the 2D SMS sequence formulated in the 3D k-space. In this 3-slice simultaneous excitation example, each solid line indicates a k-space line sampled after an RF excitation, which is also phase cycled to shift FOV among slices. The blue lines represent the auto-calibration region, where the sampling in kz is realized by the Fourier encoding imposed by RF. Unlike the SMS EPI sequence that can use a full calibration, our sequence sampled only 16 calibrated lines in the center of the k-space to separate simultaneously acquired slices.

Figure 2. A comparison of image quality between the 2D SMS and product 3D sequence. All images from a volunteer show comparable quality between the 2D and 3D sequence. Of note the 2D QSM images are even absent of streaking artifacts and slice discontinuity when looking from the sagittal and coronal planes. The images are also free of cross-talk artifacts between neighboring excitation bands, even though an even number of slices were acquired in each band. The image displaying window ranges in this and following figures are: 0~100 s-1 for R2*, -0.8~0.8 radian for phase, -0.2~0.2 ppm for QSM images.

Table 1. Tissue contrast to noise ratio from both the 2D SMS and 3D product sequences. GP = Globus Pallidus; Put = Putamen; IC = posterior limb of Internal Capsule; GM = Gray Matter along the superior frontal sulcus; WM = White Matter adjacent to the GM. *Indicates a significant difference given by the paired t-test.

Figure 4. Different QSM and phase contrast between 2D SMS and product 3D sequences from a volunteer. Colored dashed lines illustrate the ROIs defined for the CNR analysis: pink for the gray matter along superior frontal sulcus; green for the putamen; red for the globus pallidus; and yellow for the posterior limb of internal capsule. Overall 2D images show sharper contrast than 3D ones. Local regions with significantly different contrast are indicated by colored arrows, of which the green ones indicate a better differentiation between the more iron-rich outer and less iron-rich inner layers of putamen on 2D images.

Figure 5. Images from a MS patient. Three lesions are shown on T1/T2 images, and all of them are better contrasted on the images from the 2D SMS sequence. In particular, the surrounding normal-appearing cortex of the mixed-cortical-white matter lesion II is well preserved on the 2D QSM images. Preserving this cortex contrast is crucial for cortical and mixed-cortical-white matter lesion characterization. In addition, the hyperintense appearance of lesion II and III on both QSM and R2* suggests the iron deposition dominates, whereas the respect hyperintense and hypointense appearance of lesion I on QSM and R2* suggests demyelination dominates.

Proc. Intl. Soc. Mag. Reson. Med. 25 (2017)
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