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Improved quantitative accuracy using ultrahigh resolution DTI-guided QSM
Lijia Zhang1,2, Chris Petty1, and Allen Song1

1Brain Imaging and Analysis Center, Duke University, Durham, NC, United States, 2Medical Physics, Duke University, Durham, NC, United States

Synopsis

Quantitative susceptibility mapping (QSM) has been increasingly used to help access the brain development, especially white matter myelination. However, the quantitative accuracy is limited by its angle dependence to the magnetic field. In this study, ultrahigh resolution diffusion tensor imaging (DTI) was used to delineate the fiber bundles (i.e. corpus callosal fibers), followed by tract-based QSM to minimize the angle dependence and accurately assess magnetic susceptibility changes in different brain regions.

Introduction

Quantitative susceptibility mapping (QSM) has seen increased utility in assessing brain development, due to its unique sensitivity to myelin. However, magnetic susceptibility has been demonstrated to be anisotropic, dependent on the orientation with respect to the main magnetic field (B0). The purpose of this study is thus to develop ultrahigh resolution DTI tract-guided QSM to minimize the orientation dependence of susceptibility measures, capture the intricate neuronal circuitry including curvature, as well as to evaluate how the improved quantitative accuracy of QSM can better assess magnetic susceptibility changes across the fiber bundles (i.e. corpus callosal fibers).

Methods

DTI data were obtained with 2D MUSE (MUltiplexed Sensitivity Encoding) diffusion MRI sequence on a GE Premier 3T MRI scanner (Waukesha, WI), equipped with a high-power 60 cm gradient coil with a peak strength at 115 mT/m. A total of 15 diffusion directions were used at a b factor of 800 $$$s/mm^2$$$. Because of the strong gradient coil, an ultrahigh 0.8 mm isotropic spatial resolution was achieved at a TE of 63.8 ms. In the same session, a spatially matched QSM protocol using a 3D SWAN sequence (16 TE increments, TR=44.3 ms, flip angle = 15 degrees, 0.8*0.8*0.8 $$$mm^3$$$ resolution) was carried out. The T1, DTI and QSM images were all coregistered, and then the corpus callosum ROI was extracted by warping the JHU DTI MNI “Eve” WMPM Type II template1 into subject’s DTI space via Large Deformation Diffeomorpic Metric Mapping (LDDMM)2. DTI tractography was accomplished by MRtrix3 with streamline tracking followed by spline filtering3. The angle of the corpus callosal fibers at each voxel was accurately calculated from the principal eigenvector of the diffusion tensor using ultrahigh resolution DTI, and magnetic susceptibility measures were overlaid onto the fibers to illustrate the angle dependency, which can then be removed by deriving the rotationally-invariant magnetic susceptibility anisotropy (MSA)4.

Results and Discussion

Fig. 1 shows the delineation of the corpus callosal fibers, with angle-dependent magnetic susceptibility values overlaid onto the fibers of a healthy representative subject (male, 25 years old). The midbody of corpus callosum was divided into three parts based on Witelson’s scheme5. It was found that the susceptibility values of the same fiber exhibited more diamagnetic characteristics when the fibers were perpendicular to the B0 field, and the magnetic susceptibility values approach zero as fibers became parallel with the main magnetic field. This observation is consistent with theoretical prediction, as illustrated in $$$\chi_\alpha=MSA\cdot sin^2 \alpha+\chi_0$$$ [Eqn. 1]6. Magnetic susceptibility anisotropy (MSA) is rotationally-invariant and proportional to the volume fraction of local myelin lipids, and $$$\chi_0$$$ is the baseline susceptibility dependent on the choice of frame of reference and absolute susceptibility. An close oblique view from bottom right of the fibers, as shown in Fig. 2, also confirms the angle variation of the magnetic susceptibility values predicted by Eqn. 1. By fitting the magnetic susceptibility values across all the angles, MSA can be accurately determined to serve as a quantitative measure of magnetic susceptibility. Furthermore, a clear posterior-anterior pattern of myelin maturation was demonstrated in both Fig.1 and 2. The fibers perpendicular to the main magnetic field are more diamagnetic (i.e. more myelination) in the posterior region than the anterior region. For example, the sensory fibers are more diamagnetic than the motor fibers, and the motor fibers are more diamagnetic than the premotor and supplementary motor fibers, consistent with previous findings that the posterior corpus callosum matures earlier than the anterior part in childhood, adolescence and early adulthood7,8.

Conclusion

We have developed an ultrahigh resolution DTI-guided QSM method that can accurately measure the magnetic susceptibility of major fiber tracts with submillimeter spatial accuracy and minimal angle dependence, which can be used to better evaluate white matter myelin maturation during brain development. It is anticipated that this quantitative technique may find broad utility to help characterize white matter development in both healthy and diseased brains across the life span.

Acknowledgements

The study is supported in part by NIH grant R01 NS 075017.

References

1. Oishi, Kenichi, et al. Atlas-based whole brain white matter analysis using large deformation diffeomorphic metric mapping: application to normal elderly and Alzheimer's disease participants. Neuroimage 46.2 (2009): 486-499.

2. Beg, M. Faisal, et al. Computing large deformation metric mappings via geodesic flows of diffeomorphisms. International journal of computer vision 61.2 (2005): 139-157.

3. Veraart, Jelle, Els Fieremans, and Dmitry S. Novikov. Diffusion MRI noise mapping using random matrix theory. Magnetic resonance in medicine 76.5 (2016): 1582-1593.

4. Li, Wei, et al. Magnetic susceptibility anisotropy of human brain in vivo and its molecular underpinnings. Neuroimage 59.3 (2012): 2088-2097.

5. Witelson, Sandra F. Hand and sex differences in the isthmus and genu of the human corpus callosum: a postmortem morphological study. Brain 112.3 (1989): 799-835.

6. Argyridis, Ioannis, et al. Quantitative magnetic susceptibility of the developing mouse brain reveals microstructural changes in the white matter. Neuroimage 88 (2014): 134-142.

7. Luders, Eileen, Paul M. Thompson, and Arthur W. Toga. The development of the corpus callosum in the healthy human brain. Journal of Neuroscience 30.33 (2010): 10985-10990.

8. Keshavan, Matcheri S., et al. Development of the corpus callosum in childhood, adolescence and early adulthood. Life sciences 70.16 (2002): 1909-1922.

Figures

Corpus callosum parcellation and angle-dependent susceptibility overlayed onto the fibers

Close oblique view of the angle-dependent magnetic susceptibility of the corpus callosal fibers

Proc. Intl. Soc. Mag. Reson. Med. 27 (2019)
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