White matter structural and network topological changes in moyamoya disease with limb paresthesia: A study based on diffusion kurtosis imaging

Abstract

Purpose: To investigate the structural and network topological changes in the white matter (WM) in MMD patients with limb paresthesia by performing diffusion kurtosis imaging (DKI).

Materials and methods: A total of 151 MMD patients, including 46 with left-limb paresthesia (MLP), 52 with right-limb paresthesia (MRP), and 53 without paresthesia (MWP), and 28 healthy controls (HCs) underwent whole-brain DKI, while the surgical patients were reexamined 3-4 months after revascularization. The data were preprocessed to calculate the fractional anisotropy (FA) and mean kurtosis (MK) values. Voxel-wise statistics for FA and MK images were obtained by using tract-based spatial statistics (TBSS). Next, the whole-brain network was constructed, and global and local network parameters were analyzed using graph theory. All parameters were compared among the HC, MWP, MLP, and MRP groups, and changes in the MMD patients before and after revascularization were also compared.

Results: The TBSS analysis revealed significant reductions in FA and MK in extensive WM regions in the three patient groups. In comparison with the MWP group, the MLP group showed reductions in FA and MK in both right and left WM, mainly in the right WM, while the MRP group mainly showed a reduction in FA in the left WM region and demonstrated no significant change in MK. The graph theoretical analysis showed decreased global network efficiency, increased characteristic path length, and increased sigma in the MWP, MRP, and MLP groups in comparison with the HC group. Among local network parameters, the nodal efficiency decreased in the bilateral MFG and IFGtriang, while the degree decreased in the MFG.L and bilateral IFGtriang. Patients with right-limb paresthesia showed the lowest nodal efficiency and degree in MFG.L and IFGtriang.L, while those with left-limb paresthesia showed the lowest nodal efficiency in MFG.R and IFGtriang.R and the lowest degree in IFGtriang.R.

Conclusion: A DKI-based whole-brain structural and network analysis can be used to detect changes in WM damage and network topological changes in MMD patients with limb paresthesia. FA is more sensitive than MK in detecting WM injury, while MFG and IFGtriang are the key nodes related to the development of acroparesthesia.

Keywords: brain network; diffusion kurtosis imaging (DKI); limb paresthesia; magnetic resonance imaging (MRI); moyamoya disease (MMD).

FIGURE 1

Schematic diagram outlining the construction of the brain network.

FIGURE 2

Voxel-wise TBSS analysis results of fractional anisotropy (FA) images across MMD patients with or without limb paresthesia and healthy controls (HCs). (A) Significant differences in FA (red-yellow) between patients without paresthesia (MWP), patients with left-limb paresthesia (MLP), patients with right-limb paresthesia (MRP), and HCs (p < 0.05; FWE corrected based on the threshold-free cluster enhancement statistical image). Post hoc analyses revealed significant reductions in FA (red-yellow) in the MWP (B), MLP (C), and MRP (D) groups in comparison with HCs. Post hoc analyses also revealed significant reductions in FA (red-yellow) in the MLP (E) and MRP (F) groups in comparison with the MWP group. Green represents the mean white matter skeleton of all participants. The color scale (red-yellow) represents significant differences between groups, with colored regions exceeding the significance threshold of P < 0.05. The left side of the image corresponds to the right hemisphere of the brain. ANCOVA, analysis of covariance.

FIGURE 3

Voxel-wise TBSS analysis results of mean kurtosis (MK) images across MMD patients with or without limb paresthesia and healthy controls (HCs). (A) Significant differences in MK (red-yellow) between patients without acroparesthesia (MWP), patients with left-limb paresthesia (MLP), patients with right-limb paresthesia (MRP), and HCs (p < 0.05; family-wise error corrected based on the threshold-free cluster enhancement statistical image). Post hoc analyses revealed significant reductions (red-yellow) in MK in the MWP (B), MLP (C), and MRP (D) groups in comparison with the HCs. Post hoc analyses revealed significant reductions in MK in the MLP group (E) in comparison with MWP group, and no significant reductions in MK were observed in the MRP group (F) in comparison with the MWP group. Green represents the mean white matter skeleton of all participants. The color scale (red-yellow) represents significant differences between groups, with colored regions exceeding the significance threshold of P < 0.05. The left side of the image corresponds to the right hemisphere of the brain. ANCOVA, analysis of covariance.

FIGURE 4

Comparison of global network parameters. In comparison with the findings for healthy controls (HCs), global network efficiency (A) was decreased, and characteristic path length (B) was increased, both in the order of MMD patients without paresthesia (MWP), patients with right-limb paresthesia (MRP), and patients with left-limb paresthesia (MLP); in contrast, sigma values increased in the order of MRP, MWP, and MLP (C). The asterisk (*) denotes results without family-wise error (FWE) correction, **p < 0.05 after FWE correction, and ***p < 0.01 after FWE correction.

FIGURE 5

Comparison of nodal efficiency in the local network. In comparison with the healthy controls (HCs), MMD patients without paresthesia (MWP), patients with right-limb paresthesia (MRP), and patients with left-limb paresthesia (MLP) showed reductions in nodal efficiency in the following brain regions: MFG.L (A): MLP > MWP > MRP; MFG.R (B): MWP > MRP > MLP; IFGtriang.L (C): MLP > MWP > MRP; and IFGtriang.R (D):MWP > MRP > MLP;. The asterisk (*) denotes results without family-wise error (FWE) correction, **p < 0.05 after FWE correction, and ***p < 0.01 after FWE correction.

FIGURE 6

Comparison of degrees in the local network. In comparison with the healthy controls (HCs), MMD patients without paresthesia (MWP), patients with right-limb paresthesia (MRP), and patients with left-limb paresthesia (MLP) showed reductions in degree in the following brain regions: MFG.L (A): MLP > MWP > MRP; IFGtriang.L (B): MLP > MWP > MRP; and IFGtriang.R (C): MWP > MRP > MLP. Asterisk (*) denotes results without family-wise error (FWE) correction, ^**p < 0.05 after FWE correction, and ^***p < 0.01 after FWE correction.