Reorganization of gray matter networks in patients with Moyamoya disease

Abstract

Patients with Moyamoya disease (MMD) exhibit significant alterations in brain structure and function, but knowledge regarding gray matter networks is limited. The study enrolled 136 MMD patients and 99 healthy controls (HCs). Clinical characteristics and gray matter network topology were analyzed. Compared to HCs, MMD patients exhibited decreased clustering coefficient (Cp) (P = 0.006) and local efficiency (Eloc) (P = 0.013). Ischemic patients showed decreased Eloc and increased characteristic path length (Lp) compared to asymptomatic and hemorrhagic patients (P < 0.001, Bonferroni corrected). MMD patients had significant regional abnormalities, including decreased degree centrality (DC) in the left medial orbital superior frontal gyrus, left orbital inferior frontal gyrus, and right calcarine fissure and surrounding cortex (P < 0.05, FDR corrected). Increased DC was found in bilateral olfactory regions, with higher betweenness centrality (BC) in the right median cingulate, paracingulate fusiform gyrus, and left pallidum (P < 0.05, FDR corrected). Ischemic patients had lower BC in the right hippocampus compared to hemorrhagic patients, while hemorrhagic patients had decreased DC in the right triangular part of the inferior frontal gyrus compared to asymptomatic patients (P < 0.05, Bonferroni corrected). Subnetworks related to MMD and white matter hyperintensity volume were identified. There is significant reorganization of gray matter networks in patients compared to HCs, and among different types of patients. Gray matter networks can effectively detect MMD-related brain structural changes.

Keywords: Graph theory; Gray Matter Network; Gray Matter volume; Moyamoya Disease; Network-based statistic.

Fig. 1

Small-worldness properties of MMD and HC in the defined sparsity. (A) normalized clustering coefficients were larger than 1, (B) normalized characteristic path lengths were approximately equal to 1, and (C) small worldness coefficients were bigger than 1.

Fig. 2

Regions of significant differences in nodal degree centrality or betweenness centrality of gray matter morphological networks between MMD patients and healthy controls, showing both increases (red) and decreases (blue) in MMD compared to HC. OLF.L, left olfactory cortex; OLF.R, right olfactory cortex; DCG.R, right median cingulate and paracingulate gyri; FFG.R, fusiform gyrus; PAL.L, left pallidum; ORBinf.L, left orbital part of inferior frontal gyrus; ORBsupmed.L, left medial orbital superior frontal gyrus; CAL.R, right calcarine fissure and surrounding cortex.

Fig. 3

Regions exhibiting altered nodal degree centrality or betweenness centrality among MMD patients. IFGtriang.R, right triangular part of inferior frontal gyrus; HIP.R, right hippocampus; DC, degree centrality; BC, betweenness centrality.

Fig. 4

Subnetworks identified using NBS prediction (A) Subnetworks with significant classification between MMD and HC. (B) NBS-based regression on volume of white matter hyperintensity.

Fig. 5

Flowchart for the construction of gray matter morphological networks using T1-weighted MRI. (a) Gray matter volume maps created using a routine VBM procedure were smoothed with a 15 mm FWHM Gaussian kernel. (b) The gray matter volume maps were divided into 90 regions based on the AAL atlases. (c) Individual gray matter volume connectivity was constructed using the Graynet software. (d) The histogram (hi) distance between each pair of nodes was calculated, resulting in a morphological similarity. (e) The network properties of gray matter morphological networks were finally calculated at both the global and nodal levels.