The Resting-State Functional Magnetic Resonance Imaging Regional Homogeneity Metrics-Kendall's Coefficient of Concordance-Regional Homogeneity and Coherence-Regional Homogeneity-Are Valid Indicators of Tumor-Related Neurovascular Uncoupling

Abstract

The aim of this study is to determine whether regional homogeneity (ReHo) of resting-state blood oxygenation level-dependent (BOLD) functional magnetic resonance imaging (rsfMRI) data based on Kendall's coefficient of concordance (KCC-ReHo) and coherence (Cohe-ReHo) metrics may allow detection of brain tumor-induced neurovascular uncoupling (NVU) in the sensorimotor network similar to findings in standard motor task-based BOLD fMRI (tbfMRI) activation. Twelve de novo brain tumor patients undergoing clinical fMRI exams (tbfMRI and rsfMRI) were included in this Institutional Review Board (IRB)-approved study. Each patient displayed decreased/absent tbfMRI activation in the primary ipsilesional sensorimotor cortex in the absence of corresponding motor deficit or suboptimal task performance, consistent with NVU. Z-score maps for motor tasks were obtained from the general linear model (GLM) analysis (reflecting motor activation vs. rest). KCC-ReHo and Cohe-ReHo maps were calculated from rsfMRI data. Precentral and postcentral gyri in contralesional (CL) and ipsilesional (IL) hemispheres were parcellated using an automated anatomical labeling (AAL) template for each patient. Similar region of interest (ROI) analysis was performed on tbfMRI, KCC-ReHo, and Cohe-ReHo maps to allow direct comparison of results. Voxel values in CL and IL ROIs of each map were divided by the corresponding global mean of KCC-ReHo and Cohe-ReHo in bihemispheric cortical brain tissue. Group analysis revealed significantly decreased IL mean KCC-ReHo (p = 0.02) and Cohe-ReHo (p = 0.04) metrics compared with respective values in the CL ROIs, consistent with similar findings of significantly decreased ipsilesional BOLD signal for tbfMRI (p = 0.0005). Ipsilesional abnormalities in ReHo derived from rsfMRI may serve as potential indicators of NVU in patients with brain tumors and other resectable brain lesions; as such, ReHo findings may complement findings on tbfMRI used for presurgical planning.

Keywords: Kendall's coefficient of concordance regional homogeneity; coherence regional homogeneity; motor activation; neurovascular uncoupling; presurgical mapping; regional homogeneity; resting state fMRI.

FIG. 1.

Three cases are presented with the task-based activation map, KCC-ReHo map, and Cohe-ReHo map overlaid on T1-weighted structural images in each case. Patient 1: Patient with grade II oligodendroglioma. First row shows the vertical tongue motor fMRI activation map (tbfMRI) (Z-score >4.0) overlaid on T1-weighted structural images. Second and third rows show ReHo—KCC-ReHo and Cohe-ReHo, respectively—maps (KCC >0.45 and Cohe >0.3) from rsfMRI. Patient 2: Patient with grade III anaplastic astrocytoma. First row shows the tongue motor fMRI activation map (tbfMRI) (Z-score >3.5) overlaid on T1-weighted structural images. Second and third rows show ReHo—KCC-ReHo and Cohe-ReHo, respectively—maps (KCC >0.5 and Cohe >0.4) from rsfMRI. Patient 3: Patient with grade II oligoastrocytoma. First row shows the tongue motor fMRI activation map (tbfMRI) (Z-score >3.5) overlaid on T1-weighted structural images. Second and third rows show ReHo—KCC-ReHo and Cohe-ReHo, respectively—maps (KCC >0.4 and Cohe >0.3) from rsfMRI. Blue contours display ROIs from automatically parcellated combined precentral and postcentral gyri. Notice in all maps that there is abnormally decreased signal in the ipsilesional perirolandic ROIs (IL) compared with the normal contralesional perirolandic ROIs (CL). In the setting of preserved clinical motor function and excellent task performance, these findings are indicative of tumor-induced NVU. NVU, neurovascular uncoupling; ReHo, regional homogeneity; ROIs, regions of interest; rsfMRI, resting-state functional magnetic resonance imaging; tbfMRI, task-based fMRI.