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Research ArticleBrain Tumor

Pseudo-Resting-State Functional MRI Derived from Dynamic Susceptibility Contrast Perfusion MRI Can Predict Cognitive Impairment in Glioma

Nicholas S. Cho, Chencai Wang, Kathleen Van Dyk, Francesco Sanvito, Sonoko Oshima, Jingwen Yao, Albert Lai, Noriko Salamon, Timothy F. Cloughesy, Phioanh L. Nghiemphu and Benjamin M. Ellingson
American Journal of Neuroradiology October 2024, 45 (10) 1552-1561; DOI: https://doi.org/10.3174/ajnr.A8327
Nicholas S. Cho
aFrom the UCLA Brain Tumor Imaging Laboratory (BTIL) (N.S.C., C.W., F.S., S.O., J.Y., B.M.E.), Center for Computer Vision and Imaging Biomarkers, University of California, Los Angeles, Los Angeles, California
bDepartment of Radiological Sciences (N.S.C., C.W., F.S., S.O., J.Y., N.S., B.M.E.), David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California
cDepartment of Bioengineering (N.S.C., B.M.E.), Henry Samueli School of Engineering and Applied Science, University of California, Los Angeles, Los Angeles, California
dMedical Scientist Training Program (N.S.C.), David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California
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Chencai Wang
aFrom the UCLA Brain Tumor Imaging Laboratory (BTIL) (N.S.C., C.W., F.S., S.O., J.Y., B.M.E.), Center for Computer Vision and Imaging Biomarkers, University of California, Los Angeles, Los Angeles, California
bDepartment of Radiological Sciences (N.S.C., C.W., F.S., S.O., J.Y., N.S., B.M.E.), David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California
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Kathleen Van Dyk
eDepartment of Psychiatry and Biobehavioral Sciences (K.V.D, B.M.E.), David Geffen School of Medicine, Semel Institute, University of California Los Angeles, Los Angeles, California
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Francesco Sanvito
aFrom the UCLA Brain Tumor Imaging Laboratory (BTIL) (N.S.C., C.W., F.S., S.O., J.Y., B.M.E.), Center for Computer Vision and Imaging Biomarkers, University of California, Los Angeles, Los Angeles, California
bDepartment of Radiological Sciences (N.S.C., C.W., F.S., S.O., J.Y., N.S., B.M.E.), David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California
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Sonoko Oshima
aFrom the UCLA Brain Tumor Imaging Laboratory (BTIL) (N.S.C., C.W., F.S., S.O., J.Y., B.M.E.), Center for Computer Vision and Imaging Biomarkers, University of California, Los Angeles, Los Angeles, California
bDepartment of Radiological Sciences (N.S.C., C.W., F.S., S.O., J.Y., N.S., B.M.E.), David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California
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Jingwen Yao
aFrom the UCLA Brain Tumor Imaging Laboratory (BTIL) (N.S.C., C.W., F.S., S.O., J.Y., B.M.E.), Center for Computer Vision and Imaging Biomarkers, University of California, Los Angeles, Los Angeles, California
bDepartment of Radiological Sciences (N.S.C., C.W., F.S., S.O., J.Y., N.S., B.M.E.), David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California
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Albert Lai
fUCLA Neuro-Oncology Program (A.L., T.F.C., P.L.N.), David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California
gDepartment of Neurology (A.L., T.F.C., P.L.N.), David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California
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Noriko Salamon
bDepartment of Radiological Sciences (N.S.C., C.W., F.S., S.O., J.Y., N.S., B.M.E.), David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California
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Timothy F. Cloughesy
fUCLA Neuro-Oncology Program (A.L., T.F.C., P.L.N.), David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California
gDepartment of Neurology (A.L., T.F.C., P.L.N.), David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California
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Phioanh L. Nghiemphu
fUCLA Neuro-Oncology Program (A.L., T.F.C., P.L.N.), David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California
gDepartment of Neurology (A.L., T.F.C., P.L.N.), David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California
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Benjamin M. Ellingson
aFrom the UCLA Brain Tumor Imaging Laboratory (BTIL) (N.S.C., C.W., F.S., S.O., J.Y., B.M.E.), Center for Computer Vision and Imaging Biomarkers, University of California, Los Angeles, Los Angeles, California
bDepartment of Radiological Sciences (N.S.C., C.W., F.S., S.O., J.Y., N.S., B.M.E.), David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California
cDepartment of Bioengineering (N.S.C., B.M.E.), Henry Samueli School of Engineering and Applied Science, University of California, Los Angeles, Los Angeles, California
eDepartment of Psychiatry and Biobehavioral Sciences (K.V.D, B.M.E.), David Geffen School of Medicine, Semel Institute, University of California Los Angeles, Los Angeles, California
hDepartment of Neurosurgery (B.M.E.), David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California
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Abstract

BACKGROUND AND PURPOSE: Resting-state functional MRI (rs-fMRI) can be used to estimate functional connectivity (FC) between different brain regions, which may be of value for identifying cognitive impairment in patients with brain tumors. Unfortunately, neither rs-fMRI nor neurocognitive assessments are routinely assessed clinically, mostly due to limitations in examination time and cost. Since DSC perfusion MRI is often used clinically to assess tumor vascularity and similarly uses a gradient-echo-EPI sequence for T2*-sensitivity, we theorized a “pseudo-rs-fMRI” signal could be derived from DSC perfusion to simultaneously quantify FC and perfusion metrics, and these metrics can be used to estimate cognitive impairment in patients with brain tumors.

MATERIALS AND METHODS: Twenty-four consecutive patients with gliomas were enrolled in a prospective study that included DSC perfusion MRI, resting-sate functional MRI (rs-fMRI), and neurocognitive assessment. Voxelwise modeling of contrast bolus dynamics during DSC acquisition was performed and then subtracted from the original signal to generate a residual “pseudo-rs-fMRI” signal. Following the preprocessing of pseudo-rs-fMRI, full rs-fMRI, and a truncated version of the full rs-fMRI (first 100 timepoints) data, the default mode, motor, and language network maps were generated with atlas-based ROIs, Dice scores were calculated for the resting-state network maps from pseudo-rs-fMRI and truncated rs-fMRI using the full rs-fMRI maps as reference. Seed-to-voxel and ROI-to-ROI analyses were performed to assess FC differences between cognitively impaired and nonimpaired patients.

RESULTS: Dice scores for the group-level and patient-level (mean±SD) default mode, motor, and language network maps using pseudo-rs-fMRI were 0.905/0.689 ± 0.118 (group/patient), 0.973/0.730 ± 0.124, and 0.935/0.665 ± 0.142, respectively. There was no significant difference in Dice scores between pseudo-rs-fMRI and the truncated rs-fMRI default mode (P = .97) or language networks (P = .30), but there was a difference in motor networks (P = .02). A multiple logistic regression classifier applied to ROI-to-ROI FC networks using pseudo-rs-fMRI could identify cognitively impaired patients (sensitivity = 84.6%, specificity = 63.6%, receiver operating characteristic area under the curve (AUC) = 0.7762 ± 0.0954 (standard error), P = .0221) and performance was not significantly different from full rs-fMRI predictions (AUC = 0.8881 ± 0.0733 (standard error), P = .0013, P = .29 compared with pseudo-rs-fMRI).

CONCLUSIONS: DSC perfusion MRI-derived pseudo-rs-fMRI data can be used to perform typical rs-fMRI FC analyses that may identify cognitive decline in patients with brain tumors while still simultaneously performing perfusion analyses.

ABBREVIATIONS:

ASL
arterial spin-labeling
AUC
area under curve
BOLD
blood oxygenation level–dependent
FC
functional connectivity
FDR
false discovery rate
FWE
family-wise error
MNI
Montreal Neurological Institute
ROC
receiver operating characteristic
rs-fMRI
resting-state functional MRI
  • © 2024 by American Journal of Neuroradiology
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American Journal of Neuroradiology: 45 (10)
American Journal of Neuroradiology
Vol. 45, Issue 10
1 Oct 2024
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Nicholas S. Cho, Chencai Wang, Kathleen Van Dyk, Francesco Sanvito, Sonoko Oshima, Jingwen Yao, Albert Lai, Noriko Salamon, Timothy F. Cloughesy, Phioanh L. Nghiemphu, Benjamin M. Ellingson
Pseudo-Resting-State Functional MRI Derived from Dynamic Susceptibility Contrast Perfusion MRI Can Predict Cognitive Impairment in Glioma
American Journal of Neuroradiology Oct 2024, 45 (10) 1552-1561; DOI: 10.3174/ajnr.A8327

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Dynamic Perfusion MRI and Cognitive Impairment
Nicholas S. Cho, Chencai Wang, Kathleen Van Dyk, Francesco Sanvito, Sonoko Oshima, Jingwen Yao, Albert Lai, Noriko Salamon, Timothy F. Cloughesy, Phioanh L. Nghiemphu, Benjamin M. Ellingson
American Journal of Neuroradiology Oct 2024, 45 (10) 1552-1561; DOI: 10.3174/ajnr.A8327
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