Correlating Resting-State Functional Magnetic Resonance Imaging Connectivity by Independent Component Analysis-Based Epileptogenic Zones with Intracranial Electroencephalogram Localized Seizure Onset Zones and Surgical Outcomes in Prospective Pediatric Intractable Epilepsy Study

Varina L. Boerwinkle, 1 Division of Pediatric Neurology, Barrow Neurological Institute at Phoenix Children's Hospital , Phoenix, Arizona.Follow
Deepankar Mohanty, 2 Department of Pediatric Neurology, Texas Children's Hospital , Baylor College of Medicine, Houston, Texas.
Stephen T. Foldes, 3 Neuroscience Research, Barrow Neurological Institute at Phoenix Children's Hospital , Phoenix, Arizona.Follow
Danielle Guffey, 4 Dan L. Duncan Institute for Clinical and Translational Research , Baylor College of Medicine, Houston, Texas.
Charles G. Minard, 4 Dan L. Duncan Institute for Clinical and Translational Research , Baylor College of Medicine, Houston, Texas.
Aditya Vedantam, 5 Department of Pediatric Neurosurgery, Texas Children's Hospital , Baylor College of Medicine, Houston, Texas.
Jeffrey S. Raskin, 5 Department of Pediatric Neurosurgery, Texas Children's Hospital , Baylor College of Medicine, Houston, Texas.
Sandi Lam, 5 Department of Pediatric Neurosurgery, Texas Children's Hospital , Baylor College of Medicine, Houston, Texas.
Margaret Bond, 2 Department of Pediatric Neurology, Texas Children's Hospital , Baylor College of Medicine, Houston, Texas.
Lucia Mirea, 6 Department of Research, Phoenix Children's Hospital , Phoenix, Arizona.
P David Adelson, 1 Division of Pediatric Neurology, Barrow Neurological Institute at Phoenix Children's Hospital , Phoenix, Arizona.Follow
Angus A. Wilfong, 1 Division of Pediatric Neurology, Barrow Neurological Institute at Phoenix Children's Hospital , Phoenix, Arizona.
Daniel J. Curry, 5 Department of Pediatric Neurosurgery, Texas Children's Hospital , Baylor College of Medicine, Houston, Texas.

Document Type

Article

Abstract

The purpose of this study was to prospectively investigate the agreement between the epileptogenic zone(s) (EZ) localization by resting-state functional magnetic resonance imaging (rs-fMRI) and the seizure onset zone(s) (SOZ) identified by intracranial electroencephalogram (ic-EEG) using novel differentiating and ranking criteria of rs-fMRI abnormal independent components (ICs) in a large consecutive heterogeneous pediatric intractable epilepsy population without an a priori alternate modality informing EZ localization or prior declaration of total SOZ number. The EZ determination criteria were developed by using independent component analysis (ICA) on rs-fMRI in an initial cohort of 350 pediatric patients evaluated for epilepsy surgery over a 3-year period. Subsequently, these rs-fMRI EZ criteria were applied prospectively to an evaluation cohort of 40 patients who underwent ic-EEG for SOZ identification. Thirty-seven of these patients had surgical resection/disconnection of the area believed to be the primary source of seizures. One-year seizure frequency rate was collected postoperatively. Among the total 40 patients evaluated, agreement between rs-fMRI EZ and ic-EEG SOZ was 90% (36/40; 95% confidence interval [CI], 0.76-0.97). Of the 37 patients who had surgical destruction of the area believed to be the primary source of seizures, 27 (73%) rs-fMRI EZ could be classified as true positives, 7 (18%) false positives, and 2 (5%) false negatives. Sensitivity of rs-fMRI EZ was 93% (95% CI 78-98%) with a positive predictive value of 79% (95% CI, 63-89%). In those with cryptogenic localization-related epilepsy, agreement between rs-fMRI EZ and ic-EEG SOZ was 89% (8/9; 95% CI, 0.52-99), with no statistically significant difference between the agreement in the cryptogenic and symptomatic localization-related epilepsy subgroups. Two children with negative ic-EEG had removal of the rs-fMRI EZ and were seizure free 1 year postoperatively. Of the 33 patients where at least 1 rs-fMRI EZ agreed with the ic-EEG SOZ, 24% had at least 1 additional rs-fMRI EZ outside the resection area. Of these patients with un-resected rs-fMRI EZ, 75% continued to have seizures 1 year later. Conversely, among 75% of patients in whom rs-fMRI agreed with ic-EEG SOZ and had no anatomically separate rs-fMRI EZ, only 24% continued to have seizures 1 year later. This relationship between extraneous rs-fMRI EZ and seizure outcome was statistically significant (p = 0.01). rs-fMRI EZ surgical destruction showed significant association with postoperative seizure outcome. The pediatric population with intractable epilepsy studied prospectively provides evidence for use of resting-state ICA ranking criteria, to identify rs-fMRI EZ, as developed by the lead author (V.L.B.). This is a high yield test in this population, because no seizure nor particular interictal epilepiform activity needs to occur during the study. Thus, rs-fMRI EZ detected by this technique are potentially informative for epilepsy surgery evaluation and planning in this population. Independent of other brain function testing modalities, such as simultaneous EEG-fMRI or electrical source imaging, contextual ranking of abnormal ICs of rs-fMRI localized EZs correlated with the gold standard of SOZ localization, ic-EEG, across the broad range of pediatric epilepsy surgery candidates, including those with cryptogenic epilepsy.

Keywords

epilepsy surgery, functional connectivity, independent component analysis, intraoperative electrocorticography, resting-state functional MRI

Medical Subject Headings

Adolescent; Brain (diagnostic imaging, physiopathology); Child; Child, Preschool; Drug Resistant Epilepsy (physiopathology, surgery); Electrocorticography; Epilepsies, Partial (physiopathology, surgery); Female; Humans; Infant; Magnetic Resonance Imaging; Male; Predictive Value of Tests; Prospective Studies; Seizures (physiopathology); Sensitivity and Specificity; Young Adult

Publication Date

9-1-2017

Publication Title

Brain connectivity

E-ISSN

2158-0022

Volume

7

Issue

7

First Page

424

Last Page

442

PubMed ID

28782373

Digital Object Identifier (DOI)

10.1089/brain.2016.0479

Link to Full Text

Share

COinS