Surgical resection of ripple onset predicts outcome in pediatric epilepsy
Eleonora Tamilia PhD
Laboratory of Children's Brain Dynamics, Division of Newborn Medicine, Department of Medicine, Boston Children's Hospital, Harvard Medical School, Boston, MA
Fetal-Neonatal Neuroimaging and Developmental Science Center, Division of Newborn Medicine, Department of Medicine, Boston Children's Hospital, Harvard Medical School, Boston, MA
Search for more papers by this authorEun-Hyoung Park PhD
Division of Epilepsy Surgery, Department of Neurosurgery, Boston Children's Hospital, Harvard Medical School, Boston, MA
Search for more papers by this authorStefania Percivati
Laboratory of Children's Brain Dynamics, Division of Newborn Medicine, Department of Medicine, Boston Children's Hospital, Harvard Medical School, Boston, MA
Unit of Biomedical Robotics and Biomicrosystems, Engineering Department, Università Campus Bio-Medico di Roma, Rome, Italy
Search for more papers by this authorJeffrey Bolton MD
Division of Epilepsy and Clinical Neurophysiology, Department of Neurology, Boston Children's Hospital, Harvard Medical School, Boston, MA
Search for more papers by this authorFabrizio Taffoni PhD
Unit of Biomedical Robotics and Biomicrosystems, Engineering Department, Università Campus Bio-Medico di Roma, Rome, Italy
Search for more papers by this authorJurriaan M. Peters MD, PhD
Division of Epilepsy and Clinical Neurophysiology, Department of Neurology, Boston Children's Hospital, Harvard Medical School, Boston, MA
Search for more papers by this authorP. Ellen Grant MD
Fetal-Neonatal Neuroimaging and Developmental Science Center, Division of Newborn Medicine, Department of Medicine, Boston Children's Hospital, Harvard Medical School, Boston, MA
Search for more papers by this authorPhillip L. Pearl MD
Division of Epilepsy and Clinical Neurophysiology, Department of Neurology, Boston Children's Hospital, Harvard Medical School, Boston, MA
Search for more papers by this authorJoseph R. Madsen MD
Division of Epilepsy Surgery, Department of Neurosurgery, Boston Children's Hospital, Harvard Medical School, Boston, MA
Search for more papers by this authorCorresponding Author
Christos Papadelis PhD
Laboratory of Children's Brain Dynamics, Division of Newborn Medicine, Department of Medicine, Boston Children's Hospital, Harvard Medical School, Boston, MA
Fetal-Neonatal Neuroimaging and Developmental Science Center, Division of Newborn Medicine, Department of Medicine, Boston Children's Hospital, Harvard Medical School, Boston, MA
Address correspondence to Dr Christos Papadelis, Laboratory of Children's Brain Dynamics, Division of Newborn Medicine, Boston Children's Hospital, Harvard Medical School, Neonatal Neuroimaging BCH 3181, 300 Longwood Avenue, Boston, MA 02115. E-mail: [email protected]Search for more papers by this authorEleonora Tamilia PhD
Laboratory of Children's Brain Dynamics, Division of Newborn Medicine, Department of Medicine, Boston Children's Hospital, Harvard Medical School, Boston, MA
Fetal-Neonatal Neuroimaging and Developmental Science Center, Division of Newborn Medicine, Department of Medicine, Boston Children's Hospital, Harvard Medical School, Boston, MA
Search for more papers by this authorEun-Hyoung Park PhD
Division of Epilepsy Surgery, Department of Neurosurgery, Boston Children's Hospital, Harvard Medical School, Boston, MA
Search for more papers by this authorStefania Percivati
Laboratory of Children's Brain Dynamics, Division of Newborn Medicine, Department of Medicine, Boston Children's Hospital, Harvard Medical School, Boston, MA
Unit of Biomedical Robotics and Biomicrosystems, Engineering Department, Università Campus Bio-Medico di Roma, Rome, Italy
Search for more papers by this authorJeffrey Bolton MD
Division of Epilepsy and Clinical Neurophysiology, Department of Neurology, Boston Children's Hospital, Harvard Medical School, Boston, MA
Search for more papers by this authorFabrizio Taffoni PhD
Unit of Biomedical Robotics and Biomicrosystems, Engineering Department, Università Campus Bio-Medico di Roma, Rome, Italy
Search for more papers by this authorJurriaan M. Peters MD, PhD
Division of Epilepsy and Clinical Neurophysiology, Department of Neurology, Boston Children's Hospital, Harvard Medical School, Boston, MA
Search for more papers by this authorP. Ellen Grant MD
Fetal-Neonatal Neuroimaging and Developmental Science Center, Division of Newborn Medicine, Department of Medicine, Boston Children's Hospital, Harvard Medical School, Boston, MA
Search for more papers by this authorPhillip L. Pearl MD
Division of Epilepsy and Clinical Neurophysiology, Department of Neurology, Boston Children's Hospital, Harvard Medical School, Boston, MA
Search for more papers by this authorJoseph R. Madsen MD
Division of Epilepsy Surgery, Department of Neurosurgery, Boston Children's Hospital, Harvard Medical School, Boston, MA
Search for more papers by this authorCorresponding Author
Christos Papadelis PhD
Laboratory of Children's Brain Dynamics, Division of Newborn Medicine, Department of Medicine, Boston Children's Hospital, Harvard Medical School, Boston, MA
Fetal-Neonatal Neuroimaging and Developmental Science Center, Division of Newborn Medicine, Department of Medicine, Boston Children's Hospital, Harvard Medical School, Boston, MA
Address correspondence to Dr Christos Papadelis, Laboratory of Children's Brain Dynamics, Division of Newborn Medicine, Boston Children's Hospital, Harvard Medical School, Neonatal Neuroimaging BCH 3181, 300 Longwood Avenue, Boston, MA 02115. E-mail: [email protected]Search for more papers by this authorAbstract
Objective
In patients with medically refractory epilepsy (MRE), interictal ripples (80–250Hz) are observed in large brain areas whose resection may be unnecessary for seizure freedom. This limits their utility as epilepsy biomarkers for surgery. We assessed the spatiotemporal propagation of interictal ripples on intracranial electroencephalography (iEEG) in children with MRE, compared it with the propagation of spikes, identified ripples that initiated propagation (onset-ripples), and evaluated their clinical value as epilepsy biomarkers.
Methods
Twenty-seven children who underwent epilepsy surgery were studied. We identified propagation sequences of ripples and spikes across multiple iEEG contacts and calculated each ripple or spike latency from the propagation onset. We classified ripples and spikes into categories (ie, onset, spread, and isolated) based on their spatiotemporal characteristics and correlated their mean rate inside and outside resection with outcome (good outcome, Engel 1 versus poor outcome, Engel≥2). We determined, as onset-zone, spread-zone, and isolated-zone, the areas generating the corresponding ripple or spike category and evaluated the predictive value of their resection.
Results
We observed ripple propagation in all patients and spike propagation in 25 patients. Mean rate of onset-ripples inside resection predicted the outcome (odds ratio = 5.37; p = 0.02) and correlated with Engel class (rho = −0.55; p = 0.003). Resection of the onset-ripple-zone was associated with good outcome (p = 0.047). No association was found for the spread-ripple-zone, isolated-ripple-zone, or any spike-zone.
Interpretation
Interictal ripples propagate across iEEG contacts in children with MRE. The association between the onset-ripple-zone resection and good outcome indicates that onset-ripples are promising epilepsy biomarkers, which estimate the epileptogenic tissue better than spread-ripples or onset-spikes. Ann Neurol 2018;84:331–346
Potential Conflicts of Interest
Nothing to report.
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