High interictal connectivity within the resection zone is associated with favorable post-surgical outcomes in focal epilepsy patients
Patients with drug-resistant focal epilepsy are often candidates for invasive surgical therapies. In these patients, it is necessary to accurately localize seizure generators to ensure seizure freedom following intervention. While intracranial electroencephalography (iEEG) is the gold standard for m...
| Main Authors: | , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2019-01-01
|
| Series: | NeuroImage: Clinical |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S221315821930258X |
| _version_ | 1818897946953908224 |
|---|---|
| author | Preya Shah John M. Bernabei Lohith G. Kini Arian Ashourvan Jacqueline Boccanfuso Ryan Archer Kelly Oechsel Sandhitsu R. Das Joel M. Stein Timothy H. Lucas Danielle S. Bassett Kathryn A. Davis Brian Litt |
| author_facet | Preya Shah John M. Bernabei Lohith G. Kini Arian Ashourvan Jacqueline Boccanfuso Ryan Archer Kelly Oechsel Sandhitsu R. Das Joel M. Stein Timothy H. Lucas Danielle S. Bassett Kathryn A. Davis Brian Litt |
| author_sort | Preya Shah |
| collection | DOAJ |
| description | Patients with drug-resistant focal epilepsy are often candidates for invasive surgical therapies. In these patients, it is necessary to accurately localize seizure generators to ensure seizure freedom following intervention. While intracranial electroencephalography (iEEG) is the gold standard for mapping networks for surgery, this approach requires inducing and recording seizures, which may cause patient morbidity. The goal of this study is to evaluate the utility of mapping interictal (non-seizure) iEEG networks to identify targets for surgical treatment. We analyze interictal iEEG recordings and neuroimaging from 27 focal epilepsy patients treated via surgical resection. We generate interictal functional networks by calculating pairwise correlation of iEEG signals across different frequency bands. Using image coregistration and segmentation, we identify electrodes falling within surgically resected tissue (i.e. the resection zone), and compute node-level and edge-level synchrony in relation to the resection zone. We further associate these metrics with post-surgical outcomes. Greater overlap between resected electrodes and highly synchronous electrodes is associated with favorable post-surgical outcomes. Additionally, good-outcome patients have significantly higher connectivity localized within the resection zone compared to those with poorer postoperative seizure control. This finding persists following normalization by a spatially-constrained null model. This study suggests that spatially-informed interictal network synchrony measures can distinguish between good and poor post-surgical outcomes. By capturing clinically-relevant information during interictal periods, our method may ultimately reduce the need for prolonged invasive implants and provide insights into the pathophysiology of an epileptic brain. We discuss next steps for translating these findings into a prospectively useful clinical tool. Keywords: Epilepsy, Intracranial EEG, Functional connectivity |
| first_indexed | 2024-12-19T19:24:16Z |
| format | Article |
| id | doaj.art-c6c3dad978db4afe807e81463ef3c7b9 |
| institution | Directory Open Access Journal |
| issn | 2213-1582 |
| language | English |
| last_indexed | 2024-12-19T19:24:16Z |
| publishDate | 2019-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage: Clinical |
| spelling | doaj.art-c6c3dad978db4afe807e81463ef3c7b92022-12-21T20:08:52ZengElsevierNeuroImage: Clinical2213-15822019-01-0123High interictal connectivity within the resection zone is associated with favorable post-surgical outcomes in focal epilepsy patientsPreya Shah0John M. Bernabei1Lohith G. Kini2Arian Ashourvan3Jacqueline Boccanfuso4Ryan Archer5Kelly Oechsel6Sandhitsu R. Das7Joel M. Stein8Timothy H. Lucas9Danielle S. Bassett10Kathryn A. Davis11Brian Litt12Department of Bioengineering, School of Engineering & Applied Science, University of Pennsylvania, Philadelphia, PA 19104, USA; Center for Neuroengineering and Therapeutics, University of Pennsylvania, Philadelphia, PA 19104, USA; Corresponding author at: Department of Bioengineering, School of Engineering & Applied Science, University of Pennsylvania, Philadelphia, PA 19104, USA.Department of Bioengineering, School of Engineering & Applied Science, University of Pennsylvania, Philadelphia, PA 19104, USA; Center for Neuroengineering and Therapeutics, University of Pennsylvania, Philadelphia, PA 19104, USADepartment of Bioengineering, School of Engineering & Applied Science, University of Pennsylvania, Philadelphia, PA 19104, USA; Center for Neuroengineering and Therapeutics, University of Pennsylvania, Philadelphia, PA 19104, USADepartment of Bioengineering, School of Engineering & Applied Science, University of Pennsylvania, Philadelphia, PA 19104, USA; Center for Neuroengineering and Therapeutics, University of Pennsylvania, Philadelphia, PA 19104, USACenter for Neuroengineering and Therapeutics, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Neurology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USACenter for Neuroengineering and Therapeutics, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Neurology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USACenter for Neuroengineering and Therapeutics, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Neurology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USADepartment of Neurology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USADepartment of Radiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USADepartment of Neurosurgery, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USADepartment of Bioengineering, School of Engineering & Applied Science, University of Pennsylvania, Philadelphia, PA 19104, USA; Center for Neuroengineering and Therapeutics, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Neurology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Electrical & Systems Engineering, School of Engineering & Applied Science, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Physics & Astronomy, College of Arts & Sciences, University of Pennsylvania, Philadelphia, PA 19104, USACenter for Neuroengineering and Therapeutics, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Neurology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USADepartment of Bioengineering, School of Engineering & Applied Science, University of Pennsylvania, Philadelphia, PA 19104, USA; Center for Neuroengineering and Therapeutics, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Neurology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Neurosurgery, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USAPatients with drug-resistant focal epilepsy are often candidates for invasive surgical therapies. In these patients, it is necessary to accurately localize seizure generators to ensure seizure freedom following intervention. While intracranial electroencephalography (iEEG) is the gold standard for mapping networks for surgery, this approach requires inducing and recording seizures, which may cause patient morbidity. The goal of this study is to evaluate the utility of mapping interictal (non-seizure) iEEG networks to identify targets for surgical treatment. We analyze interictal iEEG recordings and neuroimaging from 27 focal epilepsy patients treated via surgical resection. We generate interictal functional networks by calculating pairwise correlation of iEEG signals across different frequency bands. Using image coregistration and segmentation, we identify electrodes falling within surgically resected tissue (i.e. the resection zone), and compute node-level and edge-level synchrony in relation to the resection zone. We further associate these metrics with post-surgical outcomes. Greater overlap between resected electrodes and highly synchronous electrodes is associated with favorable post-surgical outcomes. Additionally, good-outcome patients have significantly higher connectivity localized within the resection zone compared to those with poorer postoperative seizure control. This finding persists following normalization by a spatially-constrained null model. This study suggests that spatially-informed interictal network synchrony measures can distinguish between good and poor post-surgical outcomes. By capturing clinically-relevant information during interictal periods, our method may ultimately reduce the need for prolonged invasive implants and provide insights into the pathophysiology of an epileptic brain. We discuss next steps for translating these findings into a prospectively useful clinical tool. Keywords: Epilepsy, Intracranial EEG, Functional connectivityhttp://www.sciencedirect.com/science/article/pii/S221315821930258X |
| spellingShingle | Preya Shah John M. Bernabei Lohith G. Kini Arian Ashourvan Jacqueline Boccanfuso Ryan Archer Kelly Oechsel Sandhitsu R. Das Joel M. Stein Timothy H. Lucas Danielle S. Bassett Kathryn A. Davis Brian Litt High interictal connectivity within the resection zone is associated with favorable post-surgical outcomes in focal epilepsy patients NeuroImage: Clinical |
| title | High interictal connectivity within the resection zone is associated with favorable post-surgical outcomes in focal epilepsy patients |
| title_full | High interictal connectivity within the resection zone is associated with favorable post-surgical outcomes in focal epilepsy patients |
| title_fullStr | High interictal connectivity within the resection zone is associated with favorable post-surgical outcomes in focal epilepsy patients |
| title_full_unstemmed | High interictal connectivity within the resection zone is associated with favorable post-surgical outcomes in focal epilepsy patients |
| title_short | High interictal connectivity within the resection zone is associated with favorable post-surgical outcomes in focal epilepsy patients |
| title_sort | high interictal connectivity within the resection zone is associated with favorable post surgical outcomes in focal epilepsy patients |
| url | http://www.sciencedirect.com/science/article/pii/S221315821930258X |
| work_keys_str_mv | AT preyashah highinterictalconnectivitywithintheresectionzoneisassociatedwithfavorablepostsurgicaloutcomesinfocalepilepsypatients AT johnmbernabei highinterictalconnectivitywithintheresectionzoneisassociatedwithfavorablepostsurgicaloutcomesinfocalepilepsypatients AT lohithgkini highinterictalconnectivitywithintheresectionzoneisassociatedwithfavorablepostsurgicaloutcomesinfocalepilepsypatients AT arianashourvan highinterictalconnectivitywithintheresectionzoneisassociatedwithfavorablepostsurgicaloutcomesinfocalepilepsypatients AT jacquelineboccanfuso highinterictalconnectivitywithintheresectionzoneisassociatedwithfavorablepostsurgicaloutcomesinfocalepilepsypatients AT ryanarcher highinterictalconnectivitywithintheresectionzoneisassociatedwithfavorablepostsurgicaloutcomesinfocalepilepsypatients AT kellyoechsel highinterictalconnectivitywithintheresectionzoneisassociatedwithfavorablepostsurgicaloutcomesinfocalepilepsypatients AT sandhitsurdas highinterictalconnectivitywithintheresectionzoneisassociatedwithfavorablepostsurgicaloutcomesinfocalepilepsypatients AT joelmstein highinterictalconnectivitywithintheresectionzoneisassociatedwithfavorablepostsurgicaloutcomesinfocalepilepsypatients AT timothyhlucas highinterictalconnectivitywithintheresectionzoneisassociatedwithfavorablepostsurgicaloutcomesinfocalepilepsypatients AT daniellesbassett highinterictalconnectivitywithintheresectionzoneisassociatedwithfavorablepostsurgicaloutcomesinfocalepilepsypatients AT kathrynadavis highinterictalconnectivitywithintheresectionzoneisassociatedwithfavorablepostsurgicaloutcomesinfocalepilepsypatients AT brianlitt highinterictalconnectivitywithintheresectionzoneisassociatedwithfavorablepostsurgicaloutcomesinfocalepilepsypatients |