Predicting memory decline from left temporal lobe epilepsy surgery using preoperative fMRI: a multicenter study
Objective: While fMRI language laterality has been used to predict verbal memory after epilepsy surgery, supporting evidence is not yet definitive. The FMRI in Anterior Temporal Epilepsy Surgery (FATES) project was a prospective observational cohort study at 10 US epilepsy centers, performed to dete...
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Elsevier
2025-01-01
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| Series: | NeuroImage: Clinical |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2213158225000749 |
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| author | William L. Gross Sara J. Swanson Alexander I. Helfand Sara B. Pillay Colin J. Humphries Manoj Raghavan Wade M. Mueller Chad E. Carlson Lisa L. Conant Robyn M. Busch Mark Lowe Madalina E. Tivarus Daniel L. Drane Monica Jacobs Victoria L. Morgan Jane B. Allendorfer Jerzy P. Szaflarski Leonardo Bonilha Susan Bookheimer Thomas Grabowski Jennifer Vannest Jeffrey R. Binder |
| author_facet | William L. Gross Sara J. Swanson Alexander I. Helfand Sara B. Pillay Colin J. Humphries Manoj Raghavan Wade M. Mueller Chad E. Carlson Lisa L. Conant Robyn M. Busch Mark Lowe Madalina E. Tivarus Daniel L. Drane Monica Jacobs Victoria L. Morgan Jane B. Allendorfer Jerzy P. Szaflarski Leonardo Bonilha Susan Bookheimer Thomas Grabowski Jennifer Vannest Jeffrey R. Binder |
| author_sort | William L. Gross |
| collection | DOAJ |
| description | Objective: While fMRI language laterality has been used to predict verbal memory after epilepsy surgery, supporting evidence is not yet definitive. The FMRI in Anterior Temporal Epilepsy Surgery (FATES) project was a prospective observational cohort study at 10 US epilepsy centers, performed to determine whether a multivariable model including fMRI language laterality can predict verbal memory outcome 6 months after left temporal lobe epilepsy surgery. Methods: This analysis includes 70 adults who underwent left temporal lobe epilepsy surgeries including hippocampal resection for treatment of epilepsy. Patients completed standard protocols, including preoperative fMRI language mapping with a semantic decision versus tone decision (SDTD) task contrast and preoperative and postoperative verbal memory assessment. Five memory measures, obtained from the Selective Reminding Test, Rey Auditory Verbal Learning Test, and Wechsler Memory Scale, were selected to cover a range of episodic memory tasks including word list learning, delayed list recall, and story recall. Multiple linear regression was performed using the preoperative memory score, duration of epilepsy, age at epilepsy onset, age at surgery, hippocampal sclerosis status, and fMRI SDTD laterality index (LI) as predictor variables for 6-month postoperative verbal memory change. Results: Across different memory measures, decline (defined using Reliable Change Index) was seen in 8%–28% of patients. Changes on all five memory measures were significantly correlated with preoperative score, epilepsy duration, and fMRI SDTD LI. Variance explained by linear regression models for each test ranged from 34%–41%, with fMRI LI independently accounting for 7%–25% of the total variance (all p < 0.05). Cross-validation accuracy for predicting change scores in independent held-back samples ranged from 0.54–0.75 standard deviations of the preoperative sample. Significance: We demonstrate that models incorporating fMRI language LIs from a semantic decision task trained to predict verbal memory decline after left temporal lobe surgery provide meaningful information to help inform patients of the risk associated with left temporal lobe surgery and are practical to implement in different hospital settings. This confirms previous limited evidence that fMRI-based preoperative language protocols can be used to predict verbal episodic memory outcome after left temporal lobe epilepsy surgery. |
| format | Article |
| id | doaj-art-e93bc6a1662d4f0f8a895b5e437cf9fb |
| institution | OA Journals |
| issn | 2213-1582 |
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| publishDate | 2025-01-01 |
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| series | NeuroImage: Clinical |
| spelling | doaj-art-e93bc6a1662d4f0f8a895b5e437cf9fb2025-08-20T02:34:43ZengElsevierNeuroImage: Clinical2213-15822025-01-014610380410.1016/j.nicl.2025.103804Predicting memory decline from left temporal lobe epilepsy surgery using preoperative fMRI: a multicenter studyWilliam L. Gross0Sara J. Swanson1Alexander I. Helfand2Sara B. Pillay3Colin J. Humphries4Manoj Raghavan5Wade M. Mueller6Chad E. Carlson7Lisa L. Conant8Robyn M. Busch9Mark Lowe10Madalina E. Tivarus11Daniel L. Drane12Monica Jacobs13Victoria L. Morgan14Jane B. Allendorfer15Jerzy P. Szaflarski16Leonardo Bonilha17Susan Bookheimer18Thomas Grabowski19Jennifer Vannest20Jeffrey R. Binder21Department of Neurology, Medical College of Wisconsin, Milwaukee, WI, United States; Department of Anesthesiology, Medical College of Wisconsin, Milwaukee, WI, United States; Corresponding author at: Department of Anesthesiology and Neurology, Medical College of Wisconsin, 8701 Watertown Plank Rd, Milwaukee, WI 53226, United States.Department of Neurology, Medical College of Wisconsin, Milwaukee, WI, United StatesDepartment of Neurology, Henry Ford Health System, Detroit, MI, United StatesDepartment of Neurology, Medical College of Wisconsin, Milwaukee, WI, United StatesDepartment of Neurology, Medical College of Wisconsin, Milwaukee, WI, United StatesDepartment of Neurology, Medical College of Wisconsin, Milwaukee, WI, United StatesDepartment of Neurosurgery, Medical College of Wisconsin, Milwaukee, WI, United StatesDepartment of Neurology, Medical College of Wisconsin, Milwaukee, WI, United StatesDepartment of Neurology, Medical College of Wisconsin, Milwaukee, WI, United StatesDepartment of Neurology and Epilepsy Center, Cleveland Clinic, Cleveland, OH, United StatesDepartment of Radiology, Cleveland Clinic, Cleveland, OH, United StatesDepartment of Imaging Sciences, University of Rochester, Rochester, NY, United StatesDepartment of Neurology and Pediatrics, Emory University, Atlanta, GA, United StatesDepartment of Psychiatry, Vanderbilt University Medical Center, Nashville, TN, United StatesDepartment of Radiology, Vanderbilt University Medical Center, Nashville, TN, United StatesDepartment of Neurology, University of Alabama at Birmingham, Birmingham, AL, United StatesDepartment of Neurology, University of Alabama at Birmingham, Birmingham, AL, United StatesDepartment of Neurology, University of South Carolina, Charleston, SC, United StatesDepartment of Neurology, University of California, Los Angeles, CA, United StatesDepartments of Radiology and Neurology, University of Washington, Seattle, WA, United StatesDepartment of Neurology, University of Cincinnati, Cincinnati, OH, United StatesDepartment of Neurology, Medical College of Wisconsin, Milwaukee, WI, United StatesObjective: While fMRI language laterality has been used to predict verbal memory after epilepsy surgery, supporting evidence is not yet definitive. The FMRI in Anterior Temporal Epilepsy Surgery (FATES) project was a prospective observational cohort study at 10 US epilepsy centers, performed to determine whether a multivariable model including fMRI language laterality can predict verbal memory outcome 6 months after left temporal lobe epilepsy surgery. Methods: This analysis includes 70 adults who underwent left temporal lobe epilepsy surgeries including hippocampal resection for treatment of epilepsy. Patients completed standard protocols, including preoperative fMRI language mapping with a semantic decision versus tone decision (SDTD) task contrast and preoperative and postoperative verbal memory assessment. Five memory measures, obtained from the Selective Reminding Test, Rey Auditory Verbal Learning Test, and Wechsler Memory Scale, were selected to cover a range of episodic memory tasks including word list learning, delayed list recall, and story recall. Multiple linear regression was performed using the preoperative memory score, duration of epilepsy, age at epilepsy onset, age at surgery, hippocampal sclerosis status, and fMRI SDTD laterality index (LI) as predictor variables for 6-month postoperative verbal memory change. Results: Across different memory measures, decline (defined using Reliable Change Index) was seen in 8%–28% of patients. Changes on all five memory measures were significantly correlated with preoperative score, epilepsy duration, and fMRI SDTD LI. Variance explained by linear regression models for each test ranged from 34%–41%, with fMRI LI independently accounting for 7%–25% of the total variance (all p < 0.05). Cross-validation accuracy for predicting change scores in independent held-back samples ranged from 0.54–0.75 standard deviations of the preoperative sample. Significance: We demonstrate that models incorporating fMRI language LIs from a semantic decision task trained to predict verbal memory decline after left temporal lobe surgery provide meaningful information to help inform patients of the risk associated with left temporal lobe surgery and are practical to implement in different hospital settings. This confirms previous limited evidence that fMRI-based preoperative language protocols can be used to predict verbal episodic memory outcome after left temporal lobe epilepsy surgery.http://www.sciencedirect.com/science/article/pii/S2213158225000749Epilepsy surgeryTemporal lobe epilepsyVerbal memoryLanguage laterality |
| spellingShingle | William L. Gross Sara J. Swanson Alexander I. Helfand Sara B. Pillay Colin J. Humphries Manoj Raghavan Wade M. Mueller Chad E. Carlson Lisa L. Conant Robyn M. Busch Mark Lowe Madalina E. Tivarus Daniel L. Drane Monica Jacobs Victoria L. Morgan Jane B. Allendorfer Jerzy P. Szaflarski Leonardo Bonilha Susan Bookheimer Thomas Grabowski Jennifer Vannest Jeffrey R. Binder Predicting memory decline from left temporal lobe epilepsy surgery using preoperative fMRI: a multicenter study NeuroImage: Clinical Epilepsy surgery Temporal lobe epilepsy Verbal memory Language laterality |
| title | Predicting memory decline from left temporal lobe epilepsy surgery using preoperative fMRI: a multicenter study |
| title_full | Predicting memory decline from left temporal lobe epilepsy surgery using preoperative fMRI: a multicenter study |
| title_fullStr | Predicting memory decline from left temporal lobe epilepsy surgery using preoperative fMRI: a multicenter study |
| title_full_unstemmed | Predicting memory decline from left temporal lobe epilepsy surgery using preoperative fMRI: a multicenter study |
| title_short | Predicting memory decline from left temporal lobe epilepsy surgery using preoperative fMRI: a multicenter study |
| title_sort | predicting memory decline from left temporal lobe epilepsy surgery using preoperative fmri a multicenter study |
| topic | Epilepsy surgery Temporal lobe epilepsy Verbal memory Language laterality |
| url | http://www.sciencedirect.com/science/article/pii/S2213158225000749 |
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