Prediction of Naming Outcome With fMRI Language Lateralization in Left Temporal Epilepsy Surgery

William Louis Gross; Alexander I Helfand; Sara J Swanson; Lisa L Conant; Colin J Humphries; Manoj Raghavan; Wade M Mueller; Robyn M Busch; Linda Allen; Christopher Todd Anderson; Chad E Carlson; Mark J Lowe; John T Langfitt; Madalina E Tivarus; Daniel L Drane; David W Loring; Monica Jacobs; Victoria L Morgan; Jane B Allendorfer; Jerzy P Szaflarski; Leonardo Bonilha; Susan Bookheimer; Thomas Grabowski; Jennifer Vannest; Jeffrey R Binder; FMRI in Anterior Temporal Epilepsy Surgery (FATES) Study

doi:10.1212/WNL.0000000000200552

Prediction of Naming Outcome With fMRI Language Lateralization in Left Temporal Epilepsy Surgery

Neurology. 2022 Jun 7;98(23):e2337-e2346. doi: 10.1212/WNL.0000000000200552. Epub 2022 Apr 11.

Authors

William Louis Gross¹, Alexander I Helfand², Sara J Swanson², Lisa L Conant², Colin J Humphries², Manoj Raghavan², Wade M Mueller², Robyn M Busch², Linda Allen², Christopher Todd Anderson², Chad E Carlson², Mark J Lowe², John T Langfitt², Madalina E Tivarus², Daniel L Drane², David W Loring², Monica Jacobs², Victoria L Morgan², Jane B Allendorfer², Jerzy P Szaflarski², Leonardo Bonilha², Susan Bookheimer², Thomas Grabowski², Jennifer Vannest², Jeffrey R Binder²; FMRI in Anterior Temporal Epilepsy Surgery (FATES) Study

Affiliations

¹ From the Departments of Neurology (W.L.G., A.H., S.J.S., L.L.C., C.H., M.R., L.A., C.T.A., C.E.C., J.R.B.), Anesthesiology (W.L.G.), and Neurosurgery (W.M.M.), Medical College of Wisconsin, Milwaukee; Departments of Neurology (R.M.B.) and Radiology (M.J.L.), Cleveland Clinic Foundation, OH; Departments of Neurology (J.T.L.) and Imaging Sciences (M.E.T.), University of Rochester, NY; Departments of Neurology (D.L.D., D.W.L.) and Pediatrics (D.L.D.), Emory University, Atlanta, GA; Department of Neurology (D.L.D., T.G.), University of Washington, Seattle; Departments of Psychology (M.J.) and Radiology (V.L.M.), Vanderbilt University Medical Center, Nashville, TN; Department of Neurology (J.B.A., J.P.S.), University of Alabama at Birmingham; Department of Neurology (L.B.), Medical University of South Carolina, Charleston; Department of Neurology (S.B.), University of California, Los Angeles; and Department of Neurology (J.V.), University of Cincinnati, OH. bgross@mcw.edu.
² From the Departments of Neurology (W.L.G., A.H., S.J.S., L.L.C., C.H., M.R., L.A., C.T.A., C.E.C., J.R.B.), Anesthesiology (W.L.G.), and Neurosurgery (W.M.M.), Medical College of Wisconsin, Milwaukee; Departments of Neurology (R.M.B.) and Radiology (M.J.L.), Cleveland Clinic Foundation, OH; Departments of Neurology (J.T.L.) and Imaging Sciences (M.E.T.), University of Rochester, NY; Departments of Neurology (D.L.D., D.W.L.) and Pediatrics (D.L.D.), Emory University, Atlanta, GA; Department of Neurology (D.L.D., T.G.), University of Washington, Seattle; Departments of Psychology (M.J.) and Radiology (V.L.M.), Vanderbilt University Medical Center, Nashville, TN; Department of Neurology (J.B.A., J.P.S.), University of Alabama at Birmingham; Department of Neurology (L.B.), Medical University of South Carolina, Charleston; Department of Neurology (S.B.), University of California, Los Angeles; and Department of Neurology (J.V.), University of Cincinnati, OH.

Abstract

Background and objectives: Naming decline after left temporal lobe epilepsy (TLE) surgery is common and difficult to predict. Preoperative language fMRI may predict naming decline, but this application is still lacking evidence. We performed a large multicenter cohort study of the effectiveness of fMRI in predicting naming deficits after left TLE surgery.

Methods: At 10 US epilepsy centers, 81 patients with left TLE were prospectively recruited and given the Boston Naming Test (BNT) before and ≈7 months after anterior temporal lobectomy. An fMRI language laterality index (LI) was measured with an auditory semantic decision-tone decision task contrast. Correlations and a multiple regression model were built with a priori chosen predictors.

Results: Naming decline occurred in 56% of patients and correlated with fMRI LI (r = -0.41, p < 0.001), age at epilepsy onset (r = -0.30, p = 0.006), age at surgery (r = -0.23, p = 0.039), and years of education (r = 0.24, p = 0.032). Preoperative BNT score and duration of epilepsy were not correlated with naming decline. The regression model explained 31% of the variance, with fMRI contributing 14%, with a 96% sensitivity and 44% specificity for predicting meaningful naming decline. Cross-validation resulted in an average prediction error of 6 points.

Discussion: An fMRI-based regression model predicted naming outcome after left TLE surgery in a large, prospective multicenter sample, with fMRI as the strongest predictor. These results provide evidence supporting the use of preoperative language fMRI to predict language outcome in patients undergoing left TLE surgery.

Classification of evidence: This study provides Class I evidence that fMRI language lateralization can help in predicting naming decline after left TLE surgery.

Publication types

Multicenter Study
Research Support, N.I.H., Extramural

MeSH terms

Brain Mapping / methods
Cohort Studies
Epilepsy, Temporal Lobe* / diagnostic imaging
Epilepsy, Temporal Lobe* / surgery
Functional Laterality
Humans
Language*
Magnetic Resonance Imaging / methods
Prospective Studies

Abstract

Publication types

MeSH terms

Grants and funding