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June 09, 2015; 84 (23) Article

Seizure localization using ictal phase-locked high gamma

A retrospective surgical outcome study

Shennan A. Weiss, Athena Lemesiou, Robert Connors, Garrett P. Banks, Guy M. McKhann, Robert R. Goodman, Binsheng Zhao, Christopher G. Filippi, Mark Nowell, Roman Rodionov, Beate Diehl, Andrew W. McEvoy, Matthew C. Walker, Andrew J. Trevelyan, Lisa M. Bateman, Ronald G. Emerson, Catherine A. Schevon
First published May 13, 2015, DOI: https://doi.org/10.1212/WNL.0000000000001656
Shennan A. Weiss
From the Departments of Neurology (R.C., L.M.B., R.G.E., C.A.S.), Neurological Surgery (G.P.B., G.M.M., R.R.G.), and Radiology (B.Z., C.G.F.), Columbia University, New York; Hospital for Special Surgery (R.G.E.), Cornell University, New York, NY; Department of Clinical and Experimental Epilepsy (A.L., M.N., R.R., B.D., A.W.M., M.C.W.), Institute of Neurology, University College London; Institute for Neuroscience (A.J.T.), Newcastle University, UK; and Department of Neurology (S.A.W.), UCLA David Geffen School of Medicine, Los Angeles, CA.
MD, PhD
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Athena Lemesiou
From the Departments of Neurology (R.C., L.M.B., R.G.E., C.A.S.), Neurological Surgery (G.P.B., G.M.M., R.R.G.), and Radiology (B.Z., C.G.F.), Columbia University, New York; Hospital for Special Surgery (R.G.E.), Cornell University, New York, NY; Department of Clinical and Experimental Epilepsy (A.L., M.N., R.R., B.D., A.W.M., M.C.W.), Institute of Neurology, University College London; Institute for Neuroscience (A.J.T.), Newcastle University, UK; and Department of Neurology (S.A.W.), UCLA David Geffen School of Medicine, Los Angeles, CA.
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Robert Connors
From the Departments of Neurology (R.C., L.M.B., R.G.E., C.A.S.), Neurological Surgery (G.P.B., G.M.M., R.R.G.), and Radiology (B.Z., C.G.F.), Columbia University, New York; Hospital for Special Surgery (R.G.E.), Cornell University, New York, NY; Department of Clinical and Experimental Epilepsy (A.L., M.N., R.R., B.D., A.W.M., M.C.W.), Institute of Neurology, University College London; Institute for Neuroscience (A.J.T.), Newcastle University, UK; and Department of Neurology (S.A.W.), UCLA David Geffen School of Medicine, Los Angeles, CA.
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Garrett P. Banks
From the Departments of Neurology (R.C., L.M.B., R.G.E., C.A.S.), Neurological Surgery (G.P.B., G.M.M., R.R.G.), and Radiology (B.Z., C.G.F.), Columbia University, New York; Hospital for Special Surgery (R.G.E.), Cornell University, New York, NY; Department of Clinical and Experimental Epilepsy (A.L., M.N., R.R., B.D., A.W.M., M.C.W.), Institute of Neurology, University College London; Institute for Neuroscience (A.J.T.), Newcastle University, UK; and Department of Neurology (S.A.W.), UCLA David Geffen School of Medicine, Los Angeles, CA.
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Guy M. McKhann
From the Departments of Neurology (R.C., L.M.B., R.G.E., C.A.S.), Neurological Surgery (G.P.B., G.M.M., R.R.G.), and Radiology (B.Z., C.G.F.), Columbia University, New York; Hospital for Special Surgery (R.G.E.), Cornell University, New York, NY; Department of Clinical and Experimental Epilepsy (A.L., M.N., R.R., B.D., A.W.M., M.C.W.), Institute of Neurology, University College London; Institute for Neuroscience (A.J.T.), Newcastle University, UK; and Department of Neurology (S.A.W.), UCLA David Geffen School of Medicine, Los Angeles, CA.
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Robert R. Goodman
From the Departments of Neurology (R.C., L.M.B., R.G.E., C.A.S.), Neurological Surgery (G.P.B., G.M.M., R.R.G.), and Radiology (B.Z., C.G.F.), Columbia University, New York; Hospital for Special Surgery (R.G.E.), Cornell University, New York, NY; Department of Clinical and Experimental Epilepsy (A.L., M.N., R.R., B.D., A.W.M., M.C.W.), Institute of Neurology, University College London; Institute for Neuroscience (A.J.T.), Newcastle University, UK; and Department of Neurology (S.A.W.), UCLA David Geffen School of Medicine, Los Angeles, CA.
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Binsheng Zhao
From the Departments of Neurology (R.C., L.M.B., R.G.E., C.A.S.), Neurological Surgery (G.P.B., G.M.M., R.R.G.), and Radiology (B.Z., C.G.F.), Columbia University, New York; Hospital for Special Surgery (R.G.E.), Cornell University, New York, NY; Department of Clinical and Experimental Epilepsy (A.L., M.N., R.R., B.D., A.W.M., M.C.W.), Institute of Neurology, University College London; Institute for Neuroscience (A.J.T.), Newcastle University, UK; and Department of Neurology (S.A.W.), UCLA David Geffen School of Medicine, Los Angeles, CA.
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Christopher G. Filippi
From the Departments of Neurology (R.C., L.M.B., R.G.E., C.A.S.), Neurological Surgery (G.P.B., G.M.M., R.R.G.), and Radiology (B.Z., C.G.F.), Columbia University, New York; Hospital for Special Surgery (R.G.E.), Cornell University, New York, NY; Department of Clinical and Experimental Epilepsy (A.L., M.N., R.R., B.D., A.W.M., M.C.W.), Institute of Neurology, University College London; Institute for Neuroscience (A.J.T.), Newcastle University, UK; and Department of Neurology (S.A.W.), UCLA David Geffen School of Medicine, Los Angeles, CA.
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Mark Nowell
From the Departments of Neurology (R.C., L.M.B., R.G.E., C.A.S.), Neurological Surgery (G.P.B., G.M.M., R.R.G.), and Radiology (B.Z., C.G.F.), Columbia University, New York; Hospital for Special Surgery (R.G.E.), Cornell University, New York, NY; Department of Clinical and Experimental Epilepsy (A.L., M.N., R.R., B.D., A.W.M., M.C.W.), Institute of Neurology, University College London; Institute for Neuroscience (A.J.T.), Newcastle University, UK; and Department of Neurology (S.A.W.), UCLA David Geffen School of Medicine, Los Angeles, CA.
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Roman Rodionov
From the Departments of Neurology (R.C., L.M.B., R.G.E., C.A.S.), Neurological Surgery (G.P.B., G.M.M., R.R.G.), and Radiology (B.Z., C.G.F.), Columbia University, New York; Hospital for Special Surgery (R.G.E.), Cornell University, New York, NY; Department of Clinical and Experimental Epilepsy (A.L., M.N., R.R., B.D., A.W.M., M.C.W.), Institute of Neurology, University College London; Institute for Neuroscience (A.J.T.), Newcastle University, UK; and Department of Neurology (S.A.W.), UCLA David Geffen School of Medicine, Los Angeles, CA.
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Beate Diehl
From the Departments of Neurology (R.C., L.M.B., R.G.E., C.A.S.), Neurological Surgery (G.P.B., G.M.M., R.R.G.), and Radiology (B.Z., C.G.F.), Columbia University, New York; Hospital for Special Surgery (R.G.E.), Cornell University, New York, NY; Department of Clinical and Experimental Epilepsy (A.L., M.N., R.R., B.D., A.W.M., M.C.W.), Institute of Neurology, University College London; Institute for Neuroscience (A.J.T.), Newcastle University, UK; and Department of Neurology (S.A.W.), UCLA David Geffen School of Medicine, Los Angeles, CA.
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Andrew W. McEvoy
From the Departments of Neurology (R.C., L.M.B., R.G.E., C.A.S.), Neurological Surgery (G.P.B., G.M.M., R.R.G.), and Radiology (B.Z., C.G.F.), Columbia University, New York; Hospital for Special Surgery (R.G.E.), Cornell University, New York, NY; Department of Clinical and Experimental Epilepsy (A.L., M.N., R.R., B.D., A.W.M., M.C.W.), Institute of Neurology, University College London; Institute for Neuroscience (A.J.T.), Newcastle University, UK; and Department of Neurology (S.A.W.), UCLA David Geffen School of Medicine, Los Angeles, CA.
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Matthew C. Walker
From the Departments of Neurology (R.C., L.M.B., R.G.E., C.A.S.), Neurological Surgery (G.P.B., G.M.M., R.R.G.), and Radiology (B.Z., C.G.F.), Columbia University, New York; Hospital for Special Surgery (R.G.E.), Cornell University, New York, NY; Department of Clinical and Experimental Epilepsy (A.L., M.N., R.R., B.D., A.W.M., M.C.W.), Institute of Neurology, University College London; Institute for Neuroscience (A.J.T.), Newcastle University, UK; and Department of Neurology (S.A.W.), UCLA David Geffen School of Medicine, Los Angeles, CA.
MB BChir, PhD
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Andrew J. Trevelyan
From the Departments of Neurology (R.C., L.M.B., R.G.E., C.A.S.), Neurological Surgery (G.P.B., G.M.M., R.R.G.), and Radiology (B.Z., C.G.F.), Columbia University, New York; Hospital for Special Surgery (R.G.E.), Cornell University, New York, NY; Department of Clinical and Experimental Epilepsy (A.L., M.N., R.R., B.D., A.W.M., M.C.W.), Institute of Neurology, University College London; Institute for Neuroscience (A.J.T.), Newcastle University, UK; and Department of Neurology (S.A.W.), UCLA David Geffen School of Medicine, Los Angeles, CA.
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Lisa M. Bateman
From the Departments of Neurology (R.C., L.M.B., R.G.E., C.A.S.), Neurological Surgery (G.P.B., G.M.M., R.R.G.), and Radiology (B.Z., C.G.F.), Columbia University, New York; Hospital for Special Surgery (R.G.E.), Cornell University, New York, NY; Department of Clinical and Experimental Epilepsy (A.L., M.N., R.R., B.D., A.W.M., M.C.W.), Institute of Neurology, University College London; Institute for Neuroscience (A.J.T.), Newcastle University, UK; and Department of Neurology (S.A.W.), UCLA David Geffen School of Medicine, Los Angeles, CA.
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Ronald G. Emerson
From the Departments of Neurology (R.C., L.M.B., R.G.E., C.A.S.), Neurological Surgery (G.P.B., G.M.M., R.R.G.), and Radiology (B.Z., C.G.F.), Columbia University, New York; Hospital for Special Surgery (R.G.E.), Cornell University, New York, NY; Department of Clinical and Experimental Epilepsy (A.L., M.N., R.R., B.D., A.W.M., M.C.W.), Institute of Neurology, University College London; Institute for Neuroscience (A.J.T.), Newcastle University, UK; and Department of Neurology (S.A.W.), UCLA David Geffen School of Medicine, Los Angeles, CA.
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Catherine A. Schevon
From the Departments of Neurology (R.C., L.M.B., R.G.E., C.A.S.), Neurological Surgery (G.P.B., G.M.M., R.R.G.), and Radiology (B.Z., C.G.F.), Columbia University, New York; Hospital for Special Surgery (R.G.E.), Cornell University, New York, NY; Department of Clinical and Experimental Epilepsy (A.L., M.N., R.R., B.D., A.W.M., M.C.W.), Institute of Neurology, University College London; Institute for Neuroscience (A.J.T.), Newcastle University, UK; and Department of Neurology (S.A.W.), UCLA David Geffen School of Medicine, Los Angeles, CA.
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Full PDF
Citation
Seizure localization using ictal phase-locked high gamma
A retrospective surgical outcome study
Shennan A. Weiss, Athena Lemesiou, Robert Connors, Garrett P. Banks, Guy M. McKhann, Robert R. Goodman, Binsheng Zhao, Christopher G. Filippi, Mark Nowell, Roman Rodionov, Beate Diehl, Andrew W. McEvoy, Matthew C. Walker, Andrew J. Trevelyan, Lisa M. Bateman, Ronald G. Emerson, Catherine A. Schevon
Neurology Jun 2015, 84 (23) 2320-2328; DOI: 10.1212/WNL.0000000000001656

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Abstract

Objective: To determine whether resection of areas with evidence of intense, synchronized neural firing during seizures is an accurate indicator of postoperative outcome.

Methods: Channels meeting phase-locked high gamma (PLHG) criteria were identified retrospectively from intracranial EEG recordings (102 seizures, 46 implantations, 45 patients). Extent of removal of both the seizure onset zone (SOZ) and PLHG was correlated with seizure outcome, classified as good (Engel class I or II, n = 32) or poor (Engel class III or IV, n = 13).

Results: Patients with good outcomes had significantly greater proportions of both SOZ and the first 4 (early) PLHG sites resected. Improved outcome classification was noted with early PLHG, as measured by the area under the receiver operating characteristic curves (PLHG 0.79, SOZ 0.68) and by odds ratios for resections including at least 75% of sites identified by each measure (PLHG 9.7 [95% CI: 2.3–41.5], SOZ 5.3 [95% CI: 1.2–23.3]). Among patients with resection of at least 75% of the SOZ, 78% (n = 30) had good outcomes, increasing to 91% when the resection also included at least 75% of early PLHG sites (n = 22).

Conclusions: This study demonstrates the localizing value of early PLHG, which is comparable to that provided by the SOZ. Incorporation of PLHG into the clinical evaluation may improve surgical efficacy and help to focus resections on the most critical areas.

GLOSSARY

AUROC=
area under the receiver operating characteristic curve;
CUMC=
Columbia University Medical Center;
NHNN=
National Hospital for Neurology and Neurosurgery;
PLHG=
phase-locked high gamma;
ROC=
receiver operating characteristic;
SOZ=
seizure onset zone

Footnotes

  • Go to Neurology.org for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Supplemental data at Neurology.org

  • Received May 14, 2014.
  • Accepted in final form March 2, 2015.
  • © 2015 American Academy of Neurology
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