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July 13, 2021; 97 (2) Research Article

One-Stage, Limited-Resection Epilepsy Surgery for Bottom-of-Sulcus Dysplasia

View ORCID ProfileEmma Macdonald-Laurs, Wirginia J. Maixner, Catherine A. Bailey, Sarah M. Barton, Simone A. Mandelstam, View ORCID ProfileJoseph Yuan-Mou Yang, Aaron E.L. Warren, Michael J. Kean, Peter Francis, Duncan MacGregor, Colleen D'Arcy, Jacquie A. Wrennall, Andrew Davidson, Kate Pope, Richard J. Leventer, Jeremy L. Freeman, Alison Wray, Graeme D. Jackson, View ORCID ProfileA. Simon Harvey
First published May 4, 2021, DOI: https://doi.org/10.1212/WNL.0000000000012147
Emma Macdonald-Laurs
From the Departments of Neurology (E.M.-L., C.A.B., S.M.B., R.J.L., J.L.F., A.S.H.), Neurosurgery (W.J.M., J.Y.-M.Y., A.E.L.W., A.W.), Medical Imaging (S.A.M., M.J.K., P.F.), Anatomical Pathology (D.M., C.D.), Psychology (J.A.W.), and Anaesthesia (A.D.), The Royal Children's Hospital; Murdoch Children's Research Institute (E.M.-L., W.J.M., S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., C.D., A.D., K.P., R.J.L., A.W., A.S.H.); University of Melbourne (E.M.-L., W.J.M, S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., M.J.K., C.D., A.D., R.J.L., A.S.H.); and Florey Institute of Neuroscience and Mental Health (A.E.L.W., G.D.J., A.S.H.), Parkville, Victoria, Australia.
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Wirginia J. Maixner
From the Departments of Neurology (E.M.-L., C.A.B., S.M.B., R.J.L., J.L.F., A.S.H.), Neurosurgery (W.J.M., J.Y.-M.Y., A.E.L.W., A.W.), Medical Imaging (S.A.M., M.J.K., P.F.), Anatomical Pathology (D.M., C.D.), Psychology (J.A.W.), and Anaesthesia (A.D.), The Royal Children's Hospital; Murdoch Children's Research Institute (E.M.-L., W.J.M., S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., C.D., A.D., K.P., R.J.L., A.W., A.S.H.); University of Melbourne (E.M.-L., W.J.M, S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., M.J.K., C.D., A.D., R.J.L., A.S.H.); and Florey Institute of Neuroscience and Mental Health (A.E.L.W., G.D.J., A.S.H.), Parkville, Victoria, Australia.
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Catherine A. Bailey
From the Departments of Neurology (E.M.-L., C.A.B., S.M.B., R.J.L., J.L.F., A.S.H.), Neurosurgery (W.J.M., J.Y.-M.Y., A.E.L.W., A.W.), Medical Imaging (S.A.M., M.J.K., P.F.), Anatomical Pathology (D.M., C.D.), Psychology (J.A.W.), and Anaesthesia (A.D.), The Royal Children's Hospital; Murdoch Children's Research Institute (E.M.-L., W.J.M., S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., C.D., A.D., K.P., R.J.L., A.W., A.S.H.); University of Melbourne (E.M.-L., W.J.M, S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., M.J.K., C.D., A.D., R.J.L., A.S.H.); and Florey Institute of Neuroscience and Mental Health (A.E.L.W., G.D.J., A.S.H.), Parkville, Victoria, Australia.
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Sarah M. Barton
From the Departments of Neurology (E.M.-L., C.A.B., S.M.B., R.J.L., J.L.F., A.S.H.), Neurosurgery (W.J.M., J.Y.-M.Y., A.E.L.W., A.W.), Medical Imaging (S.A.M., M.J.K., P.F.), Anatomical Pathology (D.M., C.D.), Psychology (J.A.W.), and Anaesthesia (A.D.), The Royal Children's Hospital; Murdoch Children's Research Institute (E.M.-L., W.J.M., S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., C.D., A.D., K.P., R.J.L., A.W., A.S.H.); University of Melbourne (E.M.-L., W.J.M, S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., M.J.K., C.D., A.D., R.J.L., A.S.H.); and Florey Institute of Neuroscience and Mental Health (A.E.L.W., G.D.J., A.S.H.), Parkville, Victoria, Australia.
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Simone A. Mandelstam
From the Departments of Neurology (E.M.-L., C.A.B., S.M.B., R.J.L., J.L.F., A.S.H.), Neurosurgery (W.J.M., J.Y.-M.Y., A.E.L.W., A.W.), Medical Imaging (S.A.M., M.J.K., P.F.), Anatomical Pathology (D.M., C.D.), Psychology (J.A.W.), and Anaesthesia (A.D.), The Royal Children's Hospital; Murdoch Children's Research Institute (E.M.-L., W.J.M., S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., C.D., A.D., K.P., R.J.L., A.W., A.S.H.); University of Melbourne (E.M.-L., W.J.M, S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., M.J.K., C.D., A.D., R.J.L., A.S.H.); and Florey Institute of Neuroscience and Mental Health (A.E.L.W., G.D.J., A.S.H.), Parkville, Victoria, Australia.
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Joseph Yuan-Mou Yang
From the Departments of Neurology (E.M.-L., C.A.B., S.M.B., R.J.L., J.L.F., A.S.H.), Neurosurgery (W.J.M., J.Y.-M.Y., A.E.L.W., A.W.), Medical Imaging (S.A.M., M.J.K., P.F.), Anatomical Pathology (D.M., C.D.), Psychology (J.A.W.), and Anaesthesia (A.D.), The Royal Children's Hospital; Murdoch Children's Research Institute (E.M.-L., W.J.M., S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., C.D., A.D., K.P., R.J.L., A.W., A.S.H.); University of Melbourne (E.M.-L., W.J.M, S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., M.J.K., C.D., A.D., R.J.L., A.S.H.); and Florey Institute of Neuroscience and Mental Health (A.E.L.W., G.D.J., A.S.H.), Parkville, Victoria, Australia.
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Aaron E.L. Warren
From the Departments of Neurology (E.M.-L., C.A.B., S.M.B., R.J.L., J.L.F., A.S.H.), Neurosurgery (W.J.M., J.Y.-M.Y., A.E.L.W., A.W.), Medical Imaging (S.A.M., M.J.K., P.F.), Anatomical Pathology (D.M., C.D.), Psychology (J.A.W.), and Anaesthesia (A.D.), The Royal Children's Hospital; Murdoch Children's Research Institute (E.M.-L., W.J.M., S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., C.D., A.D., K.P., R.J.L., A.W., A.S.H.); University of Melbourne (E.M.-L., W.J.M, S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., M.J.K., C.D., A.D., R.J.L., A.S.H.); and Florey Institute of Neuroscience and Mental Health (A.E.L.W., G.D.J., A.S.H.), Parkville, Victoria, Australia.
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Michael J. Kean
From the Departments of Neurology (E.M.-L., C.A.B., S.M.B., R.J.L., J.L.F., A.S.H.), Neurosurgery (W.J.M., J.Y.-M.Y., A.E.L.W., A.W.), Medical Imaging (S.A.M., M.J.K., P.F.), Anatomical Pathology (D.M., C.D.), Psychology (J.A.W.), and Anaesthesia (A.D.), The Royal Children's Hospital; Murdoch Children's Research Institute (E.M.-L., W.J.M., S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., C.D., A.D., K.P., R.J.L., A.W., A.S.H.); University of Melbourne (E.M.-L., W.J.M, S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., M.J.K., C.D., A.D., R.J.L., A.S.H.); and Florey Institute of Neuroscience and Mental Health (A.E.L.W., G.D.J., A.S.H.), Parkville, Victoria, Australia.
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Peter Francis
From the Departments of Neurology (E.M.-L., C.A.B., S.M.B., R.J.L., J.L.F., A.S.H.), Neurosurgery (W.J.M., J.Y.-M.Y., A.E.L.W., A.W.), Medical Imaging (S.A.M., M.J.K., P.F.), Anatomical Pathology (D.M., C.D.), Psychology (J.A.W.), and Anaesthesia (A.D.), The Royal Children's Hospital; Murdoch Children's Research Institute (E.M.-L., W.J.M., S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., C.D., A.D., K.P., R.J.L., A.W., A.S.H.); University of Melbourne (E.M.-L., W.J.M, S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., M.J.K., C.D., A.D., R.J.L., A.S.H.); and Florey Institute of Neuroscience and Mental Health (A.E.L.W., G.D.J., A.S.H.), Parkville, Victoria, Australia.
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Duncan MacGregor
From the Departments of Neurology (E.M.-L., C.A.B., S.M.B., R.J.L., J.L.F., A.S.H.), Neurosurgery (W.J.M., J.Y.-M.Y., A.E.L.W., A.W.), Medical Imaging (S.A.M., M.J.K., P.F.), Anatomical Pathology (D.M., C.D.), Psychology (J.A.W.), and Anaesthesia (A.D.), The Royal Children's Hospital; Murdoch Children's Research Institute (E.M.-L., W.J.M., S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., C.D., A.D., K.P., R.J.L., A.W., A.S.H.); University of Melbourne (E.M.-L., W.J.M, S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., M.J.K., C.D., A.D., R.J.L., A.S.H.); and Florey Institute of Neuroscience and Mental Health (A.E.L.W., G.D.J., A.S.H.), Parkville, Victoria, Australia.
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Colleen D'Arcy
From the Departments of Neurology (E.M.-L., C.A.B., S.M.B., R.J.L., J.L.F., A.S.H.), Neurosurgery (W.J.M., J.Y.-M.Y., A.E.L.W., A.W.), Medical Imaging (S.A.M., M.J.K., P.F.), Anatomical Pathology (D.M., C.D.), Psychology (J.A.W.), and Anaesthesia (A.D.), The Royal Children's Hospital; Murdoch Children's Research Institute (E.M.-L., W.J.M., S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., C.D., A.D., K.P., R.J.L., A.W., A.S.H.); University of Melbourne (E.M.-L., W.J.M, S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., M.J.K., C.D., A.D., R.J.L., A.S.H.); and Florey Institute of Neuroscience and Mental Health (A.E.L.W., G.D.J., A.S.H.), Parkville, Victoria, Australia.
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Jacquie A. Wrennall
From the Departments of Neurology (E.M.-L., C.A.B., S.M.B., R.J.L., J.L.F., A.S.H.), Neurosurgery (W.J.M., J.Y.-M.Y., A.E.L.W., A.W.), Medical Imaging (S.A.M., M.J.K., P.F.), Anatomical Pathology (D.M., C.D.), Psychology (J.A.W.), and Anaesthesia (A.D.), The Royal Children's Hospital; Murdoch Children's Research Institute (E.M.-L., W.J.M., S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., C.D., A.D., K.P., R.J.L., A.W., A.S.H.); University of Melbourne (E.M.-L., W.J.M, S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., M.J.K., C.D., A.D., R.J.L., A.S.H.); and Florey Institute of Neuroscience and Mental Health (A.E.L.W., G.D.J., A.S.H.), Parkville, Victoria, Australia.
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Andrew Davidson
From the Departments of Neurology (E.M.-L., C.A.B., S.M.B., R.J.L., J.L.F., A.S.H.), Neurosurgery (W.J.M., J.Y.-M.Y., A.E.L.W., A.W.), Medical Imaging (S.A.M., M.J.K., P.F.), Anatomical Pathology (D.M., C.D.), Psychology (J.A.W.), and Anaesthesia (A.D.), The Royal Children's Hospital; Murdoch Children's Research Institute (E.M.-L., W.J.M., S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., C.D., A.D., K.P., R.J.L., A.W., A.S.H.); University of Melbourne (E.M.-L., W.J.M, S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., M.J.K., C.D., A.D., R.J.L., A.S.H.); and Florey Institute of Neuroscience and Mental Health (A.E.L.W., G.D.J., A.S.H.), Parkville, Victoria, Australia.
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Kate Pope
From the Departments of Neurology (E.M.-L., C.A.B., S.M.B., R.J.L., J.L.F., A.S.H.), Neurosurgery (W.J.M., J.Y.-M.Y., A.E.L.W., A.W.), Medical Imaging (S.A.M., M.J.K., P.F.), Anatomical Pathology (D.M., C.D.), Psychology (J.A.W.), and Anaesthesia (A.D.), The Royal Children's Hospital; Murdoch Children's Research Institute (E.M.-L., W.J.M., S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., C.D., A.D., K.P., R.J.L., A.W., A.S.H.); University of Melbourne (E.M.-L., W.J.M, S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., M.J.K., C.D., A.D., R.J.L., A.S.H.); and Florey Institute of Neuroscience and Mental Health (A.E.L.W., G.D.J., A.S.H.), Parkville, Victoria, Australia.
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Richard J. Leventer
From the Departments of Neurology (E.M.-L., C.A.B., S.M.B., R.J.L., J.L.F., A.S.H.), Neurosurgery (W.J.M., J.Y.-M.Y., A.E.L.W., A.W.), Medical Imaging (S.A.M., M.J.K., P.F.), Anatomical Pathology (D.M., C.D.), Psychology (J.A.W.), and Anaesthesia (A.D.), The Royal Children's Hospital; Murdoch Children's Research Institute (E.M.-L., W.J.M., S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., C.D., A.D., K.P., R.J.L., A.W., A.S.H.); University of Melbourne (E.M.-L., W.J.M, S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., M.J.K., C.D., A.D., R.J.L., A.S.H.); and Florey Institute of Neuroscience and Mental Health (A.E.L.W., G.D.J., A.S.H.), Parkville, Victoria, Australia.
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Jeremy L. Freeman
From the Departments of Neurology (E.M.-L., C.A.B., S.M.B., R.J.L., J.L.F., A.S.H.), Neurosurgery (W.J.M., J.Y.-M.Y., A.E.L.W., A.W.), Medical Imaging (S.A.M., M.J.K., P.F.), Anatomical Pathology (D.M., C.D.), Psychology (J.A.W.), and Anaesthesia (A.D.), The Royal Children's Hospital; Murdoch Children's Research Institute (E.M.-L., W.J.M., S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., C.D., A.D., K.P., R.J.L., A.W., A.S.H.); University of Melbourne (E.M.-L., W.J.M, S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., M.J.K., C.D., A.D., R.J.L., A.S.H.); and Florey Institute of Neuroscience and Mental Health (A.E.L.W., G.D.J., A.S.H.), Parkville, Victoria, Australia.
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Alison Wray
From the Departments of Neurology (E.M.-L., C.A.B., S.M.B., R.J.L., J.L.F., A.S.H.), Neurosurgery (W.J.M., J.Y.-M.Y., A.E.L.W., A.W.), Medical Imaging (S.A.M., M.J.K., P.F.), Anatomical Pathology (D.M., C.D.), Psychology (J.A.W.), and Anaesthesia (A.D.), The Royal Children's Hospital; Murdoch Children's Research Institute (E.M.-L., W.J.M., S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., C.D., A.D., K.P., R.J.L., A.W., A.S.H.); University of Melbourne (E.M.-L., W.J.M, S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., M.J.K., C.D., A.D., R.J.L., A.S.H.); and Florey Institute of Neuroscience and Mental Health (A.E.L.W., G.D.J., A.S.H.), Parkville, Victoria, Australia.
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Graeme D. Jackson
From the Departments of Neurology (E.M.-L., C.A.B., S.M.B., R.J.L., J.L.F., A.S.H.), Neurosurgery (W.J.M., J.Y.-M.Y., A.E.L.W., A.W.), Medical Imaging (S.A.M., M.J.K., P.F.), Anatomical Pathology (D.M., C.D.), Psychology (J.A.W.), and Anaesthesia (A.D.), The Royal Children's Hospital; Murdoch Children's Research Institute (E.M.-L., W.J.M., S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., C.D., A.D., K.P., R.J.L., A.W., A.S.H.); University of Melbourne (E.M.-L., W.J.M, S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., M.J.K., C.D., A.D., R.J.L., A.S.H.); and Florey Institute of Neuroscience and Mental Health (A.E.L.W., G.D.J., A.S.H.), Parkville, Victoria, Australia.
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A. Simon Harvey
From the Departments of Neurology (E.M.-L., C.A.B., S.M.B., R.J.L., J.L.F., A.S.H.), Neurosurgery (W.J.M., J.Y.-M.Y., A.E.L.W., A.W.), Medical Imaging (S.A.M., M.J.K., P.F.), Anatomical Pathology (D.M., C.D.), Psychology (J.A.W.), and Anaesthesia (A.D.), The Royal Children's Hospital; Murdoch Children's Research Institute (E.M.-L., W.J.M., S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., C.D., A.D., K.P., R.J.L., A.W., A.S.H.); University of Melbourne (E.M.-L., W.J.M, S.M.B., S.A.M., J.Y.-M.Y., A.E.L.W., M.J.K., C.D., A.D., R.J.L., A.S.H.); and Florey Institute of Neuroscience and Mental Health (A.E.L.W., G.D.J., A.S.H.), Parkville, Victoria, Australia.
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One-Stage, Limited-Resection Epilepsy Surgery for Bottom-of-Sulcus Dysplasia
Emma Macdonald-Laurs, Wirginia J. Maixner, Catherine A. Bailey, Sarah M. Barton, Simone A. Mandelstam, Joseph Yuan-Mou Yang, Aaron E.L. Warren, Michael J. Kean, Peter Francis, Duncan MacGregor, Colleen D'Arcy, Jacquie A. Wrennall, Andrew Davidson, Kate Pope, Richard J. Leventer, Jeremy L. Freeman, Alison Wray, Graeme D. Jackson, A. Simon Harvey
Neurology Jul 2021, 97 (2) e178-e190; DOI: 10.1212/WNL.0000000000012147

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Abstract

Objective To determine whether 1-stage, limited corticectomy controls seizures in patients with MRI-positive, bottom-of-sulcus dysplasia (BOSD).

Methods We reviewed clinical, neuroimaging, electrocorticography (ECoG), operative, and histopathology findings in consecutively operated patients with drug-resistant focal epilepsy and MRI-positive BOSD, all of whom underwent corticectomy guided by MRI and ECoG.

Results Thirty-eight patients with a median age at surgery of 10.2 (interquartile range [IQR] 6.0–14.1) years were included. BOSDs involved eloquent cortex in 15 patients. Eighty-seven percent of patients had rhythmic spiking on preresection ECoG. Rhythmic spiking was present in 22 of 24 patients studied with combined depth and surface electrodes, being limited to the dysplastic sulcus in 7 and involving the dysplastic sulcus and gyral crown in 15. Sixty-eight percent of resections were limited to the dysplastic sulcus, leaving the gyral crown. Histopathology was focal cortical dysplasia (FCD) type IIb in 29 patients and FCDIIa in 9. Dysmorphic neurons were present in the bottom of the sulcus but not the top or the gyral crown in 17 of 22 patients. Six (16%) patients required reoperation for postoperative seizures and residual dysplasia; reoperation was not correlated with ECoG, neuroimaging, or histologic abnormalities in the gyral crown. At a median 6.3 (IQR 4.8–9.9) years of follow-up, 33 (87%) patients are seizure-free, 31 off antiseizure medication.

Conclusion BOSD can be safely and effectively resected with MRI and ECoG guidance, corticectomy potentially being limited to the dysplastic sulcus, without need for intracranial EEG monitoring and functional mapping.

Classification of Evidence This study provides Class IV evidence that 1-stage, limited corticectomy for BOSD is safe and effective for control of seizures.

Glossary

ASM=
antiseizure medication;
BOSD=
bottom-of-sulcus dysplasia;
ECoG=
electrocorticography;
FCD=
focal cortical dysplasia;
FDG=
fluorodeoxyglucose;
FLAIR=
fluid-attenuated inversion recovery;
FR=
fast ripples;
IED=
interictal epileptiform discharge;
IQR=
interquartile range;
RBD=
repetitive bursting discharges;
3D=
3-dimensional

Footnotes

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

  • Class of Evidence: NPub.org/coe

  • Received November 7, 2020.
  • Accepted in final form March 31, 2021.
  • © 2021 American Academy of Neurology
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Letters: Rapid online correspondence

  • Author Response: One-Stage, Limited-Resection Epilepsy Surgery for Bottom-of-Sulcus Dysplasia
    • A. Simon Harvey, Epileptologist, Royal Children's Hospital, Melbourne
    • Emma Macdonald-Laurs, Epileptologist, Royal Children's Hospital
    Submitted September 02, 2021
  • Reader Response: One-Stage, Limited-Resection Epilepsy Surgery for Bottom-of-Sulcus Dysplasia
    • Wenhan Hu, Neurosurgeon, Beijing Neurosurgical Institute; Beijing Tiantan Hospital, Capital Medical University
    • Baotian Zhao, Neurosurgeon, Beijing Tiantan Hospital, Capital Medical University
    • Jianguo Zhang, Neurosurgeon, Beijing Neurosurgical Institute; Beijing Tiantan Hospital, Capital Medical University
    • Kai Zhang, Neurosurgeon, Beijing Neurosurgical Institute; Beijing Tiantan Hospital, Capital Medical University
    Submitted July 15, 2021
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