A prospective 5-year longitudinal study detects neurocognitive and imaging correlates of seizure remission in self-limiting Rolandic epilepsy

TY - JOUR

T1 - A prospective 5-year longitudinal study detects neurocognitive and imaging correlates of seizure remission in self-limiting Rolandic epilepsy

AU - Smith, Stuart D. W.

AU - Mcginnity, Colm J.

AU - Smith, Anna B.

AU - Barker, Gareth J.

AU - Richardson, Mark P.

AU - Pal, Deb K.

N1 - Funding Information: None of the authors has any conflict of interest to disclose. We confirm that we have read the Journal's position on issues involved in ethical publication and affirm that this report is consistent with those guidelines. We want to thank all the families involved with the study and the Waterloo Foundation for funding the research. We would also like to thank the teams at the Centre for Neuroimaging at IoPPN and Kings College Hospital CRF. This work was supported by the European Union Program of the Seventh Framework : Development of Strategies for Innovative Research to Improve Diagnosis, Prevention and Treatment in Children With Difficult to Treat Epilepsy, “DESIRE” ( 602531 , (DKP.)); UK Medical Research Council, Centre for Neurodevelopmental Disorders ( MR/N026063/1 (DKP, MPR.)); UK Medical Research Council, Programme grant ( MR/K013998/1 , MRP.); a Waterloo Foundation Project Grants ( 164‐3020 (DKP.) and 164-2358 (DKP/SDWS)); the Charles Sykes Epilepsy Research Trust (DKP.); NIHR Specialist Biomedical Research Centre for Mental Health of South London and Maudsley National Health Service Foundation Trust (DKP, MPR). Funding Information: None of the authors has any conflict of interest to disclose. We confirm that we have read the Journal's position on issues involved in ethical publication and affirm that this report is consistent with those guidelines. We want to thank all the families involved with the study and the Waterloo Foundation for funding the research. We would also like to thank the teams at the Centre for Neuroimaging at IoPPN and Kings College Hospital CRF. This work was supported by the European Union Program of the Seventh Framework: Development of Strategies for Innovative Research to Improve Diagnosis, Prevention and Treatment in Children With Difficult to Treat Epilepsy, “DESIRE” (602531, (DKP.)); UK Medical Research Council, Centre for Neurodevelopmental Disorders (MR/N026063/1 (DKP, MPR.)); UK Medical Research Council, Programme grant (MR/K013998/1, MRP.); a Waterloo Foundation Project Grants (164‐3020 (DKP.) and 164-2358 (DKP/SDWS)); the Charles Sykes Epilepsy Research Trust (DKP.); NIHR Specialist Biomedical Research Centre for Mental Health of South London and Maudsley National Health Service Foundation Trust (DKP, MPR). Publisher Copyright: © 2023 The Author(s)

PY - 2023/10/1

Y1 - 2023/10/1

N2 - ObjectiveSelf-limiting Rolandic epilepsy (RE) is the most common epilepsy in school-age children. Seizures are generally infrequent, but cognitive, language, and motor coordination problems can significantly impact the child’s life. To better understand brain structure and function changes in RE, we longitudinally assessed neurocognition, cortical thickness, and subcortical volumes.MethodsAt baseline, we recruited 30 participants diagnosed with RE and 24-healthy controls and followed up for 4.94 ± 0.8 years when the participants with RE were in seizure remission. Measures included were as follows: T1-weighted magnetic resonance brain imaging (MRI) with FreeSurfer analysis and detailed neuropsychological assessments. MRI and neuropsychological data were compared between baseline and follow-up in seizure remission.ResultsLongitudinal MRI revealed excess cortical thinning in the left-orbitofrontal (p = 0.0001) and pre-central gyrus (p = 0.044).There is a significant association (p = 0.003) between a reduction in cortical thickness in the left-orbitofrontal cluster and improved processing of filtered words.Longitudinal neuropsychology revealed significant improvements in the symptoms of developmental coordination disorder (DCD, p = 0.005) in seizure remission.ConclusionsThere is evidence for altered development of neocortical regions between active seizure state and seizure remission in RE within two clusters maximal in the left-orbitofrontal and pre-central gyrus. There is significant evidence for improvement in motor coordination between active seizures and seizure remission and suggestive evidence for a decline in fluid intelligence and gains in auditory processing.

AB - ObjectiveSelf-limiting Rolandic epilepsy (RE) is the most common epilepsy in school-age children. Seizures are generally infrequent, but cognitive, language, and motor coordination problems can significantly impact the child’s life. To better understand brain structure and function changes in RE, we longitudinally assessed neurocognition, cortical thickness, and subcortical volumes.MethodsAt baseline, we recruited 30 participants diagnosed with RE and 24-healthy controls and followed up for 4.94 ± 0.8 years when the participants with RE were in seizure remission. Measures included were as follows: T1-weighted magnetic resonance brain imaging (MRI) with FreeSurfer analysis and detailed neuropsychological assessments. MRI and neuropsychological data were compared between baseline and follow-up in seizure remission.ResultsLongitudinal MRI revealed excess cortical thinning in the left-orbitofrontal (p = 0.0001) and pre-central gyrus (p = 0.044).There is a significant association (p = 0.003) between a reduction in cortical thickness in the left-orbitofrontal cluster and improved processing of filtered words.Longitudinal neuropsychology revealed significant improvements in the symptoms of developmental coordination disorder (DCD, p = 0.005) in seizure remission.ConclusionsThere is evidence for altered development of neocortical regions between active seizure state and seizure remission in RE within two clusters maximal in the left-orbitofrontal and pre-central gyrus. There is significant evidence for improvement in motor coordination between active seizures and seizure remission and suggestive evidence for a decline in fluid intelligence and gains in auditory processing.

UR - http://www.scopus.com/inward/record.url?scp=85168578135&partnerID=8YFLogxK

U2 - 10.1016/j.yebeh.2023.109397

DO - 10.1016/j.yebeh.2023.109397

M3 - Article

SN - 1525-5050

VL - 147

JO - Epilepsy & Behavior

JF - Epilepsy & Behavior

M1 - 109397

ER -