Long-term neuropsychological trajectories in children with epilepsy: does surgery halt decline?

IQ academic attainment epilepsy surgery neuropsychology paediatric trajectories

Journal

Brain : a journal of neurology
ISSN: 1460-2156
Titre abrégé: Brain
Pays: England
ID NLM: 0372537

Informations de publication

Date de publication:
20 Apr 2024
Historique:
received: 11 11 2023
revised: 29 02 2024
accepted: 16 03 2024
medline: 21 4 2024
pubmed: 21 4 2024
entrez: 20 4 2024
Statut: aheadofprint

Résumé

Neuropsychological impairments are common in children with drug-resistant epilepsy. It has been proposed that epilepsy surgery may alleviate these impairments by providing seizure freedom; however, findings from prior studies have been inconsistent. We mapped long-term neuropsychological trajectories in children before and after undergoing epilepsy surgery, to measure the impact of disease course and surgery on functioning. We performed a retrospective cohort study of 882 children who had undergone epilepsy surgery at Great Ormond Street Hospital (1990-2018). We extracted patient information and neuropsychological functioning - obtained from IQ tests (domains: Full-Scale IQ, Verbal IQ, Performance IQ, Working Memory, and Processing Speed) and tests of academic attainment (Reading, Spelling and Numeracy) - and investigated changes in functioning using regression analyses. We identified 500 children (248 females) who had undergone epilepsy surgery (median age at surgery = 11.9 years, interquartile range = [7.8,15.0]) and neuropsychology assessment. These children showed declines in all domains of neuropsychological functioning in the time leading up to surgery (all p-values ≤ 0.001; e.g., βFSIQ = -1.9, SEFSIQ = 0.3, pFSIQ < 0.001). Children lost on average one to four points per year, depending on the domain considered; 27-43% declined by 10 or more points from their first to their last preoperative assessment. At the time of presurgical evaluation, most children (46-60%) scored one or more standard deviations below the mean (<85) on the different neuropsychological domains; 37% of these met the threshold for intellectual disability (Full-Scale IQ < 70). On a group level, there was no change in performance from pre- to postoperative assessment on any of the domains (all p-values > 0.128). However, children who became seizure-free through surgery showed higher postoperative neuropsychological performance (e.g., rrb-FSIQ = 0.37, p < 0.001). These children continued to demonstrate improvements in neuropsychological functioning over the course of their long-term follow-up (e.g., βFSIQ = 0.9, SEFSIQ = 0.3, pFSIQ = 0.004). Children who had discontinued antiseizure medication (ASM) treatment at one-year follow-up showed an eight-to-13-point advantage in postoperative Working Memory, Processing Speed, and Numeracy, and greater improvements in Verbal IQ, Working Memory, Reading, and Spelling (all p-values < 0.034) over the postoperative period compared to children who were seizure-free and still receiving ASMs. In conclusion, by providing seizure freedom and the opportunity for ASM cessation, epilepsy surgery may not only halt but reverse the downward trajectory that children with drug-resistant epilepsy display in neuropsychological functioning. To halt this decline as soon as possible, or potentially prevent it from occurring in the first place, children with focal epilepsy should be considered for epilepsy surgery as early as possible after diagnosis.

Identifiants

pubmed: 38643018
pii: 7655555
doi: 10.1093/brain/awae121
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© The Author(s) 2024. Published by Oxford University Press on behalf of the Guarantors of Brain.

Auteurs

Maria H Eriksson (MH)

Developmental Neurosciences Research and Teaching Department, UCL Great Ormond Street Institute of Child Health, London WC1N 1EH, UK.
Department of Neuropsychology, Great Ormond Street Hospital for Children, London WC1N 3JH, UK.
Department of Neurology, Great Ormond Street Hospital for Children, London WC1N 3JH, UK.

Freya Prentice (F)

Developmental Neurosciences Research and Teaching Department, UCL Great Ormond Street Institute of Child Health, London WC1N 1EH, UK.
Department of Neuropsychology, Great Ormond Street Hospital for Children, London WC1N 3JH, UK.

Rory J Piper (RJ)

Developmental Neurosciences Research and Teaching Department, UCL Great Ormond Street Institute of Child Health, London WC1N 1EH, UK.
Department of Neurosurgery, Great Ormond Street Hospital for Children, London WC1N 3JH, UK.

Konrad Wagstyl (K)

Imaging Neuroscience, UCL Queen Square Institute of Neurology, London WC1N 3BG, UK.

Sophie Adler (S)

Developmental Neurosciences Research and Teaching Department, UCL Great Ormond Street Institute of Child Health, London WC1N 1EH, UK.

Aswin Chari (A)

Developmental Neurosciences Research and Teaching Department, UCL Great Ormond Street Institute of Child Health, London WC1N 1EH, UK.
Department of Neurosurgery, Great Ormond Street Hospital for Children, London WC1N 3JH, UK.

John Booth (J)

Digital Research Environment, Great Ormond Street Hospital for Children, London WC1N 3JH, UK.

Friederike Moeller (F)

Department of Neurophysiology, Great Ormond Street Hospital for Children, London WC1N 3JH, UK.

Krishna Das (K)

Department of Neurology, Great Ormond Street Hospital for Children, London WC1N 3JH, UK.
Department of Neurophysiology, Great Ormond Street Hospital for Children, London WC1N 3JH, UK.

Christin Eltze (C)

Department of Neurophysiology, Great Ormond Street Hospital for Children, London WC1N 3JH, UK.

Gerald Cooray (G)

Department of Neurophysiology, Great Ormond Street Hospital for Children, London WC1N 3JH, UK.
Clinical Neuroscience, Karolinska Institutet, Solna 171 77, Sweden.

Ana Perez Caballero (A)

North Thames Genomic Laboratory Hub, Great Ormond Street Hospital for Children, London WC1N 3JH, UK.

Lara Menzies (L)

Department of Clinical Genetics, Great Ormond Street Hospital for Children, London WC1N 3JH, UK.

Amy McTague (A)

Developmental Neurosciences Research and Teaching Department, UCL Great Ormond Street Institute of Child Health, London WC1N 1EH, UK.
Department of Clinical Genetics, Great Ormond Street Hospital for Children, London WC1N 3JH, UK.

Sara Shavel-Jessop (S)

Developmental Neurosciences Research and Teaching Department, UCL Great Ormond Street Institute of Child Health, London WC1N 1EH, UK.
Department of Neuropsychology, Great Ormond Street Hospital for Children, London WC1N 3JH, UK.

Martin M Tisdall (MM)

Developmental Neurosciences Research and Teaching Department, UCL Great Ormond Street Institute of Child Health, London WC1N 1EH, UK.
Department of Neurosurgery, Great Ormond Street Hospital for Children, London WC1N 3JH, UK.

J Helen Cross (JH)

Developmental Neurosciences Research and Teaching Department, UCL Great Ormond Street Institute of Child Health, London WC1N 1EH, UK.
Department of Neurology, Great Ormond Street Hospital for Children, London WC1N 3JH, UK.
Department of Neurosurgery, Great Ormond Street Hospital for Children, London WC1N 3JH, UK.
Young Epilepsy, Lingfield RH7 6PW, UK.

Patricia Martin Sanfilippo (P)

Developmental Neurosciences Research and Teaching Department, UCL Great Ormond Street Institute of Child Health, London WC1N 1EH, UK.
Department of Neuropsychology, Great Ormond Street Hospital for Children, London WC1N 3JH, UK.

Torsten Baldeweg (T)

Developmental Neurosciences Research and Teaching Department, UCL Great Ormond Street Institute of Child Health, London WC1N 1EH, UK.
Department of Neuropsychology, Great Ormond Street Hospital for Children, London WC1N 3JH, UK.

Classifications MeSH