Determinants of Functional Outcome after Pediatric Hemispherotomy.
Journal
Annals of neurology
ISSN: 1531-8249
Titre abrégé: Ann Neurol
Pays: United States
ID NLM: 7707449
Informations de publication
Date de publication:
14 Nov 2023
14 Nov 2023
Historique:
revised:
04
10
2023
received:
19
04
2023
accepted:
23
10
2023
pubmed:
14
11
2023
medline:
14
11
2023
entrez:
14
11
2023
Statut:
aheadofprint
Résumé
We aimed to evaluate determinants of functional outcome after pediatric hemispherotomy in a large and recent multicenter cohort. We retrospectively investigated the functional outcomes of 455 children who underwent hemispherotomy at 5 epilepsy centers in 2000-2016. We identified determinants of unaided walking, voluntary grasping with the hemiplegic hand, and speaking through Bayesian multivariable regression modeling using missing data imputation. Seventy-five percent of children were seizure-free, and 44% stopped antiseizure medication at a 5.1-year mean follow-up (range = 1-17.1). Seventy-seven percent of children could walk unaided, 8% could grasp voluntarily, and 68% could speak at the last follow-up. Children were unlikely to walk when they had contralateral magnetic resonance imaging (MRI) abnormalities (40/73, p = 0.04), recurrent seizures following hemispherotomy (62/109, p = 0.04), and moderately (50/61, p = 0.03) or severely impaired (127/199, p = 0.001) postsurgical intellectual functioning, but were likely to walk when they were older at outcome determination (p = 0.01). Children were unlikely to grasp voluntarily with the hand contralateral to surgery when they had Rasmussen encephalitis (0/61, p = 0.001) or Sturge-Weber syndrome (0/32, p = 0.007). Children were unlikely to speak when they had contralateral MRI abnormalities (30/69, p = 0.002) and longer epilepsy duration (p = 0.01), but likely to speak when they had Sturge-Weber syndrome (29/35, p = 0.01), were older at surgery (p = 0.04), and were older at outcome determination (p < 0.001). Etiology and bilaterality of structural brain abnormalities were key determinants of functional outcome after hemispherotomy. Longer epilepsy duration affected language outcomes. Not surprisingly, walking and talking ability increased with older age at outcome evaluation. ANN NEUROL 2023.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Anna Muller Grocholski Foundation
Organisme : Deutsche Forschungsgemeinschaft
ID : NE 1383/9-1
Organisme : Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
ID : 208184
Informations de copyright
© 2023 American Neurological Association.
Références
Ramantani G, Kadish NE, Brandt A, et al. Seizure control and developmental trajectories after hemispherotomy for refractory epilepsy in childhood and adolescence. Epilepsia 2013;54:1046-1055.
Boshuisen K, van Schooneveld MMJ, Leijten FSS, et al. Contralateral MRI abnormalities affect seizure and cognitive outcome after hemispherectomy. Neurology 2010;75:1623-1630.
Delalande O, Bulteau C, Dellatolas G, et al. Vertical parasagittal hemispherotomy: surgical procedures and clinical long-term outcomes in a population of 83 children. Neurosurgery 2007;60:ONS19-ONS32.
Moosa ANV, Gupta A, Jehi L, et al. Longitudinal seizure outcome and prognostic predictors after hemispherectomy in 170 children. Neurology 2013;80:253-260.
Schramm J, Kuczaty S, Sassen R, et al. Pediatric functional hemispherectomy: outcome in 92 patients. Acta Neurochir 2012;154:2017-2028.
Ramantani G, Bulteau C, Cserpan D, et al. Not surgical technique, but etiology, contralateral MRI, prior surgery, and side of surgery determine seizure outcome after pediatric hemispherotomy. Epilepsia 2023;64:1214-1224.
Honda R, Kaido T, Sugai K, et al. Long-term developmental outcome after early hemispherotomy for hemimegalencephaly in infants with epileptic encephalopathy. Epilepsy Behav 2013;29:30-35.
Kadish NE, Bast T, Reuner G, et al. Epilepsy surgery in the first 3 years of life: predictors of seizure freedom and cognitive development. Neurosurgery 2019;84:E368-E377.
Ramantani G, Kadish NE, Strobl K, et al. Seizure and cognitive outcomes of epilepsy surgery in infancy and early childhood. Eur J Paediatr Neurol 2013;17:498-506.
Ramantani G, Strobl K, Stathi A, et al. Reoperation for refractory epilepsy in childhood: a second chance for selected patients. Neurosurgery 2013;73:695-704.
Cossu M, Nichelatti M, De Benedictis A, Rizzi M. Lateral versus vertical hemispheric disconnection for epilepsy: a systematic review and meta-analysis. J Neurosurg 2021;136:1627-1637.
Moosa ANV, Jehi L, Marashly A, et al. Long-term functional outcomes and their predictors after hemispherectomy in 115 children. Epilepsia 2013;54:1771-1779.
Devlin AM, Cross JH, Harkness W, et al. Clinical outcomes of hemispherectomy for epilepsy in childhood and adolescence. Brain 2003;126:556-566.
Pulsifer MB, Brandt J, Salorio CF, et al. The cognitive outcome of hemispherectomy in 71 children. Epilepsia 2004;45:243-254.
Verdinelli C, Olsson I, Edelvik A, et al. A long-term patient perspective after hemispherotomy - a population based study. Seizure 2015;30:76-82.
Jonas R, Nguyen S, Hu B, et al. Cerebral hemispherectomy: hospital course, seizure, developmental, language, and motor outcomes. Neurology 2004;62:1712-1721.
Rados M, Mouthaan B, Barsi P, et al. Diagnostic value of MRI in the presurgical evaluation of patients with epilepsy: influence of field strength and sequence selection: a systematic review and meta-analysis from the E-PILEPSY consortium. Epileptic Disord 2022;24:323-342.
Gaillard WD, Chiron C, Cross JH, et al. Guidelines for imaging infants and children with recent-onset epilepsy. Epilepsia 2009;50:2147-2153.
Spitzer H, Ripart M, Whitaker K, et al. Interpretable surface-based detection of focal cortical dysplasias: a multi-Centre epilepsy lesion detection study. Brain 2022;145:3859-3871.
van Schooneveld MMJ, Braun KPJ, van Rijen PC, et al. The spectrum of long-term cognitive and functional outcome after hemispherectomy in childhood. Eur J Paediatr Neurol 2016;20:376-384.
Cats EA, Kho KH, Van Nieuwenhuizen O, et al. Seizure freedom after functional hemispherectomy and a possible role for the insular cortex: the Dutch experience. J Neurosurg 2007;107:275-280.
Griessenauer CJ, Salam S, Hendrix P, et al. Hemispherectomy for treatment of refractory epilepsy in the pediatric age group: a systematic review. J Neurosurg Pediatr 2015;15:34-44.
Weil AG, Lewis EC, Ibrahim GM, et al. Hemispherectomy outcome prediction scale: development and validation of a seizure freedom prediction tool. Epilepsia 2021;62:1064-1073.
Fallah A, Lewis E, Ibrahim GM, et al. Comparison of the real-world effectiveness of vertical versus lateral functional hemispherotomy techniques for pediatric drug-resistant epilepsy: a post hoc analysis of the HOPS study. Epilepsia 2021;62:2707-2718.
van Schooneveld MMJ, Jennekens-Schinkel A, van Rijen PC, et al. Hemispherectomy: a basis for mental development in children with epilepsy. Epileptic Disord 2011;13:47-55.
Weil AG, Dimentberg E, Lewis E, et al. Development of an online calculator for the prediction of seizure freedom following pediatric hemispherectomy using HOPS. Epilepsia 2023;00:1-11.
Bjellvi J, Flink R, Rydenhag B, Malmgren K. Complications of epilepsy surgery in Sweden 1996-2010: a prospective, population-based study. J Neurosurg 2015;122:519-525.
Engel J Jr, Van Ness PC, Rasmussen TB, Ojemann LM. Outcome with respect to epileptic seizures. In: Engel J Jr, ed. Surgical treatment of the epilepsies. New York: Raven Press, 1993:609-621.
van Buuren S, Groothuis-Oudshoorn K. Mice: multivariate imputation by chained equations in R. J Stat Softw 2011;45:1-67.
Gelman A, Jakulin A, Pittau MG, Su Y-S. A weakly informative default prior distribution for logistic and other regression models. The Annals of Applied Statistics 2008;2:1360-1383.
Bürkner P-C. Bayesian item response modeling in R with brms and Stan. J Stat Softw 2021;100:1-54.
R Core Team. R: The R Project for Statistical Computing [Internet], 2022. Available from: https://www.r-project.org/.
RStudio Team. RStudio: Integrated Development for R. [Internet], 2020. Available from: http://www.rstudio.com/.
Ramantani G. Epilepsy surgery in early life: the earlier. The Better World Neurosurgery 2019;131:285-286.
Kogias E, Bast T, Schubert-Bast S, et al. Multilobar epilepsy surgery in childhood and adolescence: predictors of long-term seizure freedom. Neurosurgery 2021;88:174-182.
Sebastianelli L, Versace V, Taylor A, et al. Functional reorganization after hemispherectomy in humans and animal models: what can we learn about the brain's resilience to extensive unilateral lesions? Brain Res Bull 2017;131:156-167.
van Empelen R, Jennekens-Schinkel A, Gorter JW, et al. Epilepsy surgery does not harm motor performance of children and adolescents. Brain 2005;128:1536-1545.
de Bode S, Firestine A, Mathern GW, Dobkin B. Residual motor control and cortical representations of function following hemispherectomy: effects of etiology. J Child Neurol 2005;20:64-75.
Küpper H, Kudernatsch M, Pieper T, et al. Predicting hand function after hemidisconnection. Brain 2016;139:2456-2468.
Holloway V, Gadian DG, Vargha-Khadem F, et al. The reorganization of sensorimotor function in children after hemispherectomy. A functional MRI and somatosensory evoked potential study. Brain 2000;123:2432-2444.
Staudt M, Grodd W, Gerloff C, et al. Two types of ipsilateral reorganization in congenital hemiparesis: a TMS and fMRI study. Brain 2002;125:2222-2237.
Staudt M, Krägeloh-Mann I, Holthausen H, et al. Searching for motor functions in dysgenic cortex: a clinical transcranial magnetic stimulation and functional magnetic resonance imaging study. J Neurosurg 2004;101:69-77.
Vitali P, Minati L, D'Incerti L, et al. Functional MRI in malformations of cortical development: activation of dysplastic tissue and functional reorganization. J Neuroimaging 2008;18:296-305.
Maillard LG, Tassi L, Bartolomei F, et al. Stereoelectroencephalography and surgical outcome in polymicrogyria-related epilepsy: a multicentric study. Ann Neurol 2017;82:781-794.
Maillard L, Ramantani G. Epilepsy surgery for polymicrogyria: a challenge to be undertaken. Epileptic Disord 2018;20:319-338.
Ramantani G, Koessler L, Colnat-Coulbois S, et al. Intracranial evaluation of the epileptogenic zone in regional infrasylvian polymicrogyria. Epilepsia 2013;54:296-304.
Maegaki Y, Maeoka Y, Ishii S, et al. Mechanisms of central motor reorganization in pediatric hemiplegic patients. Neuropediatrics 1997;28:168-174.
van der Kolk NM, Boshuisen K, van Empelen R, et al. Etiology-specific differences in motor function after hemispherectomy. Epilepsy Res 2013;103:221-230.
Koudijs SM, Leijten FSS, Ramsey NF, et al. Lateralization of motor innervation in children with intractable focal epilepsy-a TMS and fMRI study. Epilepsy Res 2010;90:140-150.
Eyre JA. Development and plasticity of the corticospinal system in man. Neural Plast 2003;10:93-106.
Staudt M, Gerloff C, Grodd W, et al. Reorganization in congenital hemiparesis acquired at different gestational ages. Ann Neurol 2004;56:854-863.
Wang AC, Ibrahim GM, Poliakov AV, et al. Corticospinal tract atrophy and motor fMRI predict motor preservation after functional cerebral hemispherectomy. J Neurosurg Pediatr 2018;21:81-89.
Guerrini R, Cavallin M, Pippucci T, et al. Is focal cortical dysplasia/epilepsy caused by somatic MTOR mutations always a unilateral disorder? Neurol Genet 2021;7:e540.
Nahum AS, Liégeois FJ. Language after childhood hemispherectomy: a systematic review. Neurology 2020;95:1043-1056.
Curtiss S, de Bode S, Mathern GW. Spoken language outcomes after hemispherectomy: factoring in etiology. Brain Lang 2001;79:379-396.
Althausen A, Gleissner U, Hoppe C, et al. Long-term outcome of hemispheric surgery at different ages in 61 epilepsy patients. J Neurol Neurosurg Psychiatry 2013;84:529-536.
Anderson V, Spencer-Smith M, Leventer R, et al. Childhood brain insult: can age at insult help us predict outcome? Brain 2009;132:45-56.
Ballantyne AO, Spilkin AM, Hesselink J, Trauner DA. Plasticity in the developing brain: intellectual, language and academic functions in children with ischaemic perinatal stroke. Brain 2008;131:2975-2985.
Basheer SN, Connolly MB, Lautzenhiser A, et al. Hemispheric surgery in children with refractory epilepsy: seizure outcome, complications, and adaptive function. Epilepsia 2007;48:133-140.
Puka K, Jones M, Mathern GW. Functional cognitive and language outcomes after cerebral hemispherectomy for hemimegalencephaly. Epilepsia 2021;62:2932-2940.
Braun KPJ. Influence of epilepsy surgery on developmental outcomes in children. Eur J Paediatr Neurol 2020;24:40-42.
Ramantani G, Reuner G. Cognitive development in pediatric epilepsy surgery. Neuropediatrics 2018;49:93-103.
Loddenkemper T, Holland KD, Stanford LD, et al. Developmental outcome after epilepsy surgery in infancy. Pediatrics 2007;119:930-935.