Trends, outcomes, and complications of surgery for lesional epilepsy in infants and toddlers: A multicenter study.
developmental outcome
infants
predictors
seizure outcome
surgical treatment
Journal
Epilepsia open
ISSN: 2470-9239
Titre abrégé: Epilepsia Open
Pays: United States
ID NLM: 101692036
Informations de publication
Date de publication:
19 Jun 2024
19 Jun 2024
Historique:
revised:
13
04
2024
received:
19
11
2023
accepted:
03
05
2024
medline:
20
6
2024
pubmed:
20
6
2024
entrez:
20
6
2024
Statut:
aheadofprint
Résumé
To assess seizure and developmental outcomes, their predictors, and complications in 160 children who, between 1998 and 2022, underwent surgery for lesional epilepsy with curative intent before the age of 3 years. To compare trends in epilepsy surgery in this age group before and after the year 2014. Retrospective multicenter study. Descriptive and univariate analyses, and multivariable models for all outcomes. These 160 patients (76 F; 47.5%) underwent 169 surgeries (age at surgery 20.4 ± 9.4 months). At the last follow-up (77 ± 57.4 months), 121 patients (75.6%) were in Engel class I, 106 (66.2%) of whom were in Engel class Ia. Antiseizure medications were stopped in 84 patients (52.5%). Complications requiring reoperations were observed in 16 patients (10%; 9.5% of surgeries) and unexpected permanent deficits in 12 (7.5%; 7.1% of surgeries). Postoperative cognitive functions remained unchanged in 56 patients (44.4%), improved in 51 (40.5%), and worsened in 19 (15.1%). Multivariable analyses showed that the probability of achieving Engel class Ia was lower when the duration of epilepsy was longer, patients underwent preoperative video-EEG, and unexpected postoperative permanent deficits occurred. Cognitive improvement after surgery was associated with lower preoperative seizure frequency, better preoperative developmental level, and a longer postoperative follow-up. FCDII and tumors were the histopathologies carrying a higher probability of achieving seizure freedom, while polymicrogyria was associated with a lower probability of cognitive improvement. The number of patients operated on after 2014 was higher than before (61.3% vs. 38.7%), with stable outcomes. Epilepsy surgery is effective and safe in infants and toddlers, although the complication rate is higher than seen in older patients. Shorter duration of epilepsy, lower seizure frequency, no need for video-EEG, tumors, and some malformations of cortical development are robust predictors of seizure and cognitive outcome that may be exploited to increase earlier referral. This study analyzed the results of epilepsy surgery in 160 children who had been operated on before the age of 3 years at four Italian centers between 1998 and 2022. At the last follow-up (77 ± 57.4 months), 121 patients (75.6%) were free from disabling seizures, of which 106 (66.2%) were completely seizure-free since surgery. Major surgical complications occurred in 28 patients (17.5%), which is higher than observed with epilepsy surgery in general, but similar to hemispheric/multilobar surgery. Postoperative cognitive function remained unchanged in 56 patients (44.4%), improved in 51 (40.5%), and worsened in 19 (15.1%). Epilepsy surgery is effective and safe in infants and toddlers.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024 The Author(s). Epilepsia Open published by Wiley Periodicals LLC on behalf of International League Against Epilepsy.
Références
Wirrell E, Wong‐Kisiel L, Mandrekar J, Nickels K. Predictors and course of medically intractable epilepsy in young children presenting before 36 months of age: a retrospective, population‐based study. Epilepsia. 2012;53(9):1563–1569.
Dwivedi R, Ramanujam B, Chandra PS, Sapra S, Gulati S, Kalaivani M, et al. Surgery for drug‐resistant epilepsy in children. N Engl J Med. 2017;377(17):1639–1647.
Widjaja E, Jain P, Demoe L, Guttmann A, Tomlinson G, Sander B. Seizure outcome of pediatric epilepsy surgery. Neurology. 2020;94(7):311–321.
Baud MO, Perneger T, Rácz A, Pensel MC, Elger C, Rydenhag B, et al. European trends in epilepsy surgery. Neurology. 2018;91(2):e96–e106.
Barba C, Specchio N, Guerrini R, Tassi L, De Masi S, Cardinale F, et al. Increasing volume and complexity of pediatric epilepsy surgery with stable seizure outcome between 2008 and 2014: a nationwide multicenter study. Epilepsy Behav. 2017;75:151–157.
Englot DJ, Ouyang D, Garcia PA, Barbaro NM, Chang EF. Epilepsy surgery trends in the United States, 1990‐2008. Neurology. 2012;78(16):1200–1206.
Lamberink HJ, Otte WM, Blümcke I, Braun KPJ, Aichholzer M, Amorim I, et al. Seizure outcome and use of antiepileptic drugs after epilepsy surgery according to histopathological diagnosis: a retrospective multicentre cohort study. Lancet Neurol. 2020;19(9):748–757.
Perry MS, Shandley S, Perelman M, Singh RK, Wong‐Kisiel L, Sullivan J, et al. Surgical evaluation in children. Epilepsia. 2022;63(1):96–107.
Duchowny M, Jayakar P, Resnick T, Harvey AS, Alvarez L, Dean P, et al. Epilepsy surgery in the first three years of life. Epilepsia. 1998;39(7):737–743.
Loddenkemper T, Holland KD, Stanford LD, Kotagal P, Bingaman W, Wyllie E. Developmental outcome after epilepsy surgery in infancy. Pediatrics. 2007;119(5):930–935.
Roth J, Constantini S, Ekstein M, Weiner HL, Tripathi M, Chandra PS, et al. Epilepsy surgery in infants up to 3 months of age: safety, feasibility, and outcomes: a multicenter, multinational study. Epilepsia. 2021;62(8):1897–1906.
Tsou AY, Kessler SK, Wu M, Abend NS, Massey SL, Treadwell JR. Surgical treatments for epilepsies in children aged 1‐36 months: a systematic review. Neurology. 2023;100(1):E1–E15.
Frank NA, Greuter L, Guzman R, Soleman J. Early surgical approaches in pediatric epilepsy ‐ a systematic review and meta‐analysis. Childs Nerv Syst. 2023;39(3):677–688.
Iwasaki M, Iijima K, Kawashima T, Tachimori H, Takayama Y, Kimura Y, et al. Epilepsy surgery in children under 3 years of age: surgical and developmental outcomes. J Neurosurg Pediatr. 2021;28(4):395–403.
Li H, Ji S, Dong B, Chen L. Seizure control after epilepsy surgery in early childhood: a systematic review and meta‐analysis. Epilepsy Behav. 2021;125:108369.
Yu H, Liu Q, Wang R, Liu C, Sun Y, Wang Y, et al. Long‐term seizure and developmental outcomes of epilepsy surgery in children under 3 years old: a single‐center study of 113 patients. CNS Neurosci Ther. 2024;30(1):e14481.
Steinbok P, Gan PYC, Connolly MB, Carmant L, Barry Sinclair D, Rutka J, et al. Epilepsy surgery in the first 3 years of life: a Canadian survey. Epilepsia. 2009;50(6):1442–1449.
Wilson SJ, Baxendale S, Barr W, Hamed S, Langfitt J, Samson S, et al. Indications and expectations for neuropsychological assessment in routine epilepsy care: report of the ILAE neuropsychology task force, diagnostic methods commission, 2013‐2017. Epilepsia. 2015;56(5):674–681.
Sibilia V, Barba C, Metitieri T, Michelini G, Giordano F, Genitori L, et al. Cognitive outcome after epilepsy surgery in children: a controlled longitudinal study. Epilepsy Behav. 2017;73:23–30.
Barba C, Cossu M, Guerrini R, Di Gennaro G, Villani F, De Palma L, et al. Temporal lobe epilepsy surgery in children and adults: a multicenter study. Epilepsia. 2021;62(1):128–148.
Najm I, Lal D, Alonso Vanegas M, Cendes F, Lopes‐Cendes I, Palmini A, et al. The ILAE consensus classification of focal cortical dysplasia: an update proposed by an ad hoc task force of the ILAE diagnostic methods commission. Epilepsia. 2022;63(8):1899–1919.
Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella‐Branger D, Cavenee WK, et al. The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol. 2016;131(6):803–820.
Engel J. Update on surgical treatment of the epilepsies. Summary of the second international Palm Desert conference on the surgical treatment of the epilepsies (1992). Neurology. 1993;43(8):1612–1617.
Pelliccia V, Deleo F, Gozzo F, Giovannelli G, Mai R, Cossu M, et al. Early epilepsy surgery for non drug‐resistant patients. Epilepsy Behav Rep. 2022;19:100542.
Dunkley C, Kung J, Scott RC, Nicolaides P, Neville B, Aylett SE, et al. Epilepsy surgery in children under 3 years. Epilepsy Res. 2011;93(2–3):96–106.
Wyllie E, Comair YG, Kotagal P, Raja S, Ruggieri P. Epilepsy surgery in infants. Epilepsia. 1996;37(7):625–637.
Boshuisen K, Van Schooneveld MMJ, Uiterwaal CSPM, Cross JH, Harrison S, Polster T, et al. Intelligence quotient improves after antiepileptic drug withdrawal following pediatric epilepsy surgery. Ann Neurol. 2015;78(1):104–114.
Sylvén I, Olsson I, Hallböök T, Rydenhag B, Reilly C. “In the best case seizure‐free” ‐ parental hopes and worries before and satisfaction after their child's epilepsy surgery. Epilepsy Behav. 2020;110:107153.
Blumcke I, Spreafico R, Haaker G, Coras R, Kobow K, Bien CG, et al. Histopathological findings in brain tissue obtained during epilepsy surgery. N Engl J Med. 2017;377(17):1648–1656.
Ryvlin P, Cross JH, Rheims S. Epilepsy surgery in children and adults. Lancet Neurol. 2014;13(11):1114–1126.
Ramantani G, Bulteau C, Cserpan D, Otte WM, Dorfmüller G, Cross JH, et al. Not surgical technique, but etiology, contralateral MRI, prior surgery, and side of surgery determine seizure outcome after pediatric hemispherotomy. Epilepsia. 2023;64(5):1214–1224.
Sugimoto T, Otsubo H, Hwang PA, Hoffman HJ, Jay V, Snead OC. Outcome of epilepsy surgery in the first three years of life. Epilepsia. 1999;40(5):560–565.
Jayakar P, Gaillard WD, Tripathi M, Libenson MH, Mathern GW, Cross JH, et al. Diagnostic test utilization in evaluation for resective epilepsy surgery in children. Epilepsia. 2014;55(4):507–518.
Makridis KL, Atalay DA, Thomale UW, Tietze A, Elger CE, Kaindl AM. Epilepsy surgery in the first six months of life: a systematic review and meta‐analysis. Seizure. 2022;96:109–117.
Hader WJ, Tellez‐Zenteno J, Metcalfe A, Hernandez‐Ronquillo L, Wiebe S, Kwon CS, et al. Complications of epilepsy surgery – a systematic review of focal surgical resections and invasive EEG monitoring. Epilepsia. 2013;54(5):840–847.
Alotaibi F, Albaradie R, Almubarak S, Baeesa S, Steven DA, Girvin JP. Hemispherotomy for epilepsy: the procedure evolution and outcome. Can J Neurol Sci. 2021;48(4):451–463.
Cohen NT, Chang P, You X, Zhang A, Havens KA, Oluigbo CO, et al. Prevalence and risk factors for Pharmacoresistance in children with focal cortical dysplasia‐related epilepsy. Neurology. 2022;99(18):E2006–E2013.
Cloppenborg T, van Schooneveld M, Hagemann A, Hopf JL, Kalbhenn T, Otte WM, et al. Development and validation of prediction models for developmental and intellectual outcome following pediatric epilepsy surgery. Neurology. 2022;98(3):E225–E235.
Van Schooneveld MMJ, Braun KPJ. Cognitive outcome after epilepsy surgery in children. Brain Dev. 2013;35(8):721–729.
Puka K, Tavares TP, Lou SM. Development of intelligence 4 to 11 years after paediatric epilepsy surgery. J Neuropsychol. 2017;11(2):161–173.
Braun KPJ. Preventing cognitive impairment in children with epilepsy. Curr Opin Neurol. 2017;30(2):140–147.
Berg AT, Zelko FA, Levy SR, Testa FM. Age at onset of epilepsy, pharmacoresistance, and cognitive outcomes. Neurology. 2012;79(13):1384–1391.
Arfaie S, Amin P, Kwan ATH, Solgi A, Sarabi A, Hakak‐Zargar B, et al. Long‐term full‐scale intelligent quotient outcomes following pediatric and childhood epilepsy surgery: a systematic review and meta‐analysis. Seizure. 2023;106:58–67.
Guerrini R, Scerrati M, Rubboli G, Esposito V, Colicchio G, Cossu M, et al. Overview of presurgical assessment and surgical treatment of epilepsy from the Italian league against epilepsy. Epilepsia. 2013;54(Suppl 7):35–48.
Consales A, Casciato S, Asioli S, Barba C, Caulo M, Colicchio G, et al. The surgical treatment of epilepsy. Neurol Sci. 2021;42(6):2249–2260.
Cross JH, Jayakar P, Nordli D, Delalande O, Duchowny M, Wieser HG, et al. Proposed criteria for referral and evaluation of children for epilepsy surgery: recommendations of the subcommission for pediatric epilepsy surgery. Epilepsia. 2006;47(6):952–959.
Jayakar P, Jayakar A, Libenson M, Arzimanoglou A, Rhydenhag B, Cross JH, et al. Epilepsy surgery near or in eloquent cortex in children‐practice patterns and recommendations for minimizing and reporting deficits. Epilepsia. 2018;59(8):1484–1491.
Barba C, Cross JH, Braun K, Cossu M, Klotz KA, De Masi S, et al. Trends in pediatric epilepsy surgery in Europe between 2008 and 2015: country‐, center‐, and age‐specific variation. Epilepsia. 2020;61(2):216–222.