Download PDF
Neuropediatrics 2018; 49(02): 093-103
DOI: 10.1055/s-0037-1609034
Review Article
Georg Thieme Verlag KG Stuttgart · New York

Cognitive Development in Pediatric Epilepsy Surgery

Georgia Ramantani
1   Division of Child Neurology, University Children's Hospital, Zurich, Switzerland
2   Swiss Epilepsy Centre, Zurich, Switzerland
,
Gitta Reuner
3   Section of Neuropediatrics and Inborn Errors of Metabolism, University Children's Hospital, Heidelberg, Germany
› Author Affiliations
Further Information

Publication History

29 August 2017

10 October 2017

Publication Date:
05 December 2017 (online)

    Permissions and Reprints

Abstract

Epilepsy surgery is a very effective treatment option for children and adolescents with drug-resistant structural epilepsy, resulting in seizure freedom in the majority of cases. Beyond seizure freedom, the postsurgical stabilization or even improvement of cognitive development constitutes a fundamental objective. This study aims to address key features of cognitive development in the context of pediatric epilepsy surgery. Many surgical candidates present with severe developmental delay and cognitive deficits prior to surgery. Recent studies support that global cognitive development remains stable after surgery. Individual developmental trajectories are determined by the degree of presurgical developmental impairment, age at surgery, seizure freedom, antiepileptic drug tapering, and other case-specific factors. Compared with adults, children may better compensate for temporary postsurgical deficits in circumscribed cognitive functions such as memory. Particularly for left-sided temporal resections, children present a clear advantage in terms of postsurgical recovery with regard to verbal learning compared with adults. In the case of severe presurgical developmental impairment, minimal postsurgical improvements are often not measurable, although they are evident to patients' families and have a large impact on their quality of life. Multicenter studies with a standardized assessment protocol and longer follow-up intervals are urgently called for to provide deeper insights into the cognitive development after epilepsy surgery, to analyze the interaction between different predictors, and to facilitate the selection of appropriate candidates as well as the counseling of families.

Keywords

cognitive - development - epilepsy surgery - long-term follow-up

Authorship

Both authors have contributed equally to this study.


 

  • References

  • 1 Ryvlin P, Cross JH, Rheims S. Epilepsy surgery in children and adults. Lancet Neurol 2014; 13 (11) 1114-1126
    CrossrefPubMedGoogle Scholar
  • 2 West S, Nolan SJ, Cotton J. , et al. Surgery for epilepsy. Cochrane Database Syst Rev 2015; (07) CD010541
    PubMedGoogle Scholar
  • 3 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 (05) 498-506
    CrossrefPubMedGoogle Scholar
  • 4 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 (06) 1046-1055
    CrossrefPubMedGoogle Scholar
  • 5 Ramantani G, Kadish NE, Anastasopoulos C. , et al. Epilepsy surgery for glioneuronal tumors in childhood: avoid loss of time. Neurosurgery 2014; 74 (06) 648-657 , discussion 657
    CrossrefPubMedGoogle Scholar
  • 6 Ramantani G, Kadish NE, Mayer H. , et al. Frontal lobe epilepsy surgery in childhood and adolescence: predictors of long-term seizure freedom, overall cognitive and adaptive functioning. Neurosurgery 2017; DOI: 10.1093/neuros/nyx340. . [Epub ahead of print]
    CrossrefPubMedGoogle Scholar
  • 7 Ramantani G, Stathi A, Brandt A. , et al. Posterior cortex epilepsy surgery in childhood and adolescence: predictors of long-term seizure outcome. Epilepsia 2017; 58 (03) 412-419
    CrossrefPubMedGoogle Scholar
  • 8 Cross JH, Jayakar P, Nordli D. , et al; International League against Epilepsy, Subcommission for Paediatric Epilepsy Surgery; Commissions of Neurosurgery and Paediatrics. Proposed criteria for referral and evaluation of children for epilepsy surgery: recommendations of the Subcommission for Pediatric Epilepsy Surgery. Epilepsia 2006; 47 (06) 952-959
    CrossrefPubMedGoogle Scholar
  • 9 Van Schooneveld MM, Braun KP. Cognitive outcome after epilepsy surgery in children. Brain Dev 2013; 35 (08) 721-729
    CrossrefPubMedGoogle Scholar
  • 10 Gallagher A, Jambaqué I, Lassonde M. Cognitive outcome of surgery [Internet]. In: Dulac O, Lassonde M, Sarnat H, eds. Handbook of Clinical Neurology, Vol. 111 (3rd series), Pediatric Neurology, Part I.; 2013:797–802
    PubMedGoogle Scholar
  • 11 Lah S. Neuropsychological outcome following focal cortical removal for intractable epilepsy in children. Epilepsy Behav 2004; 5 (06) 804-817
    CrossrefPubMedGoogle Scholar
  • 12 Bayley N, Reuner G. The Bayley Scales of Infant and Toddler Development [in German]. 3rd ed. Frankfurt am Main, Germany: Pearson Assessment & Information; 2014
    Google Scholar
  • 13 Petermann F, Petermann U. , eds. Hamburg Wechsler Intelligenztest für Kinder – IV. Übersetzung und Adaptation der WISC-IV® von David Wechsler. Bern, Switzerland: Huber; 2007
    Google Scholar
  • 14 Sparrow S, Balla D, Cicchetti D. The Vineland Adaptive Behavior Scales Interview Edition, Survey Form Manual. Circle Pines, MN: American Guidance Service; 1984
    Google Scholar
  • 15 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 (01) 30-35
    CrossrefPubMedGoogle Scholar
  • 16 Loddenkemper T, Holland KD, Stanford LD, Kotagal P, Bingaman W, Wyllie E. Developmental outcome after epilepsy surgery in infancy. Pediatrics 2007; 119 (05) 930-935
    CrossrefPubMedGoogle Scholar
  • 17 Freitag H, Tuxhorn I. Cognitive function in preschool children after epilepsy surgery: rationale for early intervention. Epilepsia 2005; 46 (04) 561-567
    CrossrefPubMedGoogle Scholar
  • 18 Boshuisen K, van Schooneveld MM, Leijten FS. , et al. Contralateral MRI abnormalities affect seizure and cognitive outcome after hemispherectomy. Neurology 2010; 75 (18) 1623-1630
    CrossrefPubMedGoogle Scholar
  • 19 Busch RM, Lineweaver TT, Ferguson L, Haut JS. Reliable change indices and standardized regression-based change score norms for evaluating neuropsychological change in children with epilepsy. Epilepsy Behav 2015; 47: 45-54
    CrossrefPubMedGoogle Scholar
  • 20 Fay-McClymont TB, Hrabok M, Sherman EM. , et al. Systematic review and case series of neuropsychological functioning after epilepsy surgery in children with dysembryoplastic neuroepithelial tumors (DNET). Epilepsy Behav 2012; 23 (04) 481-486
    CrossrefPubMedGoogle Scholar
  • 21 Wethe JV, Prigatano GP, Gray J, Chapple K, Rekate HL, Kerrigan JF. Cognitive functioning before and after surgical resection for hypothalamic hamartoma and epilepsy. Neurology 2013; 81 (12) 1044-1050
    CrossrefPubMedGoogle Scholar
  • 22 Hermann BP, Jones JE, Jackson DC, Seidenberg M. Starting at the beginning: the neuropsychological status of children with new-onset epilepsies. Epileptic Disord 2012; 14 (01) 12-21
    PubMedGoogle Scholar
  • 23 Reuner G, Kadish NE, Doering JH, Balke D, Schubert-Bast S. Attention and executive functions in the early course of pediatric epilepsy. Epilepsy Behav 2016; 60: 42-49
    CrossrefPubMedGoogle Scholar
  • 24 D'Argenzio L, Colonnelli MC, Harrison S. , et al. Cognitive outcome after extratemporal epilepsy surgery in childhood. Epilepsia 2011; 52 (11) 1966-1972
    CrossrefPubMedGoogle Scholar
  • 25 Smith ML, Elliott IM, Lach L. Cognitive skills in children with intractable epilepsy: comparison of surgical and nonsurgical candidates. Epilepsia 2002; 43 (06) 631-637
    CrossrefPubMedGoogle Scholar
  • 26 Hermann BP, Dabbs K, Becker T. , et al. Brain development in children with new onset epilepsy: a prospective controlled cohort investigation. Epilepsia 2010; 51 (10) 2038-2046
    CrossrefPubMedGoogle Scholar
  • 27 Pulsifer MB, Brandt J, Salorio CF, Vining EP, Carson BS, Freeman JM. The cognitive outcome of hemispherectomy in 71 children. Epilepsia 2004; 45 (03) 243-254
    CrossrefPubMedGoogle Scholar
  • 28 Vasconcellos E, Wyllie E, Sullivan S. , et al. Mental retardation in pediatric candidates for epilepsy surgery: the role of early seizure onset. Epilepsia 2001; 42 (02) 268-274
    PubMedGoogle Scholar
  • 29 Cormack F, Cross JH, Isaacs E. , et al. The development of intellectual abilities in pediatric temporal lobe epilepsy. Epilepsia 2007; 48 (01) 201-204
    PubMedGoogle Scholar
  • 30 Vendrame M, Alexopoulos AV, Boyer K. , et al. Longer duration of epilepsy and earlier age at epilepsy onset correlate with impaired cognitive development in infancy. Epilepsy Behav 2009; 16 (03) 431-435
    CrossrefPubMedGoogle Scholar
  • 31 Moosa AN, Jehi L, Marashly A. , et al. Long-term functional outcomes and their predictors after hemispherectomy in 115 children. Epilepsia 2013; 54 (10) 1771-1779
    CrossrefPubMedGoogle Scholar
  • 32 Otte WM, Dijkhuizen RM, van Meer MPA. , et al. Characterization of functional and structural integrity in experimental focal epilepsy: reduced network efficiency coincides with white matter changes. PLoS One 2012; 7 (07) e39078
    CrossrefPubMedGoogle Scholar
  • 33 Smith ML, Elliott IM, Lach L. Cognitive, psychosocial, and family function one year after pediatric epilepsy surgery. Epilepsia 2004; 45 (06) 650-660
    CrossrefPubMedGoogle Scholar
  • 34 Skirrow C, Cross JH, Cormack F, Harkness W, Vargha-Khadem F, Baldeweg T. Long-term intellectual outcome after temporal lobe surgery in childhood. Neurology 2011; 76 (15) 1330-1337
    CrossrefPubMedGoogle Scholar
  • 35 Puka K, Tavares TP, Smith ML. Development of intelligence 4 to 11 years after paediatric epilepsy surgery. J Neuropsychol 2017; 11 (02) 161-173
    CrossrefPubMedGoogle Scholar
  • 36 Battaglia D, Chieffo D, Lettori D, Perrino F, Di Rocco C, Guzzetta F. Cognitive assessment in epilepsy surgery of children. Childs Nerv Syst 2006; 22 (08) 744-759
    CrossrefPubMedGoogle Scholar
  • 37 Chieffo D, Lettori D, Contaldo I. , et al. Surgery of children with frontal lobe lesional epilepsy: neuropsychological study. Brain Dev 2011; 33 (04) 310-315
    CrossrefPubMedGoogle Scholar
  • 38 Smith ML, Olds J, Snyder T, Elliott I, Lach L, Whiting S. A follow-up study of cognitive function in young adults who had resective epilepsy surgery in childhood. Epilepsy Behav 2014; 32: 79-83
    CrossrefPubMedGoogle Scholar
  • 39 Roulet-Perez E, Davidoff V, Mayor-Dubois C. , et al. Impact of severe epilepsy on development: recovery potential after successful early epilepsy surgery. Epilepsia 2010; 51 (07) 1266-1276
    CrossrefPubMedGoogle Scholar
  • 40 Gleissner U, Sassen R, Schramm J, Elger CE, Helmstaedter C. Greater functional recovery after temporal lobe epilepsy surgery in children. Brain 2005; 128 (Pt 12): 2822-2829
    CrossrefPubMedGoogle Scholar
  • 41 Viggedal G, Kristjansdottir R, Olsson I, Rydenhag B, Uvebrant P. Cognitive development from two to ten years after pediatric epilepsy surgery. Epilepsy Behav 2012; 25 (01) 2-8
    CrossrefPubMedGoogle Scholar
  • 42 Oitment C, Vriezen E, Smith ML. Everyday memory in children after resective epilepsy surgery. Epilepsy Behav 2013; 28 (02) 141-146
    CrossrefPubMedGoogle Scholar
  • 43 Harvey AS, Cross JH, Shinnar S, Mathern GW. ; ILAE Pediatric Epilepsy Surgery Survey Taskforce. Defining the spectrum of international practice in pediatric epilepsy surgery patients. Epilepsia 2008; 49 (01) 146-155
    CrossrefPubMedGoogle Scholar
  • 44 Jonas R, Asarnow RF, LoPresti C. , et al. Surgery for symptomatic infant-onset epileptic encephalopathy with and without infantile spasms. Neurology 2005; 64 (04) 746-750
    CrossrefPubMedGoogle Scholar
  • 45 Guerrini R, Duchowny M, Jayakar P. , et al. Diagnostic methods and treatment options for focal cortical dysplasia. Epilepsia 2015; 56 (11) 1669-1686
    CrossrefPubMedGoogle Scholar
  • 46 Hemb M, Velasco TR, Parnes MS. , et al. Improved outcomes in pediatric epilepsy surgery: the UCLA experience, 1986-2008. Neurology 2010; 74 (22) 1768-1775
    CrossrefPubMedGoogle Scholar
  • 47 Lendt M, Gleissner U, Helmstaedter C, Sassen R, Clusmann H, Elger CE. Neuropsychological outcome in children after frontal lobe epilepsy surgery. Epilepsy Behav 2002; 3 (01) 51-59
    CrossrefPubMedGoogle Scholar
  • 48 Lippé S, Bulteau C, Dorfmuller G, Audren F, Delalande O, Jambaqué I. Cognitive outcome of parietooccipital resection in children with epilepsy. Epilepsia 2010; 51 (10) 2047-2057
    CrossrefPubMedGoogle Scholar
  • 49 Asarnow RF, LoPresti C, Guthrie D. , et al. Developmental outcomes in children receiving resection surgery for medically intractable infantile spasms. Dev Med Child Neurol 1997; 39 (07) 430-440
    PubMedGoogle Scholar
  • 50 Ikonomidou C, Turski L. Antiepileptic drugs and brain development. Epilepsy Res 2010; 88 (01) 11-22
    CrossrefPubMedGoogle Scholar
  • 51 Loring DW, Meador KJ. Cognitive side effects of antiepileptic drugs in children. Neurology 2004; 62 (06) 872-877
    CrossrefPubMedGoogle Scholar
  • 52 Aldenkamp A, Besag F, Gobbi G, Caplan R, Dunn DW, Sillanpää M. Psychiatric and Behavioural Disorders in Children with Epilepsy (ILAE Task Force Report): Adverse cognitive and behavioural effects of antiepileptic drugs in children. Epileptic Disord 2016; DOI: 10.1684/epd.2016.0817.
    CrossrefPubMedGoogle Scholar
  • 53 Boshuisen K, Arzimanoglou A, Cross JH. , et al; TimeToStop study group. Timing of antiepileptic drug withdrawal and long-term seizure outcome after paediatric epilepsy surgery (TimeToStop): a retrospective observational study. Lancet Neurol 2012; 11 (09) 784-791
    CrossrefPubMedGoogle Scholar
  • 54 Boshuisen K, van Schooneveld MM, Uiterwaal CS. , et al; TimeToStop cognitive outcome study group. Intelligence quotient improves after antiepileptic drug withdrawal following pediatric epilepsy surgery. Ann Neurol 2015; 78 (01) 104-114
    CrossrefPubMedGoogle Scholar
  • 55 Bourgeois M, Crimmins DW, de Oliveira RS. , et al. Surgical treatment of epilepsy in Sturge-Weber syndrome in children. J Neurosurg 2007; 106 (1, Suppl): 20-28
    PubMedGoogle Scholar
  • 56 Westerveld M, Sass KJ, Chelune GJ. , et al. Temporal lobectomy in children: cognitive outcome. J Neurosurg 2000; 92 (01) 24-30
    CrossrefPubMedGoogle Scholar
  • 57 Miranda C, Smith ML. Predictors of intelligence after temporal lobectomy in children with epilepsy. Epilepsy Behav 2001; 2 (01) 13-19
    CrossrefPubMedGoogle Scholar
  • 58 Puka K, Khattab M, Kerr EN, Smith ML. Academic achievement one year after resective epilepsy surgery in children. Epilepsy Behav 2015; 47: 1-5
    CrossrefPubMedGoogle Scholar
  • 59 Warren AEL, Harvey AS, Abbott DF. , et al. Cognitive network reorganization following surgical control of seizures in Lennox-Gastaut syndrome. Epilepsia 2017; 58 (05) e757-81
    PubMedGoogle Scholar