Prevalence, Significance and Clinical Characteristics of Seizures, Epilepsy and Subclinical Electrical Activity in Autism
Abstract
This manuscript reviews epilepsy, seizures and/or subclinical electrical discharges (SEDs) in individuals with autism spectrum disorder (ASD), including prevalence of epilepsy and SEDs, clinical characteristics of this ASD subgroup and seizure types. The prevalence of epilepsy in ASD is higher than the prevalence of epilepsy in typically developing individuals and depends on age and gender as well as comorbid genetic, metabolic and intellectual abnormalities. Studies suggest that, in ASD, the prevalence of clinical seizures increases with age and that adults with ASD and epilepsy have greater behavioral and cognitive problem as well as elevated mortality. Temporal and frontal lobe epilepsies as well as electrical status epilepticus during sleep syndromes share characteristics with ASD yet these syndromes are rarely diagnosed in ASD. The prevalence of SEDs is very high in ASD. Studies suggest that SEDs and epilepsy share common underlying neuropathology but that children with epilepsy have greater cognitive and behavioral impairments than those with SEDs. Studies, mostly on children with epilepsy, provide evidence that SEDs are related to cognitive impairment. One study suggests that the patterns of temporal and frontal SEDs are related to the ASD diagnosis. These studies are consistent with the cognitive and behavioral abnormalities associated with temporal and frontal lobe epilepsies. This adds support for that fact that SEDs are significant. However, carefully controlled studies on the significance of SEDs in ASD are lacking.
Keywords
Full Text:
PDFReferences
Volkmar FR, Nelson DS. Seizure disorders in autism. J Am Acad Child Adolesc Psychiatry. 1990;29:127-129.
Tuchman R, Rapin I. Epilepsy in autism. Lancet Neurol. 2002;1:352- 358.
Deykin EY, MacMahon B. The incidence of seizures among children with autistic symptoms. Am J Psychiatry. 1979;136:1310-1312.
Danielsson S, Gillberg IC, Billstedt E, Gillberg C, Olsson I. Epilepsy in young adults with autism: a prospective population-based follow-up study of 120 individuals diagnosed in childhood. Epilepsia. 2005;46:918-923.
Hara H. Autism and epilepsy: a retrospective follow-up study. Brain Dev. 2007;29:486-490.
Frye RE, Butler I, Strickland D, Castillo E, Papanicolaou A. Electroencephalogram discharges in atypical cognitive development. J Child Neurol. 2010;25:556-566.
Turk J, Bax M, Williams C, Amin P, Eriksson M, Gillberg C. Autism spectrum disorder in children with and without epilepsy: impact on social functioning and communication. Acta Paediatr. 2009;98:675-681.
Frye RE. Metabolic and mitochondrial disorders associated with epilepsy in children with autism spectrum disorder. Epilepsy Behav. 2015;47:147-157.
Frye RE, Rossignol D, Casanova MF, et al. A review of traditional and novel treatments for seizures in autism spectrum disorder: findings from a systematic review and expert panel. Front Public Health. 2013;1:31.
Frye RE, Rossignol DA. Mitochondrial dysfunction can connect the diverse medical symptoms associated with autism spectrum disorders. Pediatr Res. 2011;69:41R-47R.
Rossignol DA, Frye RE. Mitochondrial dysfunction in autism spectrum disorders: a systematic review and meta-analysis. Mol Psychiatry. 2012;17:290-314.
Amiet C, Gourfinkel-An I, Bouzamondo A, et al. Epilepsy in autism is associated with intellectual disability and gender: evidence from a meta-analysis. Biol Psychiatry. 2008;64:577-582.
El Achkar CM, Spence SJ. Clinical characteristics of children and young adults with co-occurring autism spectrum disorder and epilepsy. Epilepsy Behav. 2015;47:183-190.
Levisohn PM. The autism-epilepsy connection. Epilepsia. 2007;48:33- 35.
Kim HL, Donnelly JH, Tournay AE, Book TM, Filipek P. Absence of seizures despite high prevalence of epileptiform EEG abnormalities in children with autism monitored in a tertiary care center. Epilepsia. 2006;47:394-398.
McVicar KA, Ballaban-Gil K, Rapin I, Moshe SL, Shinnar S. Epileptiform EEG abnormalities in children with language regression. Neurology. 2005;65:129-131.
Chez MG, Chang M, Krasne V, Coughlan C, Kominsky M, Schwartz A. Frequency of epileptiform EEG abnormalities in a sequential screening of autistic patients with no known clinical epilepsy from 1996 to 2005. Epilepsy Behav. 2006;8:267-271.
Lewine JD, Andrews R, Chez M, et al. Magnetoencephalographic patterns of epileptiform activity in children with regressive autism spectrum disorders. Pediatrics. 1999;104:405-418.
Munoz-Yunta JA, Ortiz T, Palau-Baduell M, et al. Magnetoencephalo- graphic pattern of epileptiform activity in children with early-onset autism spectrum disorders. Clin Neurophysiol. 2008;119:626-634.
Saemundsen E, Ludvigsson P, Hilmarsdottir I, Rafnsson V. Autism spectrum disorders in children with seizures in the first year of life - a population-based study. Epilepsia. 2007;48:1724-1730.
Berg AT, Berkovic SF, Brodie MJ, et al. Revised terminology and concepts for organization of seizures and epilepsies: report of the ILAE Commission on Classification and Terminology, 2005-2009. Epilepsia. 2010;51:676-685.
Saemundsen E, Ludvigsson P, Rafnsson V. Risk of autism spectrum disorders after infantile spasms: a population-based study nested in a cohort with seizures in the first year of life. Epilepsia. 2008;49:1865- 1870.
Saemundsen E, Ludvigsson P, Rafnsson V. Autism spectrum disorders in children with a history of infantile spasms: a population-based study. J Child Neurol. 2007;22:1102-1107.
Parmeggiani A, Barcia G, Posar A, Raimondi E, Santucci M, Scaduto MC. Epilepsy and EEG paroxysmal abnormalities in autism spectrum disorders. Brain Dev. 2010;32:783-789.
Bolton PF, Carcani-Rathwell I, Hutton J, Goode S, Howlin P, Rutter M. Epilepsy in autism: features and correlates. Br J Psychiatry. 2011;198:289-294.
Pavone P, Incorpora G, Fiumara A, Parano E, Trifiletti RR, Ruggieri M. Epilepsy is not a prominent feature of primary autism. Neuropediatrics. 2004;35:207-210.
Oslejskova H, Dusek L, Makovska Z, Rektor I. Epilepsia, epileptiform abnormalities, non-right-handedness, hypotonia and severe decreased IQ are associated with language impairment in autism. Epileptic Disord. 2007;9:S9-S18.
Unal O, Ozcan O, Oner O, Akcakin M, Aysev A, Deda G. EEG and MRI findings and their relation with intellectual disability in pervasive developmental disorders. World J Pediatr. 2009:5:196-200.
Huang CH, Peng SS, Weng WC, Su YN, Lee WT. The relationship of neuroimaging findings and neuropsychiatric comorbidities in children with tuberous sclerosis complex. J Formos Med Assoc. 2014. pii: S0929-6646(14)00071-0.
Bolton PF, Griffiths PD. Association of tuberous sclerosis of temporal lobes with autism and atypical autism. Lancet. 1997;349:392-395.
Blackmon K. Structural MRI biomarkers of shared pathogenesis in
autism spectrum disorder and epilepsy. Epilepsy Behav. 2015;47:172-
Blackmon K, Bluvstein J, MacAllister WS, et al. Treatment Resistant
Epilepsy in Autism Spectrum Disorder: Increased Risk for Females.
Autism Res. 2015. [ in press]
Sasaki M. SPECT findings in autism spectrum disorders and medically
refractory seizures. Epilepsy Behav. 2015;47:167-171.
Sasaki M, Nakagawa E, Sugai K, et al. Brain perfusion SPECT and EEG findings in children with autism spectrum disorders and
medically intractable epilepsy. Brain Dev. 2010;32:776-782.
Deonna T, Roulet E. Autistic spectrum disorder: evaluating a possible
contributing or causal role of epilepsy. Epilepsia. 2006;47:79-82.
Tuchman RF, Rapin I. Regression in pervasive developmental disorders: seizures and epileptiform electroencephalogram correlates.
Pediatrics. 1997;99:560-566.
Oslejskova H, Dusek L, Makovska Z, Pejcochova J, Autrata R, Slapak
I. Complicated relationship between autism with regression and epilepsy. Neuro Endocrinol Lett. 2008;29:558-570.
Pickett J, Xiu E, Tuchman R, Dawson G, Lajonchere C. Mortality in individuals with Autism, with and without Epilepsy. J Child Neurol. 2011;26:932-939.
Hartley-McAndrew M, Weinstock A. Autism Spectrum Disorder: Correlation between aberrant behaviors, EEG abnormalities and seizures. Neurol Int. 2010;2:e10.
Shavelle RM, Strauss DJ, Pickett J. Causes of death in autism. J Autism Dev Disord. 2001;31:569-576.
Tuchman RF, Rapin I, Shinnar S. Autistic and dysphasic children. II: Epilepsy. Pediatrics. 1991;88:1219-1225.
Steffenburg S, Gillberg C, Steffenburg U. Psychiatric disorders in children and adolescents with mental retardation and active epilepsy. Arch Neurol. 1996;53:904-912.
Rossi PG, Parmeggiani A, Bach V, Santucci M, Visconti P. EEG features and epilepsy in patients with autism. Brain Dev. 1995;17:169- 174.
Matsuo M, Maeda T, Sasaki K, Ishii K, Hamasaki Y. Frequent association of autism spectrum disorder in patients with childhood onset epilepsy. Brain Dev. 2010;32:759-763.
Matsuo M, Maeda T, Ishii K, Tajima D, Koga M, Hamasaki Y. Characterization of childhood-onset complex partial seizures associated with autism spectrum disorder. Epilepsy Behav. 2011; 20:524-527.
Marin JC, Moura PJ, Cysneiros RM, et al. Temporal lobe epilepsy and social behavior: an animal model for autism? Epilepsy Behav. 2008;13:43-46.
Besag FM. Behavioral aspects of pediatric epilepsy syndromes. Epilepsy Behav. 2004;5:S3-S13.
DeLong GR, Heinz ER. The clinical syndrome of early-life bilateral hippocampal sclerosis. Ann Neurol. 1997;42:11-17.
Pascual-Castroviejo I, Pascual-Pascual SI. Bilateral arachnoid cysts, seizures and severe encephalopathy: case report. Neuropediatrics. 1994;25:42-43.
Strauss KA, Puffenberger EG, Huentelman MJ, et al. Recessive symptomatic focal epilepsy and mutant contactin-associated protein- like 2. N Engl J Med. 2006;354:1370-1377.
Mikati MA, El-Bitar MK, Najjar MW, et al. A child with refractory complex partial seizures, right temporal ganglioglioma, contralateral continuous electrical status epilepticus, and a secondary Landau- Kleffner autistic syndrome. Epilepsy Behav. 2009;14:411-417.
McLellan A, Davies S, Heyman I, et al. Psychopathology in children with epilepsy before and after temporal lobe resection. Dev Med Child Neurol. 2005;47:666-672.
Taylor DC, Neville BG, Cross JH. Autistic spectrum disorders in childhood epilepsy surgery candidates. Eur Child Adolesc Psychiatry. 1999;8:189-192.
Parkinson GM. Pragmatic difficulties in children with autism associated with childhood epilepsy. Ped Rehab. 2006;9:229-246.
Patrikelis P, Angelakis E, Gatzonis S. Neurocognitive and behavioral functioning in frontal lobe epilepsy: a review. Epilepsy Behav. 2009;14:19-26.
Fohlen M, Bulteau C, Jalin C, Jambaque I, Delalande O. Behavioral epileptic seizures: a clinical and intracranial EEG study in 8 children with frontal lobe epilepsy. Neuropediatrics. 2004;35:336-345.
Hashimoto T, Sasaki M, Sugai K, Hanaoka S, Fukumizu M, Kato T. Paroxysmal discharges on EEG in young autistic patients are frequent in frontal regions. J Med Invest. 2001;48:175-180.
Landau WM, Kleffner FR. Syndrome of acquired aphasia with convulsive disorder in children. Neurology. 1957;7:523-530.
Morrell F, Whisler WW, Smith MC, et al. Landau-Kleffner syndrome. Treatment with subpial intracortical transection. Brain. 1995;118:1529- 1546.
Roulet Perez E, Davidoff V, Despland PA, Deonna T. Mental and behavioural deterioration of children with epilepsy and CSWS: acquired epileptic frontal syndrome. Dev Med Child Neurol. 1993;35:661-674.
Tuchman R. CSWS-related autistic regression versus autistic regression without CSWS. Epilepsia. 2009;50:18-20.
Lee H, Kang HC, Kim SW, Kim YK, Chung HJ. Characteristics of late-onset epilepsy and EEG findings in children with autism spectrum disorders. Korean J Pediatr. 2011;54:22-28.
Otsubo H, Chitoku S, Ochi A, et al. Malignant rolandic-sylvian epilepsy in children: diagnosis, treatment, and outcomes. Neurology. 2001;57:590-596.
Ong HT, Wyllie E. Benign childhood epilepsy with centrotemporal spikes: is it always benign? Neurology. 2000;54:1182-1185.
Nicolai J, Aldenkamp AP, Arends J, Weber JW, Vles JS. Cognitive and behavioral effects of nocturnal epileptiform discharges in children with benign childhood epilepsy with centrotemporal spikes. Epilepsy Behav. 2006;8:56-70.
Beaumanoir A, Ballis T, Varfis G, Ansari K. Benign epilepsy of childhood with Rolandic spikes. A clinical, electroencephalographic, and telencephalographic study. Epilepsia. 1974;15:301-315.
Beaussart M, Faou R. Evolution of epilepsy with rolandic paroxysmal foci: a study of 324 cases. Epilepsia. 1978;19:337-342.
Staden U, Isaacs E, Boyd SG, Brandl U, Neville BG. Language dysfunction in children with Rolandic epilepsy. Neuropediatrics. 1998;29:242-248.
Lerman P, Kivity S. Benign focal epilepsy of childhood. A follow-up study of 100 recovered patients. Arch Neurol. 1975;32:261-264.
Kohrman MH, Carney PR. Sleep-related disorders in neurologic disease during childhood. Ped Neurol. 2000;23:107-113.
D'Alessandro P, Piccirilli M, Tiacci C, et al. Neuropsychological features of benign partial epilepsy in children. Ital J Neurol Sci. 1990;11:265-269.
Metz-Lutz MN, Kleitz C, de Saint Martin A, Massa R, Hirsch E, Marescaux C. Cognitive development in benign focal epilepsies of childhood. Dev Neurosci. 1999;21:182-190.
Papavasiliou A, Mattheou D, Bazigou H, Kotsalis C, Paraskevoulakos E. Written language skills in children with benign childhood epilepsy with centrotemporal spikes. Epilepsy Behav. 2005;6:50-58.
Baglietto MG, Battaglia FM, Nobili L, et al. Neuropsychological disorders related to interictal epileptic discharges during sleep in benign epilepsy of childhood with centrotemporal or Rolandic spikes. Dev Med Child Neurol. 2001;43:407-412.
Piccirilli M, D'Alessandro P, Tiacci C, Ferroni A. Language lateralization in children with benign partial epilepsy. Epilepsia. 1988;29:19-25.
Piccirilli M, D'Alessandro P, Sciarma T, et al. Attention problems in epilepsy: possible significance of the epileptogenic focus. Epilepsia. 1994;35:1091-1096.
Northcott E, Connolly AM, Berroya A, et al. The neuropsychological and language profile of children with benign rolandic epilepsy. Epilepsia. 2005;46:924-930.
Wolff M, Weiskopf N, Serra E, Preissl H, Birbaumer N, Kraegeloh- Mann I. Benign partial epilepsy in childhood: selective cognitive deficits are related to the location of focal spikes determined by combined EEG/MEG. Epilepsia. 2005;46:1661-1667.
Weglage J, Demsky A, Pietsch M, Kurlemann G. Neuropsychological, intellectual, and behavioral findings in patients with centrotemporal spikes with and without seizures. Dev Med Child Neurol. 1997;39:646- 651.
Fonseca LC, Tedrus GM, Tonelotto JM, Antunes Td Tde A, Chiodi MG. School performance in children with benign childhood epilepsy with centrotemporal spikes. Arquivos de neuro-psiquiatria. 2004;62:459-462.
Massa R, de Saint-Martin A, Carcangiu R, et al. EEG criteria predictive of complicated evolution in idiopathic rolandic epilepsy. Neurology. 2001;57:1071-1079.
Aldenkamp AP, Arends J, de la Parra NM, Migchelbrink EJ. The cognitive impact of epileptiform EEG discharges and short epileptic seizures: relationship to characteristics of the cognitive tasks. Epilepsy Behav. 2010;17:205-209.
Aldenkamp AP, Arends J, Verspeek S, Berting M. The cognitive impact of epileptiform EEG-discharges; relationship with type of cognitive task. Child Neuropsychol. 2004;10:297-305.
Aldenkamp AP, Weber B, Overweg-Plandsoen WC, Reijs R, van Mil S. Educational underachievement in children with epilepsy: a model to predict the effects of epilepsy on educational achievement. J Child Neurol. 2005;20:175-180.
Aldenkamp A, Arends J. The relative influence of epileptic EEG discharges, short nonconvulsive seizures, and type of epilepsy on cognitive function. Epilepsia. 2004;45(1):54-63.
Aldenkamp AP, Overweg J, Gutter T, Beun AM, Diepman L, Mulder OG. Effect of epilepsy, seizures and epileptiform EEG discharges on cognitive function. Acta Neurol Scand. 1996;93:253-259.
Laporte N, Sebire G, Gillerot Y, Guerrini R, Ghariani S. Cognitive epilepsy: ADHD related to focal EEG discharges. Pediatr Neurol. 2002;27:307-311.
Pressler RM, Robinson RO, Wilson GA, Binnie CD. Treatment of interictal epileptiform discharges can improve behavior in children with behavioral problems and epilepsy. J Pediatr. 2005;146:112-117.
Marston D, Besag F, Binnie CD, Fowler M. Effects of transitory cognitive impairment on psychosocial functioning of children with epilepsy: a therapeutic trial. Dev Med Child Neurol. 1993;35:574-581.
Richer LP, Shevell MI, Rosenblatt BR. Epileptiform abnormalities in children with attention-deficit-hyperactivity disorder. Ped Neurol. 2002;26:125-129.
Millichap JJ, Stack CV, Millichap JG. Frequency of epileptiform discharges in the sleep-deprived electroencephalogram in children evaluated for attention-deficit disorders. J Child Neurol. 2011 ;26:6-11.
Politi K, Kivity S, Goldberg-Stern H, Halevi A, Shuper A. Selective Mutism and Abnormal Electroencephalography (EEG) Tracings. J Child Neurol. 2011;26:1377-1382.
Aldenkamp AP, Overweg-Plandsoen WC, Diepman LAM. Factors involved in learning problems and educational delay in children with epilepsy. Child Neuropsychol. 1999;5:130-138.
Aldenkamp AP, Overweg-Plandsoen WC, Arends J. An open, nonrandomized clinical comparative study evaluating the effect of epilepsy on learning. J Child Neurol. 1999;14:795-800.
Kasteleijn-Nolst Trenite DG. Transient cognitive impairment during subclinical epileptiform electroencephalographic discharges. Semin Pediatr Neurol. 1995;2:246-253.
Engler F, Maeder-Ingvar M, Roulet E, Deonna T. Treatment with Sulthiame (Ospolot) in benign partial epilepsy of childhood and related syndromes: an open clinical and EEG study. Neuropediatrics. 2003; 34:105-109.
Ronen GM, Richards JE, Cunningham C, Secord M, Rosenbloom D. Can sodium valproate improve learning in children with epileptiform bursts but without clinical seizures? Dev Med Child Neurol. 2000;42:751-755.
Yasuhara A. Correlation between EEG abnormalities and symptoms of autism spectrum disorder (ASD). Brain Dev. 2010;32:791-798.
Refbacks
- There are currently no refbacks.