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Submitted
August 5, 2020
Accepted
October 4, 2021
Published
December 11, 2021
Main Article Content
Abstract
Background: Autism in children is frequently associated with Intellectual disability (ID) and epilepsy. It is known that lower IQ
influences epilepsy rates; however, electroencephalographic (EEG) findings in different grades of intellectual functioning are less well studied. Objectives: This study aimed to evaluate the EEG findings and their association with the degrees of ID in children with autism. Methods: Fifty-two children, diagnosed with autism according to the DSM-IV-TR criteria, aged between 2 to 12 years, were included in the study. Participants were recruited from outpatient clinic in the Institute for Paediatric Neurodisorder and Autism (IPNA) in Bangabandhu Sheikh Mujib Medical University (BSMMU), Dhaka, Bangladesh. All of them were subjected to physical and neurological examination. Intelligence quotients (IQ) were measured in all the participants. Psychometric tests Bayley Scales of Infant and Toddler Development, Third edition (BSID III) or Weschler Intelligence Scale for Patients-Revised (WISC-R) were used for evaluating IQ. EEG recordings were done in all the participants. Results: The frequency of EEG abnormalities were observed in 51.9% participants. Among these abnormalities, 36.5% were epileptiform and 15.4% were non-epileptiform. Majority of the focal discharges, in this study were from temporal and frontal ((50% and 40% of focal discharge). Among generalized abnormalities, 89% were symmetrical spike-wave complexes. EEG abnormalities were associated with epilepsy in 66.7% of participants. ID was present in 84.6% and of them, 77% had moderate to severe ID. Mild, moderate or severe ID did not show significant association with EEG abnormalities (p>0.05). However, patients with moderate to severe ID (IQ <50) had a higher rate of EEG abnormalities compared to those without ID or mild ID (81.5% versus 18.5%) (P=0.03). Conclusion: Relatively large number of children with autism and ID had EEG abnormalities and there was a significant association with moderate to severe ID (IQ <50) and EEG abnormalities.
Keywords
Autism, electroencephalography, intellectual disability
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How to Cite
Akhter, S., Shefa, J. ., & Mannan, M. . (2021). EEG changes and their relationship with intellectual disability in children with autism spectrum disorders in a tertiary care hospital. Journal of the International Child Neurology Association, 1(1). https://doi.org/10.17724/jicna.2021.205
References
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1. Samra N.M., Ghaffar H.M.A., El-Awady H.A., Soltan M.R. and Moktader R.M.A. Epilepsy and EEG Findings in Children with Autism Spectrum Disorders Autism. Open Access 2017, 7:3 DOI: 10.4172/2165-7890.1000211
2. Ünal Ö, Özcan Ö, Öner Ö, Akcakin M., Aysev A., Deda G.EEG and MRI findings and their relation with intellectual disability in pervasive developmental disorders. World J Pediatr, 2009 August; 5(3): 196–200. doi:10.1007/s12519-009-0037-y
3. Dawson M, Soulieres I, Gernsbacher MA, Mottron L. The level and nature of autistic intelligence. Psychol Sci, 2007; 18:657– 662.
4. Pacheva I. , Ivanov I. , Yordanova R. , Gaberova K., Galabova F., Panova M. , Petkova A., Timova E. and Sotkova I. Epilepsy in Children with Autistic Spectrum Disorder . Children 2019, 6, 15; doi:10.3390/children6020015…new number www.mdpi.com/journal/children
5. Elkholy N., Ezedin A., Hamdy M., Wafa H.A.E. Electroencephalographic pattern among autistic children and their relatives. Egypt J Psychiatry 2017, 36:150–157
6. Yasuhara A. Correlation between EEG abnormalities and symptoms of autism spectrum disorder (ASD). Brain Dev, 2010, 32: 791-798.
7. Chez MG, Krasne CM, 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
8. 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.
9. Canitano R, Luchetti A, Zappella M. Epilepsy, electroencephalographic abnormalities, and regression in children with autism. J Child Neurol 2005; 20:27–31
10. Gubbay SS, Lobascher M, Kingerlee P. A neurological appraisal of autistic children: results of a western Australian survey. Dev MedChild Neurol 1970; 12:422–429.
11. Small JG. EEG and neurophysiological studies of early infantile autism. Biol Psychiatry 1975; 10:385–397
12. Kagan-Kushnir T; Roberts SW; Snead OC. Screening electroencephalograms in autism spectrum disorders: evidence-based guideline. J Child Neurol. 2005; 20(3):197-206 (ISSN: 0883-0738)
13. Spence, S.J.; Schneider, M.T. The role of epilepsy and epileptiform EEGs in autism spectrum disorders. Pediatr. Res. 2009, 65, 599–606
14. Amiet, C.; Gourfinkel-An, I.; Bouzamondo, A.; Tordjman, S.; Baulac, M.; Lechat, P.; Mottron, L.; Cohen, D. Epilepsy in autism is associated with intellectual disability and gender: Evidence from a meta-analysis. Biol. Psychiatry 2008, 64, 577–582
15. Tuchman RF, Rapin I. Regression in pervasive developmental disorders: seizures and epileptiform electroencephalogram correlates. Pediatrics 1997; 99:560–6
16. Parmeggiani A, Barcia G, Posar A, Raimondi E, Santucci M, Scaduto MC. Epilepsy and EEG paroxysmal abnormalities in autism spectrum disorders. Brain and Development 2010; 32:783–9.
17. Rossi PG, Parmeggiani A, Santucci M, Visconti P. Bach V. EEG features and epilepsy in patients with autism. Brain Dev 1995; 17:169–174. [PubMed: 7573755]
18. Tuchman R., Rapin, I. Epilepsy in autism. Lancet Neurol. 2002, 1, 352–358.
19. American Psychiatric Association. In: DSM-IV-TR, editor. Diagnostic and statistical manual of mental disorders (DSMIV-TR). Washington, DC: American Psychiatric Association; 2000.
20. Spencer-Smith MM, Spittle AJ, Lee KJ, Doyle LW, Anderson PJ. (2015). Bayley-III Cognitive and Language Scales in Preterm Children. Pediatrics. 135(5):e1258‐e1265. doi:10.1542/peds.2014-3039
21. Franzen M.D. (2000) The Wechsler Intelligence Scales for Children—the WISC-R, WISC-III, and WPPSI-R. In: Reliability and Validity in Neuropsychological Assessment. Critical Issues in Neuropsychology. Springer, Boston, MA DOI: https://doi.org/10.1007/978-1-4757-3224-5
22. Srivastava, A.K., & Schwartz, C.E. Intellectual disability and autism spectrum disorders: Causal genes and molecular mechanisms. Neuroscience and Biobehavioral Reviews,2014, 46, 161–164….
23. Mizrahi EM. Avoiding the pitfalls of EEG interpretation in childhood epilepsy. Epilepsia 1996, 37(Suppl 1): S41–51.
24. Samra N.M., Ghaffar H.M.A., El-Awady H.A., Soltan M.R. and Moktader R.M.A. Epilepsy and EEG Findings in Children with Autism Spectrum Disorders Autism. Open Access 2017, 7:3 DOI: 10.4172/2165-7890.1000211
25. Ekinci O, Arman AR, Isik U, Bez Y, Berkem M. EEG abnormalities and epilepsy in autistic spectrum disorders: Clinical and familial correlates. Epilepsy Behav 2010, 17: 178-182.
26. Hrdlicka M, Komarek V, Propper L, Kulisek R, Zumrova A, Faladova L, Havlovicova M, Sedlacek Z, Blatny M, Urbanek T . Not EEG abnormalities but epilepsy is associated with autistic regression and mental functioning in childhood autism.Eur Child Adolesc Psychiatry 2004, 13:209–213
27. Akshoomoff N, Farid N, Courchesne E, Haas R. Abnormalities on the neurological examination and EEG in young children with pervasive developmental disorders. J Autism Dev Disord 2007; 37:887–893
28. Gabis L, Pomeroy J, Andriola MR. Autism and epilepsy: cause, consequence,comorbidity, or coincidence? Epilepsy Behav 2005, 7:652–656
29. Olsson I, Steffenburg S, Gillberg C. Epilepsy in autism and autistic like conditions. A population-based study. Arch Neurol 1988, 45:666–668.
30. Galanopoulou A, Vidaurre J, McVicar K. Language and behavioral disturbances associated with epileptiform EEGs. Am J Electroneurodiagnostic Tech 2002, 42:181–234
31. Hughes JR, Melyn M. EEG and seizures in autistic children and adolescents: further findings with therapeutic implications. Clin EEG Neurosci 2005, 36:15–20
32. Reinhold JA, Molloy CA, Manning-Courtney P. Electroencephalogram abnormalities in children with autism spectrum disorders.J Neurosci Nurs. 2005 Jun;37(3):136-8.
33. Lewine J, Andrews R, Chez M. Magnetoencephalographic patterns of epileptiform activity in children with regressive autism spectrum disorders.Pediatr 1999, 104:405–418.
34. Giannotti F, Cortesi F, Cerquiglini A, Miraglia D, Vagnoni C, Sebastiani T, Bernabei P. An investigation of sleep characteristics, EEG abnormalities and epilepsy in developmentally regressed and non-regressed children with autism. J Autism Dev Disord 2008, 38:1888–1897.
35. Eeg-Olofsson O, Petersen I, Sellden U. The development of the electroencephalogram in normal children from the age of 1through 15 years: paroxysmal activity. Neurop¨adiatrie 1971; 2:375–404.
36. Cavazutti GB, Cappella L, Nalin A. Longitudinal study of epileptiform EEG patterns in normal children. Epilepsia 1980; 21:43–55.
37. Amira M. Yousefa, Usama M. Youssefa, Amany El-Shabrawya, Nelly R.A. Abdel Fattaha, Haytham Khedra, Haytham Khedr. EEG abnormalities and severity of symptoms in non-epileptic. Egyptian Journal of Psychiatry 2017, 38(2); P: 59-64
38. Gabis L, Pomeroy J, Andriola MR. Autism and epilepsy: cause, consequence, comorbidity, or coincidence? Epilepsy Behav 2005, 7:652–656. [cross reference]
39. Scott RC, Neville BG. Developmental perspectives on epilepsy. CurrOpin Neurol. 1998; 11:115–118. [PubMed: 9551290]
40. Ballaban-Gil K, Tuchman R. Epilepsy and epileptiform EEG: association with autism and languagedisorders. Ment Retard Dev Disabil Res Rev. 2000; 6:300–308. [PubMed: 11107195]
41. Riikonen R, Amnell G. Psychiatric disorders in children with earlier infantile spasms. Dev Med Child Neurol 1981; 23: 747-60.
42. Alderkamp A. Arends J. The Relative Influence of Epileptic EEG Discharges, Short Nonconvulsive Seizures, Type of Epilepsy on Cognitive Function. Epilepsia 2004, 45 (1):54-63
43. Baird G, Robinson RO, Boyd S, Charman T. Sleep electroencephalograms in young children with autism with and without regression. Dev Med Child Neurol 2006, 48:604–6080
References
1. Samra N.M., Ghaffar H.M.A., El-Awady H.A., Soltan M.R. and Moktader R.M.A. Epilepsy and EEG Findings in Children with Autism Spectrum Disorders Autism. Open Access 2017, 7:3 DOI: 10.4172/2165-7890.1000211
2. Ünal Ö, Özcan Ö, Öner Ö, Akcakin M., Aysev A., Deda G.EEG and MRI findings and their relation with intellectual disability in pervasive developmental disorders. World J Pediatr, 2009 August; 5(3): 196–200. doi:10.1007/s12519-009-0037-y
3. Dawson M, Soulieres I, Gernsbacher MA, Mottron L. The level and nature of autistic intelligence. Psychol Sci, 2007; 18:657– 662.
4. Pacheva I. , Ivanov I. , Yordanova R. , Gaberova K., Galabova F., Panova M. , Petkova A., Timova E. and Sotkova I. Epilepsy in Children with Autistic Spectrum Disorder . Children 2019, 6, 15; doi:10.3390/children6020015…new number www.mdpi.com/journal/children
5. Elkholy N., Ezedin A., Hamdy M., Wafa H.A.E. Electroencephalographic pattern among autistic children and their relatives. Egypt J Psychiatry 2017, 36:150–157
6. Yasuhara A. Correlation between EEG abnormalities and symptoms of autism spectrum disorder (ASD). Brain Dev, 2010, 32: 791-798.
7. Chez MG, Krasne CM, 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
8. 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.
9. Canitano R, Luchetti A, Zappella M. Epilepsy, electroencephalographic abnormalities, and regression in children with autism. J Child Neurol 2005; 20:27–31
10. Gubbay SS, Lobascher M, Kingerlee P. A neurological appraisal of autistic children: results of a western Australian survey. Dev MedChild Neurol 1970; 12:422–429.
11. Small JG. EEG and neurophysiological studies of early infantile autism. Biol Psychiatry 1975; 10:385–397
12. Kagan-Kushnir T; Roberts SW; Snead OC. Screening electroencephalograms in autism spectrum disorders: evidence-based guideline. J Child Neurol. 2005; 20(3):197-206 (ISSN: 0883-0738)
13. Spence, S.J.; Schneider, M.T. The role of epilepsy and epileptiform EEGs in autism spectrum disorders. Pediatr. Res. 2009, 65, 599–606
14. Amiet, C.; Gourfinkel-An, I.; Bouzamondo, A.; Tordjman, S.; Baulac, M.; Lechat, P.; Mottron, L.; Cohen, D. Epilepsy in autism is associated with intellectual disability and gender: Evidence from a meta-analysis. Biol. Psychiatry 2008, 64, 577–582
15. Tuchman RF, Rapin I. Regression in pervasive developmental disorders: seizures and epileptiform electroencephalogram correlates. Pediatrics 1997; 99:560–6
16. Parmeggiani A, Barcia G, Posar A, Raimondi E, Santucci M, Scaduto MC. Epilepsy and EEG paroxysmal abnormalities in autism spectrum disorders. Brain and Development 2010; 32:783–9.
17. Rossi PG, Parmeggiani A, Santucci M, Visconti P. Bach V. EEG features and epilepsy in patients with autism. Brain Dev 1995; 17:169–174. [PubMed: 7573755]
18. Tuchman R., Rapin, I. Epilepsy in autism. Lancet Neurol. 2002, 1, 352–358.
19. American Psychiatric Association. In: DSM-IV-TR, editor. Diagnostic and statistical manual of mental disorders (DSMIV-TR). Washington, DC: American Psychiatric Association; 2000.
20. Spencer-Smith MM, Spittle AJ, Lee KJ, Doyle LW, Anderson PJ. (2015). Bayley-III Cognitive and Language Scales in Preterm Children. Pediatrics. 135(5):e1258‐e1265. doi:10.1542/peds.2014-3039
21. Franzen M.D. (2000) The Wechsler Intelligence Scales for Children—the WISC-R, WISC-III, and WPPSI-R. In: Reliability and Validity in Neuropsychological Assessment. Critical Issues in Neuropsychology. Springer, Boston, MA DOI: https://doi.org/10.1007/978-1-4757-3224-5
22. Srivastava, A.K., & Schwartz, C.E. Intellectual disability and autism spectrum disorders: Causal genes and molecular mechanisms. Neuroscience and Biobehavioral Reviews,2014, 46, 161–164….
23. Mizrahi EM. Avoiding the pitfalls of EEG interpretation in childhood epilepsy. Epilepsia 1996, 37(Suppl 1): S41–51.
24. Samra N.M., Ghaffar H.M.A., El-Awady H.A., Soltan M.R. and Moktader R.M.A. Epilepsy and EEG Findings in Children with Autism Spectrum Disorders Autism. Open Access 2017, 7:3 DOI: 10.4172/2165-7890.1000211
25. Ekinci O, Arman AR, Isik U, Bez Y, Berkem M. EEG abnormalities and epilepsy in autistic spectrum disorders: Clinical and familial correlates. Epilepsy Behav 2010, 17: 178-182.
26. Hrdlicka M, Komarek V, Propper L, Kulisek R, Zumrova A, Faladova L, Havlovicova M, Sedlacek Z, Blatny M, Urbanek T . Not EEG abnormalities but epilepsy is associated with autistic regression and mental functioning in childhood autism.Eur Child Adolesc Psychiatry 2004, 13:209–213
27. Akshoomoff N, Farid N, Courchesne E, Haas R. Abnormalities on the neurological examination and EEG in young children with pervasive developmental disorders. J Autism Dev Disord 2007; 37:887–893
28. Gabis L, Pomeroy J, Andriola MR. Autism and epilepsy: cause, consequence,comorbidity, or coincidence? Epilepsy Behav 2005, 7:652–656
29. Olsson I, Steffenburg S, Gillberg C. Epilepsy in autism and autistic like conditions. A population-based study. Arch Neurol 1988, 45:666–668.
30. Galanopoulou A, Vidaurre J, McVicar K. Language and behavioral disturbances associated with epileptiform EEGs. Am J Electroneurodiagnostic Tech 2002, 42:181–234
31. Hughes JR, Melyn M. EEG and seizures in autistic children and adolescents: further findings with therapeutic implications. Clin EEG Neurosci 2005, 36:15–20
32. Reinhold JA, Molloy CA, Manning-Courtney P. Electroencephalogram abnormalities in children with autism spectrum disorders.J Neurosci Nurs. 2005 Jun;37(3):136-8.
33. Lewine J, Andrews R, Chez M. Magnetoencephalographic patterns of epileptiform activity in children with regressive autism spectrum disorders.Pediatr 1999, 104:405–418.
34. Giannotti F, Cortesi F, Cerquiglini A, Miraglia D, Vagnoni C, Sebastiani T, Bernabei P. An investigation of sleep characteristics, EEG abnormalities and epilepsy in developmentally regressed and non-regressed children with autism. J Autism Dev Disord 2008, 38:1888–1897.
35. Eeg-Olofsson O, Petersen I, Sellden U. The development of the electroencephalogram in normal children from the age of 1through 15 years: paroxysmal activity. Neurop¨adiatrie 1971; 2:375–404.
36. Cavazutti GB, Cappella L, Nalin A. Longitudinal study of epileptiform EEG patterns in normal children. Epilepsia 1980; 21:43–55.
37. Amira M. Yousefa, Usama M. Youssefa, Amany El-Shabrawya, Nelly R.A. Abdel Fattaha, Haytham Khedra, Haytham Khedr. EEG abnormalities and severity of symptoms in non-epileptic. Egyptian Journal of Psychiatry 2017, 38(2); P: 59-64
38. Gabis L, Pomeroy J, Andriola MR. Autism and epilepsy: cause, consequence, comorbidity, or coincidence? Epilepsy Behav 2005, 7:652–656. [cross reference]
39. Scott RC, Neville BG. Developmental perspectives on epilepsy. CurrOpin Neurol. 1998; 11:115–118. [PubMed: 9551290]
40. Ballaban-Gil K, Tuchman R. Epilepsy and epileptiform EEG: association with autism and languagedisorders. Ment Retard Dev Disabil Res Rev. 2000; 6:300–308. [PubMed: 11107195]
41. Riikonen R, Amnell G. Psychiatric disorders in children with earlier infantile spasms. Dev Med Child Neurol 1981; 23: 747-60.
42. Alderkamp A. Arends J. The Relative Influence of Epileptic EEG Discharges, Short Nonconvulsive Seizures, Type of Epilepsy on Cognitive Function. Epilepsia 2004, 45 (1):54-63
43. Baird G, Robinson RO, Boyd S, Charman T. Sleep electroencephalograms in young children with autism with and without regression. Dev Med Child Neurol 2006, 48:604–6080
2. Ünal Ö, Özcan Ö, Öner Ö, Akcakin M., Aysev A., Deda G.EEG and MRI findings and their relation with intellectual disability in pervasive developmental disorders. World J Pediatr, 2009 August; 5(3): 196–200. doi:10.1007/s12519-009-0037-y
3. Dawson M, Soulieres I, Gernsbacher MA, Mottron L. The level and nature of autistic intelligence. Psychol Sci, 2007; 18:657– 662.
4. Pacheva I. , Ivanov I. , Yordanova R. , Gaberova K., Galabova F., Panova M. , Petkova A., Timova E. and Sotkova I. Epilepsy in Children with Autistic Spectrum Disorder . Children 2019, 6, 15; doi:10.3390/children6020015…new number www.mdpi.com/journal/children
5. Elkholy N., Ezedin A., Hamdy M., Wafa H.A.E. Electroencephalographic pattern among autistic children and their relatives. Egypt J Psychiatry 2017, 36:150–157
6. Yasuhara A. Correlation between EEG abnormalities and symptoms of autism spectrum disorder (ASD). Brain Dev, 2010, 32: 791-798.
7. Chez MG, Krasne CM, 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
8. 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.
9. Canitano R, Luchetti A, Zappella M. Epilepsy, electroencephalographic abnormalities, and regression in children with autism. J Child Neurol 2005; 20:27–31
10. Gubbay SS, Lobascher M, Kingerlee P. A neurological appraisal of autistic children: results of a western Australian survey. Dev MedChild Neurol 1970; 12:422–429.
11. Small JG. EEG and neurophysiological studies of early infantile autism. Biol Psychiatry 1975; 10:385–397
12. Kagan-Kushnir T; Roberts SW; Snead OC. Screening electroencephalograms in autism spectrum disorders: evidence-based guideline. J Child Neurol. 2005; 20(3):197-206 (ISSN: 0883-0738)
13. Spence, S.J.; Schneider, M.T. The role of epilepsy and epileptiform EEGs in autism spectrum disorders. Pediatr. Res. 2009, 65, 599–606
14. Amiet, C.; Gourfinkel-An, I.; Bouzamondo, A.; Tordjman, S.; Baulac, M.; Lechat, P.; Mottron, L.; Cohen, D. Epilepsy in autism is associated with intellectual disability and gender: Evidence from a meta-analysis. Biol. Psychiatry 2008, 64, 577–582
15. Tuchman RF, Rapin I. Regression in pervasive developmental disorders: seizures and epileptiform electroencephalogram correlates. Pediatrics 1997; 99:560–6
16. Parmeggiani A, Barcia G, Posar A, Raimondi E, Santucci M, Scaduto MC. Epilepsy and EEG paroxysmal abnormalities in autism spectrum disorders. Brain and Development 2010; 32:783–9.
17. Rossi PG, Parmeggiani A, Santucci M, Visconti P. Bach V. EEG features and epilepsy in patients with autism. Brain Dev 1995; 17:169–174. [PubMed: 7573755]
18. Tuchman R., Rapin, I. Epilepsy in autism. Lancet Neurol. 2002, 1, 352–358.
19. American Psychiatric Association. In: DSM-IV-TR, editor. Diagnostic and statistical manual of mental disorders (DSMIV-TR). Washington, DC: American Psychiatric Association; 2000.
20. Spencer-Smith MM, Spittle AJ, Lee KJ, Doyle LW, Anderson PJ. (2015). Bayley-III Cognitive and Language Scales in Preterm Children. Pediatrics. 135(5):e1258‐e1265. doi:10.1542/peds.2014-3039
21. Franzen M.D. (2000) The Wechsler Intelligence Scales for Children—the WISC-R, WISC-III, and WPPSI-R. In: Reliability and Validity in Neuropsychological Assessment. Critical Issues in Neuropsychology. Springer, Boston, MA DOI: https://doi.org/10.1007/978-1-4757-3224-5
22. Srivastava, A.K., & Schwartz, C.E. Intellectual disability and autism spectrum disorders: Causal genes and molecular mechanisms. Neuroscience and Biobehavioral Reviews,2014, 46, 161–164….
23. Mizrahi EM. Avoiding the pitfalls of EEG interpretation in childhood epilepsy. Epilepsia 1996, 37(Suppl 1): S41–51.
24. Samra N.M., Ghaffar H.M.A., El-Awady H.A., Soltan M.R. and Moktader R.M.A. Epilepsy and EEG Findings in Children with Autism Spectrum Disorders Autism. Open Access 2017, 7:3 DOI: 10.4172/2165-7890.1000211
25. Ekinci O, Arman AR, Isik U, Bez Y, Berkem M. EEG abnormalities and epilepsy in autistic spectrum disorders: Clinical and familial correlates. Epilepsy Behav 2010, 17: 178-182.
26. Hrdlicka M, Komarek V, Propper L, Kulisek R, Zumrova A, Faladova L, Havlovicova M, Sedlacek Z, Blatny M, Urbanek T . Not EEG abnormalities but epilepsy is associated with autistic regression and mental functioning in childhood autism.Eur Child Adolesc Psychiatry 2004, 13:209–213
27. Akshoomoff N, Farid N, Courchesne E, Haas R. Abnormalities on the neurological examination and EEG in young children with pervasive developmental disorders. J Autism Dev Disord 2007; 37:887–893
28. Gabis L, Pomeroy J, Andriola MR. Autism and epilepsy: cause, consequence,comorbidity, or coincidence? Epilepsy Behav 2005, 7:652–656
29. Olsson I, Steffenburg S, Gillberg C. Epilepsy in autism and autistic like conditions. A population-based study. Arch Neurol 1988, 45:666–668.
30. Galanopoulou A, Vidaurre J, McVicar K. Language and behavioral disturbances associated with epileptiform EEGs. Am J Electroneurodiagnostic Tech 2002, 42:181–234
31. Hughes JR, Melyn M. EEG and seizures in autistic children and adolescents: further findings with therapeutic implications. Clin EEG Neurosci 2005, 36:15–20
32. Reinhold JA, Molloy CA, Manning-Courtney P. Electroencephalogram abnormalities in children with autism spectrum disorders.J Neurosci Nurs. 2005 Jun;37(3):136-8.
33. Lewine J, Andrews R, Chez M. Magnetoencephalographic patterns of epileptiform activity in children with regressive autism spectrum disorders.Pediatr 1999, 104:405–418.
34. Giannotti F, Cortesi F, Cerquiglini A, Miraglia D, Vagnoni C, Sebastiani T, Bernabei P. An investigation of sleep characteristics, EEG abnormalities and epilepsy in developmentally regressed and non-regressed children with autism. J Autism Dev Disord 2008, 38:1888–1897.
35. Eeg-Olofsson O, Petersen I, Sellden U. The development of the electroencephalogram in normal children from the age of 1through 15 years: paroxysmal activity. Neurop¨adiatrie 1971; 2:375–404.
36. Cavazutti GB, Cappella L, Nalin A. Longitudinal study of epileptiform EEG patterns in normal children. Epilepsia 1980; 21:43–55.
37. Amira M. Yousefa, Usama M. Youssefa, Amany El-Shabrawya, Nelly R.A. Abdel Fattaha, Haytham Khedra, Haytham Khedr. EEG abnormalities and severity of symptoms in non-epileptic. Egyptian Journal of Psychiatry 2017, 38(2); P: 59-64
38. Gabis L, Pomeroy J, Andriola MR. Autism and epilepsy: cause, consequence, comorbidity, or coincidence? Epilepsy Behav 2005, 7:652–656. [cross reference]
39. Scott RC, Neville BG. Developmental perspectives on epilepsy. CurrOpin Neurol. 1998; 11:115–118. [PubMed: 9551290]
40. Ballaban-Gil K, Tuchman R. Epilepsy and epileptiform EEG: association with autism and languagedisorders. Ment Retard Dev Disabil Res Rev. 2000; 6:300–308. [PubMed: 11107195]
41. Riikonen R, Amnell G. Psychiatric disorders in children with earlier infantile spasms. Dev Med Child Neurol 1981; 23: 747-60.
42. Alderkamp A. Arends J. The Relative Influence of Epileptic EEG Discharges, Short Nonconvulsive Seizures, Type of Epilepsy on Cognitive Function. Epilepsia 2004, 45 (1):54-63
43. Baird G, Robinson RO, Boyd S, Charman T. Sleep electroencephalograms in young children with autism with and without regression. Dev Med Child Neurol 2006, 48:604–6080