Seminars in Pediatric Neurology
Volume 14, Issue 4 , Pages 173-180 , December 2007

Cognitive and Magnetic Resonance Volumetric Abnormalities in New-Onset Pediatric Epilepsy

  • Bruce P. Hermann, PhD

      Affiliations

    • Department of Neurology, University of Wisconsin School of Medicine and Public Health, Madison, WI.
    • Corresponding Author InformationAddress reprint requests to Bruce Hermann, PhD, Department of Neurology, University of Wisconsin, 600 N Highland Ave, Madison WI 53792.
    • ,
  • Jana Jones, PhD

      Affiliations

    • Department of Neurology, University of Wisconsin School of Medicine and Public Health, Madison, WI.
    • ,
  • Raj Sheth, MD

      Affiliations

    • Department of Neurology, University of Wisconsin School of Medicine and Public Health, Madison, WI.
    • ,
  • Michael Seidenberg, PhD

      Affiliations

    • Department of Psychology, Rosalind Franklin University of Medicine and Science, North Chicago, IL.

References 

  1. Elger CE, Helmstaedter C, Kurthen M. Chronic epilepsy and cognition. Lancet Neurol. 2004;3:663–672
  2. Saling MM, Berkovic SF, O’Shea MF, et al. Lateralization of verbal memory and unilateral hippocampal sclerosis: Evidence of task-specific effects. J Clin Exp Neuropsychol. 1993;15:608–618
  3. Aldenkamp A, Arends J. The relative influence of epileptic EEG discharges, short nonconvulsive seizures, and type of epilepsy on cognitive function. Epilepsia. 2004;45:54–63
  4. Dodrill CB. Neuropsychological effects of seizures. Epilepsy Behav. 2004;5(suppl 1):S21–S24
  5. Helmstaedter C, Kurthen M. Memory and epilepsy: Characteristics, course, and influence of drugs and surgery. Curr Opin Neurol. 2001;14:211–216
  6. Jones-Gotman M. Clinical neuropsychology and neocortical epilepsies. Adv Neurol. 2000;84:457–462
  7. Jokeit H, Ebner A. Effects of chronic epilepsy on intellectual functions. Prog Brain Res. 2002;135:455–463
  8. Koop JI, Fastenau PS, Dunn DW, et al. Neuropsychological correlates of electroencephalograms in children with epilepsy. Epilepsy Res. 2005;64:49–62
  9. Marsh ED, Brooks-Kayal AR, Porter BE. Seizures and antiepileptic drugs: Does exposure alter normal brain development?. Epilepsia. 2006;47:1999–2010
  10. Lassonde M, Sauerwein HC, Jambaque I, et al. Neuropsychology of childhood epilepsy: Pre- and postsurgical assessment. Epileptic Disord. 2000;2:3–13
  11. Nolan MA, Redoblado MA, Lah S, et al. Intelligence in childhood epilepsy syndromes. Epilepsy Res. 2003;53:139–150
  12. Nolan MA, Redoblado MA, Lah S, et al. Memory function in childhood epilepsy syndromes. J Paediatr Child Health. 2004;40:20–27
  13. Riva D, Avanzini G, Franceschetti S, et al. Unilateral frontal lobe epilepsy affects executive functions in children. Neurol Sci. 2005;26:263–270
  14. Hommet C, Sauerwein HC, De Toffol B, et al. Idiopathic epileptic syndromes and cognition. Neurosci Biobehav Rev. 2006;30:85–96
  15. Sart ZH, Demirbilek V, Korkmaz B, et al. The consequences of idiopathic partial epilepsies in relation to neuropsychological functioning: A closer look at the associated mathematical disability. Epileptic Disord. 2006;8:24–31
  16. Henkin Y, Sadeh M, Kivity S, et al. Cognitive function in idiopathic generalized epilepsy of childhood. Dev Med Child Neurol. 2005;47:126–132
  17. Pitkanen A, Sutula TP. Is epilepsy a progressive disorder? (Prospects for new therapeutic approaches in temporal-lobe epilepsy). Lancet Neurol. 2002;1:173–181
  18. Fox JT. The response of epileptic children to mental and educational tests. Br J Med Psychol. 1924;4:235–248
  19. Dikmen S, Matthews CG, Harley JP. The effect of early versus late onset of major motor epilepsy upon cognitive-intellectual performance. Epilepsia. 1975;16:73–81
  20. Dikmen S, Matthews CG, Harley JP. Effect of early versus late onset of major motor epilepsy on cognitive-intellectual performance: Further considerations. Epilepsia. 1977;18:31–36
  21. Dodrill CB, Matthews CG. The role of neuropsychology in the assessment and treatment of persons with epilepsy. Am Psychol. 1992;47:1139–1142
  22. Lennox WG. Epilepsy and Related Disorders. Boston, MA: Little, Brown and Co; 1960;
  23. Glosser G, Cole LC, French JA, et al. Predictors of intellectual performance in adults with intractable temporal lobe epilepsy. J Int Neuropsychol Soc. 1997;3:252–259
  24. O’Leary DS, Seidenberg M, Berent S, et al. Effects of age of onset of tonic-clonic seizures on neuropsychological performance in children. Epilepsia. 1981;22:197–204
  25. O’Leary DS, Lovell MR, Sackellares JC, et al. Effects of age of onset of partial and generalized seizures on neuropsychological performance in children. J Nerv Ment Dis. 1983;171:624–629
  26. Schoenfeld J, Seidenberg M, Woodard A, et al. Neuropsychological and behavioral status of children with complex partial seizures. Dev Med Child Neurol. 1999;41:724–731
  27. Cormack F, Cross JH, Isaacs E, et al. The development of intellectual abilities in pediatric temporal lobe epilepsy. Epilepsia. 2007;48:201–204
  28. Hermann BP, Seidenberg M, Schoenfeld J, et al. Neuropsychological characteristics of the syndrome of mesial temporal lobe epilepsy. Arch Neurol. 1997;54:369–376
  29. Engel J. Surgery for seizures. N Engl J Med. 1996;334:647–652
  30. Jack CR, Sharbrough FW, Cascino GD, et al. Magnetic resonance image-based hippocampal volumetry: Correlation with outcome after temporal lobectomy. Ann Neurol. 1992;31:138–146
  31. Quigg M, Bertram EH, Jackson T, et al. Volumetric magnetic resonance imaging evidence of bilateral hippocampal atrophy in mesial temporal lobe epilepsy. Epilepsia. 1997;38:588–594
  32. Woermann FG, Barker GJ, Birnie KD, et al. Regional changes in hippocampal T2 relaxation and volume: A quantitative magnetic resonance imaging study of hippocampal sclerosis. J Neurol Neurosurg Psychiatry. 1998;65:656–664
  33. Tasch E, Cendes F, Li LM, et al. Neuroimaging evidence of progressive neuronal loss and dysfunction in temporal lobe epilepsy. Ann Neurol. 1999;45:568–576
  34. Kalviainen R, Salmenpera T, Partanen K, et al. MRI volumetry and T2 relaxometry of the amygdala in newly diagnosed and chronic temporal lobe epilepsy. Epilepsy Res. 1997;28:39–50
  35. Bernasconi N, Bernasconi A, Andermann F, et al. Entorhinal cortex in temporal lobe epilepsy: A quantitative MRI study. Neurology. 1999;52:1870–1876
  36. Kuzniecky R, Bilir E, Gilliam F, et al. Quantitative MRI in temporal lobe epilepsy: Evidence for fornix atrophy. Neurology. 1999;53:496–501
  37. DeCarli C, Hatta J, Fazilat S, et al. Extratemporal atrophy in patients with complex partial seizures of left temporal origin. Ann Neurol. 1998;43:41–45
  38. Breier JI, Leonard CM, Bauer RM, et al. Quantified volumes of temporal lobe structures in patients with epilepsy. J Neuroimaging. 1996;6:108–114
  39. Marsh L, Morrell MJ, Shear PK, et al. Cortical and hippocampal volume deficits in temporal lobe epilepsy. Epilepsia. 1997;38:576–587
  40. Lee JW, Andermann F, Dubeau F, et al. Morphometric analysis of the temporal lobe in temporal lobe epilepsy. Epilepsia. 1998;39:727–736
  41. Moran NF, Lemieux L, Kitchen ND, et al. Extrahippocampal temporal lobe atrophy in temporal lobe epilepsy and mesial temporal sclerosis. Brain. 2001;124:167–175
  42. Sandok EK, O’Brien TJ, Jack CR, et al. Significance of cerebellar atrophy in intractable temporal lobe epilepsy: A quantitative MRI study. Epilepsia. 2000;41:1315–1320
  43. Sisodiya SM, Moran N, Free SL, et al. Correlation of widespread preoperative magnetic resonance imaging changes with unsuccessful surgery for hippocampal sclerosis. Ann Neurol. 1997;41:490–496
  44. Wasterlain CG, Plum F. Vulnerability of developing rat brain to electroconvulsive seizures. Arch Neurol. 1973;29:38–45
  45. Dwyer BE, Wasterlain CG. Electroconvulsive seizures in the immature rat adversely affect myelin accumulation. Exp Neurol. 1982;78:616–628
  46. Wasterlain CG, Thompson KW, Kornblum H, et al. Long-term effects of recurrent seizures on the developing brain. In:  Nehlig A,  Motte J,  Moshe SL, et al. editor. Childhood Epilepsies and Brain Development. London: John Libbey & Company Ltd; 1999;p. 237–254
  47. Roeschl-Heils A, Bledowski C, Elger CE, et al. Neuropsychological functioning among 32 patients with temporal lobe epilepsy and their discordant siblings. Epilepsia. 2002;43:185
  48. Smith ML, Elliott IM, Lach L. Cognitive skills in children with intractable epilepsy: Comparison of surgical and nonsurgical candidates. Epilepsia. 2002;43:631–637
  49. Germano E, Gagliano A, Magazu A, et al. Benign childhood epilepsy with occipital paroxysms: Neuropsychological findings. Epilepsy Res. 2005;64:137–150
  50. Farwell JR, Dodrill CB, Batzel LW. Neuropsychological abilities of children with epilepsy. Epilepsia. 1985;26:395–400
  51. Bourgeois BF, Prensky AL, Palkes HS, et al. Intelligence in epilepsy: A prospective study in children. Ann Neurol. 1983;14:438–444
  52. Oostrom KJ, Smeets-Schouten A, Kruitwagen CL, et al. Not only a matter of epilepsy: Early problems of cognition and behavior in children with “epilepsy only”—A prospective, longitudinal, controlled study starting at diagnosis. Pediatrics. 2003;112:1338–1344
  53. Kolk A, Beilmann A, Tomberg T, et al. Neurocognitive development of children with congenital unilateral brain lesion and epilepsy. Brain Dev. 2001;23:88–96
  54. Stores G, Williams PL, Styles E, et al. Psychological effects of sodium valproate and carbamazepine in epilepsy. Arch Dis Child. 1992;67:1330–1337
  55. Williams J, Bates S, Griebel ML, et al. Does short-term antiepileptic drug treatment in children result in cognitive or behavioral changes?. Epilepsia. 1998;39:1064–1069
  56. Berg AT, Smith SN, Frobish D, et al. Special education needs of children with newly diagnosed epilepsy. Dev Med Child Neurol. 2005;47:749–753
  57. McNelis AM, Johnson CS, Huberty TJ, et al. Factors associated with academic achievement in children with recent-onset seizures. Seizure. 2005;14:331–339
  58. Cendes F. Progressive hippocampal and extrahippocampal atrophy in drug resistant epilepsy. Curr Opin Neurol. 2005;18:173–177
  59. Bernasconi A. Quantitative MR imaging of the neocortex. Neuroimaging Clin N Am. 2004;14:425–436
  60. Koepp MJ, Duncan JS. Epilepsy Curr Opin Neurol. 2004;17:467–474
  61. Kuzniecky RI, Knowlton RC. Neuroimaging of epilepsy. Semin Neurol. 2002;22:279–288
  62. Baxendale SA, van Paesschen W, Thompson PJ, et al. The relationship between quantitative MRI and neuropsychological functioning in temporal lobe epilepsy. Epilepsia. 1998;39:158–166
  63. Baxendale SA, Sisodiya SM, Thompson PJ, et al. Disproportion in the distribution of gray and white matter: Neuropsychological correlates. Neurology. 1999;52:248–252
  64. Martin R, Dowler R, Gilliam F, et al. Cognitive consequences of coexisting temporal lobe developmental malformations and hippocampal sclerosis. Neurology. 1999;53:709–715
  65. Burneo JG, Bilir E, Faught E, et al. Significance of fornix atrophy in temporal lobe epilepsy surgery outcome. Arch Neurol. 2003;60:1238–1242
  66. Dow C, Seidenberg M, Hermann B. Relationship between information processing speed in temporal lobe epilepsy and white matter volume. Epilepsy Behav. 2004;5:919–925
  67. Hermann B, Seidenberg M, Sears L, et al. Cerebellar atrophy in temporal lobe epilepsy affects procedural memory. Neurology. 2004;63:2129–2131
  68. Griffith HR, Pyzalski RW, Seidenberg M, et al. Memory relationships between MRI volumes and resting PET metabolism of medial temporal lobe structures. Epilepsy Behav. 2004;5:669–676
  69. Seidenberg M, Geary E, Hermann B. Investigating temporal lobe contribution to confrontation naming using MRI quantitative volumetrics. J Int Neuropsychol Soc. 2005;11:358–366
  70. Lawson JA, Cook MJ, Bleasel AF, et al. Quantitative MRI in outpatient childhood epilepsy. Epilepsia. 1997;38:1289–1293
  71. Lawson JA, Nguyen W, Bleasel AF, et al. ILAE-defined epilepsy syndromes in children: Correlation with quantitative MRI. Epilepsia. 1998;39:1345–1349
  72. Lawson JA, Vogrin S, Bleasel AF, et al. Predictors of hippocampal, cerebral, and cerebellar volume reduction in childhood epilepsy. Epilepsia. 2000;41:1540–1545
  73. Lawson JA, Vogrin S, Bleasel AF, et al. Cerebral and cerebellar volume reduction in children with intractable epilepsy. Epilepsia. 2000;41:1456–1462
  74. Lawson JA, Cook MJ, Vogrin S, et al. Clinical EEG and quantitative MRI differences in pediatric frontal and temporal lobe epilepsy. Neurology. 2002;58:723–729
  75. Cormack F, Gadian DG, Vargha-Khadem F, et al. Extra-hippocampal grey matter density abnormalities in paediatric mesial temporal sclerosis. Neuroimage. 2005;27:635–643
  76. Woermann FG, Free SL, Koepp MJ, et al. Voxel-by-voxel comparison of automatically segmented cerebral gray matter–A rater-independent comparison of structural MRI in patients with epilepsy. Neuroimage. 1999;10:373–384
  77. Keller SS, Mackay CE, Barrick TR, et al. Voxel-based morphometric comparison of hippocampal and extrahippocampal abnormalities in patients with left and right hippocampal atrophy. Neuroimage. 2002;16:23–31
  78. Keller SS, Wieshmann UC, Mackay CE, et al. Voxel based morphometry of grey matter abnormalities in patients with medically intractable temporal lobe epilepsy: Effects of side of seizure onset and epilepsy duration. J Neurol Neurosurg Psychiatry. 2002;73:648–655
  79. McMillan AB, Hermann BP, Johnson SC, et al. Voxel-based morphometry of unilateral temporal lobe epilepsy reveals abnormalities in cerebral white matter. Neuroimage. 2004;23:167–174
  80. Bonilha L, Rorden C, Castellano G, et al. Voxel-based morphometry reveals gray matter network atrophy in refractory medial temporal lobe epilepsy. Arch Neurol. 2004;61:1379–1384
  81. Bonilha L, Rorden C, Castellano G, et al. Voxel-based morphometry of the thalamus in patients with refractory medial temporal lobe epilepsy. Neuroimage. 2005;25:1016–1021
  82. Byars AW, deGrauw TJ, Johnson CS, et al. The association of MRI findings and neuropsychological functioning after the first recognized seizure. Epilepsia. 2007;48:1067–1074
  83. Andreasen NC, Rajarethinam R, Cizadlo T, et al. Automatic atlas-based volume estimation of human brain regions from MR images. J Comput Assist Tomogr. 1996;20:98–106
  84. Harris G, Andreasen NC, Cizadlo T, et al. Improving tissue classification in MRI: A three-dimensional multispectral discriminant analysis method with automated training class selection. J Comput Assist Tomogr. 1999;23:144–154
  85. Magnotta VA, Heckel D, Andreasen NC, et al. Measurement of brain structures with artificial neural networks: Two- and three-dimensional applications. Radiology. 1999;211:781–790
  86. Magnotta VA, Harris G, Andreasen NC, et al. Structural MR image processing using the BRAINS2 toolbox. Comput Med Imaging Graph. 2002;26:251–264
  87. Hermann B, Jones J, Sheth R, et al. Children with new-onset epilepsy: neuropsychological status and brain structure. Brain. 2006;129:2609–2619
  88. Fastenau PS, Shen J, Dunn DW, et al. Neuropsychological predictors of academic underachievement in pediatric epilepsy: Moderating roles of demographic, seizure, and psychosocial variables. Epilepsia. 2004;45:1261–1272
  89. Cortez MA, Perez Velazquez JL, Snead OC. Animal models of epilepsy and progressive effects of seizures. Adv Neurol. 2006;97:293–304
  90. Paus T, Zijdenbos A, Worsley K, et al. Structural maturation of neural pathways in children and adolescents: In vivo study. Science. 1999;283:1908–1911
  91. Giedd JN, Blumenthal J, Jeffries NO, et al. Brain development during childhood and adolescence: A longitudinal MRI study. Nat Neurosci. 1999;2:861–863
  92. Sowell ER, Peterson BS, Thompson PM, et al. Mapping cortical change across the human life span. Nat Neurosci. 2003;6:309–315
  93. Sowell ER, Thompson PM, Leonard CM, et al. Longitudinal mapping of cortical thickness and brain growth in normal children. J Neurosci. 2004;24:8223–8231
  94. Gogtay N, Giedd JN, Lusk L, et al. Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci U S A. 2004;101:8174–8179
  95. Wilke M, Krageloh-Mann I, Holland SK. Global and local development of gray and white matter volume in normal children and adolescents. Exp Brain Res. 2006;178:296–307
  96. Lenroot RK, Giedd JN. Brain development in children and adolescents: Insights from anatomical magnetic resonance imaging. Neurosci Biobehav Rev. 2006;30:718–729
  97. Hermann BP, Seidenberg M, Bell B. The neurodevelopmental impact of childhood onset temporal lobe epilepsy on brain structure and function and the risk of progressive cognitive effects. Prog Brain Res. 2002;135:429–438
  98. Helmstaedter C, Kurthen M, Lux S, et al. Chronic epilepsy and cognition: A longitudinal study in temporal lobe epilepsy. Ann Neurol. 2003;54:425–432
  99. Sillanpaa M, Jalava M, Kaleva O, et al. Long-term prognosis of seizures with onset in childhood. N Engl J Med. 1998;338:1715–1722
  100. Camfield C, Camfield P, Smith B, et al. Biologic factors as predictors of social outcome of epilepsy in intellectually normal children: A population-based study. J Pediatr. 1993;122:869–873
  101. Austin JK, Harezlak J, Dunn DW, et al. Behavior problems in children before first recognized seizures. Pediatrics. 2001;107:115–122
  102. Dunn DW, Harezlak J, Ambrosius WT, et al. Teacher assessment of behavior in children with new-onset seizures. Seizure. 2002;11:169–175
  103. Hesdorffer DC, Ludvigsson P, Olafsson E, et al. ADHD as a risk factor for incident unprovoked seizures and epilepsy in children. Arch Gen Psychiatry. 2004;61:731–736
  104. Jones JE, Watson R, Sheth R, et al. Psychiatric comorbidity in children with new onset epilepsy. Dev Med Child Neurol. 2007;49:493–497
  105. Hesdorffer DC, Hauser WA, Annegers JF, et al. Major depression is a risk factor for seizures in older adults. Ann Neurol. 2000;47:246–249
  106. Hesdorffer DC, Hauser WA, Olafsson E, et al. Depression and suicide attempt as risk factors for incident unprovoked seizures. Ann Neurol. 2006;59:35–41

 Supported by NIH grant no. RO1 44351.

PII: S1071-9091(07)00056-3

doi: 10.1016/j.spen.2007.08.003

Seminars in Pediatric Neurology
Volume 14, Issue 4 , Pages 173-180 , December 2007

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