Journal of Pediatric Epilepsy 2021; 10(02): 065-080
DOI: 10.1055/s-0040-1722301
Review Article

Neuroimaging of Childhood Epilepsy: Focal versus Generalized Epilepsy

Reza Assadsangabi
1   Department of Neuroradiology, Radiology, University of California Davis School of Medicine, Sacramento, California, United States
,
Arzu Ozturk
1   Department of Neuroradiology, Radiology, University of California Davis School of Medicine, Sacramento, California, United States
,
Trishna Kantamneni
2   Department of Neurology, University of California Davis School of Medicine, Sacramento, California, United States
,
Nazarin Azizi
1   Department of Neuroradiology, Radiology, University of California Davis School of Medicine, Sacramento, California, United States
,
Shailesh M. Asaikar
3   Child & Adolescent Neurology Consultants, Sacramento, California, United States
,
Lotfi Hacein-Bey
1   Department of Neuroradiology, Radiology, University of California Davis School of Medicine, Sacramento, California, United States
› Author Affiliations
Funding None.

Abstract

Neuroimaging plays an increasingly crucial role in delineating the pathophysiology, and guiding the evaluation, management and monitoring of epilepsy. Imaging contributes to adequately categorizing seizure/epilepsy types in complex clinical situations by demonstrating anatomical and functional changes associated with seizure activity. This article reviews the current status of multimodality neuroimaging in the pediatric population, including focal lesions which may result in focal epileptic findings, focal structural abnormalities that may manifest as generalized epileptiform discharges, and generalized epilepsy without evidence of detectable focal abnormalities.



Publication History

Received: 16 November 2020

Accepted: 01 November 2020

Article published online:
02 February 2021

© 2021. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Aaberg KM, Gunnes N, Bakken IJ. et al. Incidence and prevalence of childhood epilepsy: a nationwide cohort study. Pediatrics 2017; 139 (05) e20163908
  • 2 Scheffer IE, Berkovic S, Capovilla G. et al. ILAE classification of the epilepsies: position paper of the ILAE commission for classification and terminology. Epilepsia 2017; 58 (04) 512-521
  • 3 Aktekin B. Up-to-date critical review of the classification of epilepsies and epileptic seizures. Noro Psikiyatri Arsivi 2015; 52 (02) 109-110
  • 4 Parrini E, Conti V, Dobyns WB, Guerrini R. Genetic basis of brain malformations. Mol Syndromol 2016; 7 (04) 220-233
  • 5 Jayakar P, Gaillard WD, Tripathi M, Libenson MH, Mathern GW, Cross JH. Task Force for Paediatric Epilepsy Surgery, Commission for Paediatrics, and the Diagnostic Commission of the International League Against Epilepsy. Diagnostic test utilization in evaluation for resective epilepsy surgery in children. Epilepsia 2014; 55 (04) 507-518
  • 6 Téllez-Zenteno JF, Hernández Ronquillo L, Moien-Afshari F, Wiebe S. Surgical outcomes in lesional and non-lesional epilepsy: a systematic review and meta-analysis. Epilepsy Res 2010; 89 (2-3): 310-318
  • 7 Von Oertzen J, Urbach H, Jungbluth S. et al. Standard magnetic resonance imaging is inadequate for patients with refractory focal epilepsy. J Neurol Neurosurg Psychiatry 2002; 73 (06) 643-647
  • 8 Craven IJ, Griffiths PD, Bhattacharyya D. et al. 3.0 T MRI of 2000 consecutive patients with localisation-related epilepsy. Br J Radiol 2012; 85 (1017): 1236-1242
  • 9 Zijlmans M, de Kort GA, Witkamp TD. et al. 3T versus 1.5T phased-array MRI in the presurgical work-up of patients with partial epilepsy of uncertain focus. J Magn Reson Imaging 2009; 30 (02) 256-262
  • 10 Obusez EC, Lowe M, Oh S-H. et al. 7T MR of intracranial pathology: preliminary observations and comparisons to 3T and 1.5T. Neuroimage 2018; 168: 459-476
  • 11 Coras R, Milesi G, Zucca I. et al. 7T MRI features in control human hippocampus and hippocampal sclerosis: an ex vivo study with histologic correlations. Epilepsia 2014; 55 (12) 2003-2016
  • 12 Kelley SA, Robinson S, Crone NE, Soares BP. Bottom-of-sulcus focal cortical dysplasia presenting as epilepsia partialis continua multimodality characterization including 7T MRI. Childs Nerv Syst 2018; 34 (06) 1267-1269
  • 13 Pradhan S, Bonekamp S, Gillen JS. et al. Comparison of single voxel brain MRS AT 3T and 7T using 32-channel head coils. Magn Reson Imaging 2015; 33 (08) 1013-1018
  • 14 Henning A. Proton and multinuclear magnetic resonance spectroscopy in the human brain at ultra-high field strength: a review. Neuroimage 2018; 168: 181-198
  • 15 Pan JW, Duckrow RB, Gerrard J. et al. 7T MR spectroscopic imaging in the localization of surgical epilepsy. Epilepsia 2013; 54 (09) 1668-1678
  • 16 Knowlton RC. Can magnetoencephalography aid epilepsy surgery?. Epilepsy Curr 2008; 8 (01) 1-5
  • 17 Aydin Ü, Vorwerk J, Dümpelmann M. et al. Combined EEG/MEG can outperform single modality EEG or MEG source reconstruction in presurgical epilepsy diagnosis. PLoS One 2015; 10 (03) e0118753-e0118753
  • 18 Giraud A-L, Lorenzi C, Ashburner J. et al. Representation of the temporal envelope of sounds in the human brain. J Neurophysiol 2000; 84 (03) 1588-1598
  • 19 Nissen IA, van Klink NEC, Zijlmans M, Stam CJ, Hillebrand A. Brain areas with epileptic high frequency oscillations are functionally isolated in MEG virtual electrode networks. Clin Neurophysiol 2016; 127 (07) 2581-2591
  • 20 Englot DJ, Nagarajan SS, Imber BS. et al. Epileptogenic zone localization using magnetoencephalography predicts seizure freedom in epilepsy surgery. Epilepsia 2015; 56 (06) 949-958
  • 21 Sarikaya I. PET studies in epilepsy. Am J Nucl Med Mol Imaging 2015; 5 (05) 416-430
  • 22 Duncan JS, Winston GP, Koepp MJ, Ourselin S. Brain imaging in the assessment for epilepsy surgery. Lancet Neurol 2016; 15 (04) 420-433
  • 23 Wolf RL, Alsop DC, Levy-Reis I. et al. Detection of mesial temporal lobe hypoperfusion in patients with temporal lobe epilepsy by use of arterial spin labeled perfusion MR imaging. AJNR Am J Neuroradiol 2001; 22 (07) 1334-1341
  • 24 Szmuda M, Szmuda T, Springer J. et al. Diffusion tensor tractography imaging in pediatric epilepsy: a systematic review. Neurol Neurochir Pol 2016; 50 (01) 1-6
  • 25 Widjaja E, Geibprasert S, Otsubo H, Snead III OC, Mahmoodabadi SZ. Diffusion tensor imaging assessment of the epileptogenic zone in children with localization-related epilepsy. AJNR Am J Neuroradiol 2011; 32 (10) 1789-1794
  • 26 Krsek P, Hajek M, Dezortova M. et al. (1)H MR spectroscopic imaging in patients with MRI-negative extratemporal epilepsy: correlation with ictal onset zone and histopathology. Eur Radiol 2007; 17 (08) 2126-2135
  • 27 Lee SK, Lee SY, Kim K-K, Hong K-S, Lee D-S, Chung C-K. Surgical outcome and prognostic factors of cryptogenic neocortical epilepsy. Ann Neurol 2005; 58 (04) 525-532
  • 28 Zentner J, Hufnagel A, Wolf HK. et al. Surgical treatment of temporal lobe epilepsy: clinical, radiological, and histopathological findings in 178 patients. J Neurol Neurosurg Psychiatry 1995; 58 (06) 666-673
  • 29 Winston GP, Micallef C, Symms MR, Alexander DC, Duncan JS, Zhang H. Advanced diffusion imaging sequences could aid assessing patients with focal cortical dysplasia and epilepsy. Epilepsy Res 2014; 108 (02) 336-339
  • 30 Woermann FG, Jokeit H, Luerding R. et al. Language lateralization by Wada test and fMRI in 100 patients with epilepsy. Neurology 2003; 61 (05) 699-701
  • 31 Shurtleff H, Warner M, Poliakov A. et al. Functional magnetic resonance imaging for presurgical evaluation of very young pediatric patients with epilepsy. J Neurosurg Pediatr 2010; 5 (05) 500-506
  • 32 Pasquier B, Péoc'H M, Fabre-Bocquentin B. et al. Surgical pathology of drug-resistant partial epilepsy. A 10-year-experience with a series of 327 consecutive resections. Epileptic Disord 2002; 4 (02) 99-119
  • 33 Wirrell EC, Wong-Kisiel LC-L, Mandrekar J, Nickels KC. What predicts enduring intractability in children who appear medically intractable in the first 2 years after diagnosis?. Epilepsia 2013; 54 (06) 1056-1064
  • 34 Desikan RS, Barkovich AJ. Malformations of cortical development. Ann Neurol 2016; 80 (06) 797-810
  • 35 Barkovich AJ, Dobyns WB, Guerrini R. Malformations of cortical development and epilepsy. Cold Spring Harb Perspect Med 2015; 5 (05) a022392
  • 36 Colombo N, Tassi L, Deleo F. et al. Focal cortical dysplasia type IIa and IIb: MRI aspects in 118 cases proven by histopathology. Neuroradiology 2012; 54 (10) 1065-1077
  • 37 Assadsangabi R, Baldassano S, Gibson A. et al. Update on adult epilepsy: what neuroradiologists should know. Neurographics 2020; 10 (03) 103-124
  • 38 Blümcke I, Thom M, Aronica E. et al. The clinicopathologic spectrum of focal cortical dysplasias: a consensus classification proposed by an ad hoc Task Force of the ILAE Diagnostic Methods Commission. Epilepsia 2011; 52 (01) 158-174
  • 39 Jansen AC, Robitaille Y, Honavar M. et al. The histopathology of polymicrogyria: a series of 71 brain autopsy studies. Dev Med Child Neurol 2016; 58 (01) 39-48
  • 40 Leventer RJ, Jansen A, Pilz DT. et al. Clinical and imaging heterogeneity of polymicrogyria: a study of 328 patients. Brain 2010; 133 (Pt 5): 1415-1427
  • 41 Barkovich AJ. Current concepts of polymicrogyria. Neuroradiology 2010; 52 (06) 479-487
  • 42 González G, Vedolin L, Barry B, Poduri A, Walsh C, Barkovich AJ. Location of periventricular nodular heterotopia is related to the malformation phenotype on MRI. AJNR Am J Neuroradiol 2013; 34 (04) 877-883
  • 43 Nabavizadeh SA, Vossough A. High-resolution 3-T MR imaging of the temporal part of the caudate tail in children. Childs Nerv Syst 2014; 30 (03) 485-489
  • 44 Barkovich AJ, Guerrini R, Battaglia G. et al. Band heterotopia: correlation of outcome with magnetic resonance imaging parameters. Ann Neurol 1994; 36 (04) 609-617
  • 45 Shuper A, Yaniv I, Michowitz S. et al. Epilepsy associated with pediatric brain tumors: the neuro-oncologic perspective. Pediatr Neurol 2003; 29 (03) 232-235
  • 46 Rastogi S, Lee C, Salamon N. Neuroimaging in pediatric epilepsy: a multimodality approach. Radiographics 2008; 28 (04) 1079-1095
  • 47 Cersósimo R, Flesler S, Bartuluchi M, Soprano AM, Pomata H, Caraballo R. Mesial temporal lobe epilepsy with hippocampal sclerosis: study of 42 children. Seizure 2011; 20 (02) 131-137
  • 48 Suresh S, Sweet J, Fastenau PS, Lüders H, Landazuri P, Miller J. Temporal lobe epilepsy in patients with nonlesional MRI and normal memory: an SEEG study. J Neurosurg 2015; 123 (06) 1368-1374
  • 49 Josephson CB, Rosenow F, Al-Shahi Salman R. Intracranial vascular malformations and epilepsy. Semin Neurol 2015; 35 (03) 223-234
  • 50 Vezzani A, Fujinami RS, White HS. et al. Infections, inflammation and epilepsy. Acta Neuropathol 2016; 131 (02) 211-234
  • 51 Wanigasinghe J, Reid SM, Mackay MT, Reddihough DS, Harvey AS, Freeman JL. Epilepsy in hemiplegic cerebral palsy due to perinatal arterial ischaemic stroke. Dev Med Child Neurol 2010; 52 (11) 1021-1027
  • 52 Bien CG, Granata T, Antozzi C. et al. Pathogenesis, diagnosis and treatment of Rasmussen encephalitis: a European consensus statement. Brain 2005; 128 (Pt 3): 454-471
  • 53 Varadkar S, Bien CG, Kruse CA. et al. Rasmussen's encephalitis: clinical features, pathobiology, and treatment advances. Lancet Neurol 2014; 13 (02) 195-205
  • 54 Shirley MD, Tang H, Gallione CJ. et al. Sturge-Weber syndrome and port-wine stains caused by somatic mutation in GNAQ. N Engl J Med 2013; 368 (21) 1971-1979
  • 55 Nabbout R, Juhász C. Sturge-Weber syndrome. Handb Clin Neurol 2013; 111: 315-321
  • 56 De la Torre AJ, Luat AF, Juhász C. et al. A multidisciplinary consensus for clinical care and research needs for Sturge-Weber syndrome. Pediatr Neurol 2018; 84: 11-20
  • 57 Arzimanoglou A, Aicardi J. The epilepsy of Sturge-Weber syndrome: clinical features and treatment in 23 patients. Acta Neurol Scand Suppl 1992; 140: 18-22
  • 58 Au KS, Williams AT, Roach ES. et al. Genotype/phenotype correlation in 325 individuals referred for a diagnosis of tuberous sclerosis complex in the United States. Genet Med 2007; 9 (02) 88-100
  • 59 Manoukian SB, Kowal DJ. Comprehensive imaging manifestations of tuberous sclerosis. AJR Am J Roentgenol 2015; 204 (05) 933-943
  • 60 Wu JY, Salamon N, Kirsch HE. et al. Noninvasive testing, early surgery, and seizure freedom in tuberous sclerosis complex. Neurology 2010; 74 (05) 392-398
  • 61 Bernhardt BC, Rozen DA, Worsley KJ, Evans AC, Bernasconi N, Bernasconi A. Thalamo-cortical network pathology in idiopathic generalized epilepsy: insights from MRI-based morphometric correlation analysis. Neuroimage 2009; 46 (02) 373-381
  • 62 Cavanna AE, Monaco F. Brain mechanisms of altered conscious states during epileptic seizures. Nat Rev Neurol 2009; 5 (05) 267-276
  • 63 Woermann FG, Sisodiya SM, Free SL, Duncan JS. Quantitative MRI in patients with idiopathic generalized epilepsy. Evidence of widespread cerebral structural changes. Brain 1998; 121 (Pt 9): 1661-1667
  • 64 Wang Z, Zhang Z, Jiao Q. et al. Impairments of thalamic nuclei in idiopathic generalized epilepsy revealed by a study combining morphological and functional connectivity MRI. PLoS One 2012; 7 (07) e39701-e39701
  • 65 Carney PW, Masterton RAJ, Harvey AS, Scheffer IE, Berkovic SF, Jackson GD. The core network in absence epilepsy. Differences in cortical and thalamic BOLD response. Neurology 2010; 75 (10) 904-911
  • 66 Achard S, Salvador R, Whitcher B, Suckling J, Bullmore E. A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. J Neurosci 2006; 26 (01) 63-72
  • 67 Lv H, Wang Z, Tong E. et al. Resting-state functional MRI: everything that nonexperts have always wanted to know. AJNR Am J Neuroradiol 2018; 39 (08) 1390-1399
  • 68 Ji G-J, Zhang Z, Xu Q. et al. Identifying corticothalamic network epicenters in patients with idiopathic generalized epilepsy. AJNR Am J Neuroradiol 2015; 36 (08) 1494-1500
  • 69 Yang T, Guo Z, Luo C. et al. White matter impairment in the basal ganglia-thalamocortical circuit of drug-naïve childhood absence epilepsy. Epilepsy Res 2012; 99 (03) 267-273
  • 70 Zhang Z, Liao W, Chen H. et al. Altered functional-structural coupling of large-scale brain networks in idiopathic generalized epilepsy. Brain 2011; 134 (Pt 10): 2912-2928
  • 71 Wyllie E, Lachhwani DK, Gupta A. et al. Successful surgery for epilepsy due to early brain lesions despite generalized EEG findings. Neurology 2007; 69 (04) 389-397
  • 72 Garzon E, Gupta A, Bingaman W, Sakamoto AC, Lüders H. Paradoxical ictal EEG lateralization in children with unilateral encephaloclastic lesions. Epileptic Disord 2009; 11 (03) 215-221
  • 73 Gupta A, Chirla A, Wyllie E, Lachhwani DK, Kotagal P, Bingaman WE. Pediatric epilepsy surgery in focal lesions and generalized electroencephalogram abnormalities. Pediatr Neurol 2007; 37 (01) 8-15
  • 74 Shukla G, Kazutaka J, Gupta A. et al. Magnetoencephalographic identification of epileptic focus in children with generalized electroencephalographic (EEG) features but focal imaging abnormalities. J Child Neurol 2017; 32 (12) 981-995
  • 75 Chang EF, Nagarajan SS, Mantle M, Barbaro NM, Kirsch HE. Magnetic source imaging for the surgical evaluation of electroencephalography-confirmed secondary bilateral synchrony in intractable epilepsy. J Neurosurg 2009; 111 (06) 1248-1256
  • 76 Gelisse P, Corda D, Raybaud C, Dravet C, Bureau M, Genton P. Abnormal neuroimaging in patients with benign epilepsy with centrotemporal spikes. Epilepsia 2003; 44 (03) 372-378
  • 77 Gaillard WD, Chiron C, Cross JH. et al; ILAE, Committee for Neuroimaging, Subcommittee for Pediatric. Guidelines for imaging infants and children with recent-onset epilepsy. Epilepsia 2009; 50 (09) 2147-2153
  • 78 Coryell J, Gaillard WD, Shellhaas RA. et al. Neuroimaging of early life epilepsy. Pediatrics 2018; 142 (03) e20180672
  • 79 Hwang ST, Stevens SJ, Fu AX, Proteasa SV. Intractable generalized epilepsy: therapeutic approaches. Curr Neurol Neurosci Rep 2019; 19 (04) 16
  • 80 Kang JW, Eom S, Hong W. et al. Long-term outcome of resective epilepsy surgery in patients with Lennox-Gastaut syndrome. Pediatrics 2018; 142 (04) e20180449
  • 81 Freeman JL, Coleman LT, Wellard RM. et al. MR imaging and spectroscopic study of epileptogenic hypothalamic hamartomas: analysis of 72 cases. AJNR Am J Neuroradiol 2004; 25 (03) 450-462
  • 82 Alkawadri R, So NK, Van Ness PC, Alexopoulos AV. Cingulate epilepsy: report of 3 electroclinical subtypes with surgical outcomes. JAMA Neurol 2013; 70 (08) 995-1002
  • 83 Alkawadri R, Mickey BE, Madden CJ, Van Ness PC. Cingulate gyrus epilepsy: clinical and behavioral aspects, with surgical outcomes. Arch Neurol 2011; 68 (03) 381-385
  • 84 Hirtz D, Ashwal S, Berg A. et al. Practice parameter: evaluating a first nonfebrile seizure in children: report of the quality standards subcommittee of the American Academy of Neurology, The Child Neurology Society, and The American Epilepsy Society. Neurology 2000; 55 (05) 616-623
  • 85 Sharma S, Riviello JJ, Harper MB, Baskin MN. The role of emergent neuroimaging in children with new-onset afebrile seizures. Pediatrics 2003; 111 (01) 1-5
  • 86 Kalnin AJ, Fastenau PS, deGrauw TJ. et al. Magnetic resonance imaging findings in children with a first recognized seizure. Pediatr Neurol 2008; 39 (06) 404-414
  • 87 Hsieh DT, Chang T, Tsuchida TN. et al. New-onset afebrile seizures in infants: role of neuroimaging. Neurology 2010; 74 (02) 150-156
  • 88 Kadom N, Trofimova A, Vezina GL. Utility of magnetization transfer T1 imaging in children with seizures. AJNR Am J Neuroradiol 2013; 34 (04) 895-898