DOI QR코드

DOI QR Code

Advanced neuroimaging techniques for evaluating pediatric epilepsy

  • Lee, Yun Jeong (Department of Pediatrics, Kyungpook National University Hospital, School of Medicine, Kyungpook National University)
  • Received : 2019.07.28
  • Accepted : 2019.11.06
  • Published : 2020.03.15

Abstract

Accurate localization of the seizure onset zone is important for better seizure outcomes and preventing deficits following epilepsy surgery. Recent advances in neuroimaging techniques have increased our understanding of the underlying etiology and improved our ability to noninvasively identify the seizure onset zone. Using epilepsy-specific magnetic resonance imaging (MRI) protocols, structural MRI allows better detection of the seizure onset zone, particularly when it is interpreted by experienced neuroradiologists. Ultra-high-field imaging and postprocessing analysis with automated machine learning algorithms can detect subtle structural abnormalities in MRI-negative patients. Tractography derived from diffusion tensor imaging can delineate white matter connections associated with epilepsy or eloquent function, thus, preventing deficits after epilepsy surgery. Arterial spin-labeling perfusion MRI, simultaneous electroencephalography (EEG)-functional MRI (fMRI), and magnetoencephalography (MEG) are noinvasive imaging modalities that can be used to localize the epileptogenic foci and assist in planning epilepsy surgery with positron emission tomography, ictal single-photon emission computed tomography, and intracranial EEG monitoring. MEG and fMRI can localize and lateralize the area of the cortex that is essential for language, motor, and memory function and identify its relationship with planned surgical resection sites to reduce the risk of neurological impairments. These advanced structural and functional imaging modalities can be combined with postprocessing methods to better understand the epileptic network and obtain valuable clinical information for predicting long-term outcomes in pediatric epilepsy.

Keywords

References

  1. Hauser WA. The prevalence and incidence of convulsive disorders in children. Epilepsia 1994;35 Suppl 2:S1-6. https://doi.org/10.1111/j.1528-1157.1994.tb05932.x
  2. Wirrell EC, Grossardt BR, Wong-Kisiel LC, Nickels KC. Incidence and classification of new-onset epilepsy and epilepsy syndromes in children in Olmsted County, Minnesota from 1980 to 2004: a population-based study. Epilepsy Res 2011;95:110-8. https://doi.org/10.1016/j.eplepsyres.2011.03.009
  3. Sillanpaa M, Schmidt D. Natural history of treated childhood-onset epilepsy: prospective, long-term population-based study. Brain 2006;129(Pt 3):617-24. https://doi.org/10.1093/brain/awh726
  4. Semah F, Picot MC, Adam C, Broglin D, Arzimanoglou A, Bazin B, et al. Is the underlying cause of epilepsy a major prognostic factor for recurrence? Neurology 1998;51:1256-62. https://doi.org/10.1212/WNL.51.5.1256
  5. Garcia Gracia C, Yardi R, Kattan MW, Nair D, Gupta A, Najm I, et al. Seizure freedom score: a new simple method to predict success of epilepsy surgery. Epilepsia 2015;56:359-65. https://doi.org/10.1111/epi.12892
  6. Bronen RA, Fulbright RK, Spencer DD, Spencer SS, Kim JH, Lange RC, et al. Refractory epilepsy: comparison of MR imaging, CT, and histopathologic findings in 117 patients. Radiology 1996;201:97-105. https://doi.org/10.1148/radiology.201.1.8816528
  7. King MA, Newton MR, Jackson GD, Fitt GJ, Mitchell LA, Silvapulle MJ, et al. Epileptology of the first-seizure presentation: a clinical, electroencephalographic, and magnetic resonance imaging study of 300 consecutive patients. Lancet 1998;352:1007-11. https://doi.org/10.1016/S0140-6736(98)03543-0
  8. Ho K, Lawn N, Bynevelt M, Lee J, Dunne J. Neuroimaging of first-ever seizure: Contribution of MRI if CT is normal. Neurol Clin Pract 2013;3:398-403. https://doi.org/10.1212/CPJ.0b013e3182a78f25
  9. Resta M, Palma M, Dicuonzo F, Spagnolo P, Specchio LM, Laneve A, et al. Imaging studies in partial epilepsy in children and adolescents. Epilepsia 1994;35:1187-93. https://doi.org/10.1111/j.1528-1157.1994.tb01787.x
  10. Bien CG, Szinay M, Wagner J, Clusmann H, Becker AJ, Urbach H. Characteristics and surgical outcomes of patients with refractory magnetic resonance imaging-negative epilepsies. Arch Neurol 2009;66:1491-9. https://doi.org/10.1001/archneurol.2009.283
  11. Von Oertzen J, Urbach H, Jungbluth S, Kurthen M, Reuber M, Fernandez G, et al. Standard magnetic resonance imaging is inadequate for patients with refractory focal epilepsy. J Neurol Neurosurg Psychiatry 2002;73:643-7. https://doi.org/10.1136/jnnp.73.6.643
  12. Wellmer J, Quesada CM, Rothe L, Elger CE, Bien CG, Urbach H. Proposal for a magnetic resonance imaging protocol for the detection of epileptogenic lesions at early outpatient stages. Epilepsia 2013;54:1977-87. https://doi.org/10.1111/epi.12375
  13. Cendes F. Neuroimaging in investigation of patients with epilepsy. Continuum (Minneap Minn) 2013;19(3 Epilepsy):623-42. https://doi.org/10.1212/01.CON.0000431379.29065.d3
  14. Gaillard WD, Chiron C, Cross JH, Harvey AS, Kuzniecky R, Hertz-Pannier L, et al. Guidelines for imaging infants and children with recentonset epilepsy. Epilepsia 2009;50:2147-53. https://doi.org/10.1111/j.1528-1167.2009.02075.x
  15. Montenegro MA, Li LM, Guerreiro MM, Guerreiro CA, Cendes F. Focal cortical dysplasia: improving diagnosis and localization with magnetic resonance imaging multiplanar and curvilinear reconstruction. J Neuroimaging 2002;12:224-30. https://doi.org/10.1111/j.1552-6569.2002.tb00125.x
  16. Martin P, Bender B, Focke NK. Post-processing of structural MRI for individualized diagnostics. Quant Imaging Med Surg 2015;5:188-203. https://doi.org/10.3978/j.issn.2223-4292.2015.01.10
  17. Vezina LG. MRI-negative epilepsy: protocols to optimize lesion detection. Epilepsia 2011;52 Suppl 4:25-7. https://doi.org/10.1111/j.1528-1167.2011.03147.x
  18. Yagishita A, Arai N, Maehara T, Shimizu H, Tokumaru AM, Oda M. Focal cortical dysplasia: appearance on MR images. Radiology 1997;203:553-9. https://doi.org/10.1148/radiology.203.2.9114120
  19. Daghistani R, Widjaja E. Role of MRI in patient selection for surgical treatment of intractable epilepsy in infancy. Brain Dev 2013;35:697-705. https://doi.org/10.1016/j.braindev.2013.03.009
  20. Eltze CM, Chong WK, Bhate S, Harding B, Neville BG, Cross JH. Taylortype focal cortical dysplasia in infants: some MRI lesions almost disappear with maturation of myelination. Epilepsia 2005;46:1988-92. https://doi.org/10.1111/j.1528-1167.2005.00339.x
  21. Nguyen DK, Rochette E, Leroux JM, Beaudoin G, Cossette P, Lassonde M, et al. Value of 3.0 T MR imaging in refractory partial epilepsy and negative 1.5 T MRI. Seizure 2010;19:475-8. https://doi.org/10.1016/j.seizure.2010.07.002
  22. Phal PM, Usmanov A, Nesbit GM, Anderson JC, Spencer D, Wang P, et al. Qualitative comparison of 3-T and 1.5-T MRI in the evaluation of epilepsy. AJR Am J Roentgenol 2008;191:890-5. https://doi.org/10.2214/AJR.07.3933
  23. Zijlmans M, de Kort GA, Witkamp TD, Huiskamp GM, Seppenwoolde JH, van Huffelen AC, 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;30:256-62. https://doi.org/10.1002/jmri.21811
  24. Knake S, Triantafyllou C, Wald LL, Wiggins G, Kirk GP, Larsson PG, et al. 3T phased array MRI improves the presurgical evaluation in focal epilepsies: a prospective study. Neurology 2005;65:1026-31. https://doi.org/10.1212/01.wnl.0000179355.04481.3c
  25. De Ciantis A, Barkovich AJ, Cosottini M, Barba C, Montanaro D, Costagli M, et al. Ultra-high-field MR imaging in polymicrogyria and epilepsy. AJNR Am J Neuroradiol 2015;36:309-16. https://doi.org/10.3174/ajnr.A4116
  26. Oh BH, Moon HC, Baek HM, Lee YJ, Kim SW, Jeon YJ, et al. Comparison of 7T and 3T MRI in patients with moyamoya disease. Magn Reson Imaging 2017;37:134-8. https://doi.org/10.1016/j.mri.2016.11.019
  27. Coras R, Milesi G, Zucca I, Mastropietro A, Scotti A, Figini M, et al. 7T MRI features in control human hippocampus and hippocampal sclerosis: an ex vivo study with histologic correlations. Epilepsia 2014;55:2003-16. https://doi.org/10.1111/epi.12828
  28. Lupo JM, Li Y, Hess CP, Nelson SJ. Advances in ultra-high field MRI for the clinical management of patients with brain tumors. Curr Opin Neurol 2011;24:605-15. https://doi.org/10.1097/WCO.0b013e32834cd495
  29. De Cocker LJ, Lindenholz A, Zwanenburg JJ, van der Kolk AG, Zwartbol M, Luijten PR, et al. Clinical vascular imaging in the brain at 7T. Neuroimage 2018;168:452-8. https://doi.org/10.1016/j.neuroimage.2016.11.044
  30. Tallantyre EC, Dixon JE, Donaldson I, Owens T, Morgan PS, Morris PG, et al. Ultra-high-field imaging distinguishes MS lesions from asymptomatic white matter lesions. Neurology 2011;76:534-9. https://doi.org/10.1212/WNL.0b013e31820b7630
  31. De Ciantis A, Barba C, Tassi L, Cosottini M, Tosetti M, Costagli M, et al. 7T MRI in focal epilepsy with unrevealing conventional field strength imaging. Epilepsia 2016;57:445-54. https://doi.org/10.1111/epi.13313
  32. Veersema TJ, van Eijsden P, Gosselaar PH, Hendrikse J, Zwanenburg JJ, Spliet WG, et al. 7 tesla T2*-weighted MRI as a tool to improve detection of focal cortical dysplasia. Epileptic Disord 2016;18:315-23. https://doi.org/10.1684/epd.2016.0838
  33. Balchandani P, Naidich TP. Ultra-high-field MR neuroimaging. AJNR Am J Neuroradiol 2015;36:1204-15. https://doi.org/10.3174/ajnr.A4180
  34. Braakman HM, Vaessen MJ, Jansen JF, Debeij-van Hall MH, de Louw A, Hofman PA, et al. Pediatric frontal lobe epilepsy: white matter abnormalities and cognitive impairment. Acta Neurol Scand 2014;129:252-62. https://doi.org/10.1111/ane.12183
  35. Concha L, Beaulieu C, Collins DL, Gross DW. White-matter diffusion abnormalities in temporal-lobe epilepsy with and without mesial temporal sclerosis. J Neurol Neurosurg Psychiatry 2009;80:312-9. https://doi.org/10.1136/jnnp.2007.139287
  36. Winston GP, Yogarajah M, Symms MR, McEvoy AW, Micallef C, Duncan JS. Diffusion tensor imaging tractography to visualize the relationship of the optic radiation to epileptogenic lesions prior to neurosurgery. Epilepsia 2011;52:1430-8. https://doi.org/10.1111/j.1528-1167.2011.03088.x
  37. Jeong JW, Asano E, Juhasz C, Chugani HT. Quantification of primary motor pathways using diffusion MRI tractography and its application to predict postoperative motor deficits in children with focal epilepsy. Hum Brain Mapp 2014;35:3216-26. https://doi.org/10.1002/hbm.22396
  38. Jeong JW, Asano E, Juhasz C, Chugani HT. Localization of specific language pathways using diffusion-weighted imaging tractography for presurgical planning of children with intractable epilepsy. Epilepsia 2015;56:49-57. https://doi.org/10.1111/epi.12863
  39. Hutchings F, Han CE, Keller SS, Weber B, Taylor PN, Kaiser M. Predicting surgery targets in temporal lobe epilepsy through structural connectome based simulations. PLoS Comput Biol 2015;11:e1004642. https://doi.org/10.1371/journal.pcbi.1004642
  40. Essayed WI, Zhang F, Unadkat P, Cosgrove GR, Golby AJ, O'Donnell LJ. White matter tractography for neurosurgical planning: a topographybased review of the current state of the art. Neuroimage Clin 2017;15:659-72. https://doi.org/10.1016/j.nicl.2017.06.011
  41. 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;108:336-9. https://doi.org/10.1016/j.eplepsyres.2013.11.004
  42. Bruggemann JM, Wilke M, Som SS, Bye AM, Bleasel A, Lawson JA. Voxel-based morphometry in the detection of dysplasia and neoplasia in childhood epilepsy: combined grey/white matter analysis augments detection. Epilepsy Res 2007;77:93-101. https://doi.org/10.1016/j.eplepsyres.2007.09.004
  43. Colliot O, Bernasconi N, Khalili N, Antel SB, Naessens V, Bernasconi A. Individual voxel-based analysis of gray matter in focal cortical dysplasia. Neuroimage 2006;29:162-71. https://doi.org/10.1016/j.neuroimage.2005.07.021
  44. Bonilha L, Montenegro MA, Rorden C, Castellano G, Guerreiro MM, Cendes F, et al. Voxel-based morphometry reveals excess gray matter concentration in patients with focal cortical dysplasia. Epilepsia 2006;47:908-15. https://doi.org/10.1111/j.1528-1167.2006.00548.x
  45. Wagner J, Weber B, Urbach H, Elger CE, Huppertz HJ. Morphometric MRI analysis improves detection of focal cortical dysplasia type II. Brain 2011;134(Pt 10):2844-54. https://doi.org/10.1093/brain/awr204
  46. Besson P, Bernasconi N, Colliot O, Evans A, Bernasconi A. Surface-based texture and morphological analysis detects subtle cortical dysplasia. Med Image Comput Comput Assist Interv 2008;11(Pt 1):645-52.
  47. Briellmann RS, Syngeniotis A, Fleming S, Kalnins RM, Abbott DF, Jackson GD. Increased anterior temporal lobe T2 times in cases of hippocampal sclerosis: a multi-echo T2 relaxometry study at 3 T. AJNR Am J Neuroradiol 2004;25:389-94.
  48. Winston GP, Vos SB, Burdett JL, Cardoso MJ, Ourselin S, Duncan JS. Automated T2 relaxometry of the hippocampus for temporal lobe epilepsy. Epilepsia 2017;58:1645-52. https://doi.org/10.1111/epi.13843
  49. Wang I, Alexopoulos A. MRI postprocessing in presurgical evaluation. Curr Opin Neurol 2016;29:168-74. https://doi.org/10.1097/WCO.0000000000000305
  50. Hong SJ, Kim H, Schrader D, Bernasconi N, Bernhardt BC, Bernasconi A. Automated detection of cortical dysplasia type II in MRI-negative epilepsy. Neurology 2014;83:48-55. https://doi.org/10.1212/WNL.0000000000000543
  51. Jin B, Krishnan B, Adler S, Wagstyl K, Hu W, Jones S, et al. Automated detection of focal cortical dysplasia type II with surface-based magnetic resonance imaging postprocessing and machine learning. Epilepsia 2018;59:982-92. https://doi.org/10.1111/epi.14064
  52. Burneo JG, Poon R, Kellett S, Snead OC. The utility of positron emission tomography in epilepsy. Can J Neurol Sci 2015;42:360-71. https://doi.org/10.1017/cjn.2015.279
  53. Vinton AB, Carne R, Hicks RJ, Desmond PM, Kilpatrick C, Kaye AH, et al. The extent of resection of FDG-PET hypometabolism relates to outcome of temporal lobectomy. Brain 2007;130(Pt2):548-60. https://doi.org/10.1093/brain/awl232
  54. Knowlton RC, Elgavish RA, Bartolucci A, Ojha B, Limdi N, Blount J, et al. Functional imaging: II. Prediction of epilepsy surgery outcome. Ann Neurol 2008;64:35-41. https://doi.org/10.1002/ana.21419
  55. Tomas J, Pittau F, Hammers A, Bouvard S, Picard F, Vargas MI, et al. The predictive value of hypometabolism in focal epilepsy: a prospective study in surgical candidates. Eur J Nucl Med Mol Imaging 2019;46:1806-16. https://doi.org/10.1007/s00259-019-04356-x
  56. Haller S, Zaharchuk G, Thomas DL, Lovblad KO, Barkhof F, Golay X. Arterial spin labeling perfusion of the brain: emerging clinical applications. Radiology 2016;281:337-56. https://doi.org/10.1148/radiol.2016150789
  57. Pendse N, Wissmeyer M, Altrichter S, Vargas M, Delavelle J, Viallon M, et al. Interictal arterial spin-labeling MRI perfusion in intractable epilepsy. J Neuroradiol 2010;37:60-3. https://doi.org/10.1016/j.neurad.2009.05.006
  58. Blauwblomme T, Boddaert N, Chemaly N, Chiron C, Pages M, Varlet P, et al. Arterial Spin Labeling MRI: a step forward in non-invasive delineation of focal cortical dysplasia in children. Epilepsy Res 2014;108:1932-9. https://doi.org/10.1016/j.eplepsyres.2014.09.029
  59. Lee SM, Kwon S, Lee YJ. Diagnostic usefulness of arterial spin labeling in MR negative children with new onset seizures. Seizure 2019;65:151-8. https://doi.org/10.1016/j.seizure.2019.01.024
  60. Sepeta LN, Berl MM, Wilke M, You X, Mehta M, Xu B, et al. Agedependent mesial temporal lobe lateralization in language fMRI. Epilepsia 2016;57:122-30. https://doi.org/10.1111/epi.13258
  61. Collinge S, Prendergast G, Mayers ST, Marshall D, Siddell P, Neilly E, et al. Pre-surgical mapping of eloquent cortex for paediatric epilepsy surgery candidates: Evidence from a review of advanced functional neuroimaging. Seizure 2017:136-46.
  62. Lee MH, Smyser CD, Shimony JS. Resting-state fMRI: a review of methods and clinical applications. AJNR Am J Neuroradiol 2013;34:1866-72. https://doi.org/10.3174/ajnr.A3263
  63. Vadivelu S, Wolf VL, Bollo RJ, Wilfong A, Curry DJ. Resting-state functional MRI in pediatric epilepsy surgery. Pediatr Neurosurg 2013;49:261-73. https://doi.org/10.1159/000363605
  64. Moeller F, Stephani U, Siniatchkin M. Simultaneous EEG and fMRI recordings (EEG-fMRI) in children with epilepsy. Epilepsia 2013;54:971-82. https://doi.org/10.1111/epi.12197
  65. Nordli D, Xiao F, Zhou D. Real-time effects of centrotemporal spikes on cognition in rolandic epilepsy: An EEG-fMRI study. Neurology 2016;87:552. https://doi.org/10.1212/01.wnl.0000490409.57774.19
  66. Negishi M, Martuzzi R, Novotny EJ, Spencer DD, Constable RT. Functional MRI connectivity as a predictor of the surgical outcome of epilepsy. Epilepsia 2011;52:1733-40. https://doi.org/10.1111/j.1528-1167.2011.03191.x
  67. Oishi M, Otsubo H, Kameyama S, Morota N, Masuda H, Kitayama M, et al. Epileptic spikes: magnetoencephalography versus simultaneous electrocorticography. Epilepsia 2002;43:1390-5. https://doi.org/10.1046/j.1528-1157.2002.10702.x
  68. Knowlton RC, Elgavish RA, Limdi N, Bartolucci A, Ojha B, Blount J, et al. Functional imaging: I. Relative predictive value of intracranial electroencephalography. Ann Neurol 2008;64:25-34. https://doi.org/10.1002/ana.21389
  69. Stefan H, Hummel C, Scheler G, Genow A, Druschky K, Tilz C, et al. Magnetic brain source imaging of focal epileptic activity: a synopsis of 455 cases. Brain 2003;126(Pt11):2396-405. https://doi.org/10.1093/brain/awg239
  70. Aydin U, Vorwerk J, Dumpelmann M, Kupper P, Kugel H, Heers M, et al. Combined EEG/MEG can outperform single modality EEG or MEG source reconstruction in presurgical epilepsy diagnosis. PLoS One 2015;10:e0118753. https://doi.org/10.1371/journal.pone.0118753
  71. Bercovici E, Pang EW, Sharma R, Mohamed IS, Imai K, Fujimoto A, et al. Somatosensory-evoked fields on magnetoencephalography for epilepsy infants younger than 4 years with total intravenous anesthesia. Clin Neurophysiol 2008;119:1328-34. https://doi.org/10.1016/j.clinph.2008.02.018

Cited by

  1. Guideline for advanced neuroimaging in pediatric epilepsy vol.63, pp.3, 2020, https://doi.org/10.3345/cep.2019.01403
  2. Magnetic Resonance Imaging Findings in Childhood Epilepsy at a Tertiary Hospital in Kenya vol.12, 2020, https://doi.org/10.3389/fneur.2021.623960