The utility of arterial spin labeling in the presurgical evaluation of poorly defined focal epilepsy in children

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  • 1 McConnell Brain Imaging Center, Montreal Neurological Institute, McGill University, Montréal;
  • 2 Philips Canada, MRI Research Department, Montréal; and Departments of
  • 3 Adult and Pediatric Pathology,
  • 4 Pediatric Neurosurgery,
  • 5 Pediatric Radiology, and
  • 6 Neonatology, McGill University Health Network, Montréal, Quebec, Canada
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OBJECTIVE

The authors sought to assess the utility of arterial spin labeling (ASL) perfusion 3T-MRI for the presurgical evaluation of poorly defined focal epilepsy in pediatric patients.

METHODS

Pseudocontinuous ASL perfusion 3T-MRI was performed in 25 consecutive children with poorly defined focal epilepsy. ASL perfusion abnormalities were detected qualitatively by visual inspection and quantitatively by calculating asymmetry index (AI) maps and significant z-score cluster maps based on successfully operated cases. ASL results were prospectively compared to scalp EEG, structural 3T-MRI, FDG-PET, ictal/interictal SPECT, magnetoencephalography (MEG), and intracranial recording results, as well as the final surgically proven epileptogenic zone (EZ) in operated patients who had at least 1 year of good (Engel class I/II) seizure outcome and positive histopathology results.

RESULTS

Qualitative ASL perfusion abnormalities were found in 17/25 cases (68%), specifically in 17/20 MRI-positive cases (85.0%) and in none of the 5 MRI-negative cases. ASL was concordant with localizing scalp EEG findings in 66.7%, structural 3T-MRI in 90%, FDG-PET in 75%, ictal/interictal SPECT in 62.5%, and MEG in 75% of cases, and with intracranial recording results in 40% of cases. Eleven patients underwent surgery; in all 11 cases the EZ was surgically proven by positive histopathology results and the patient having at least 1 year of good seizure outcome. ASL results were concordant with this final surgically proven EZ in 10/11 cases (sensitivity 91%, specificity 50%). All 10 ASL-positive patients who underwent surgery had positive surgical pathology results and good long-term postsurgical seizure outcome at a mean follow-up of 39 months. Retrospective quantitative analysis based on significant z-score clusters found 1 true-positive result that was missed by qualitative analysis and 3 additional false-positive results (sensitivity 100%, specificity 23%).

CONCLUSIONS

ASL supports the hypothesis regarding the EZ in poorly defined focal epilepsy cases in children. Due to its convenience and noninvasive nature, the authors recommend that ASL be added routinely to the presurgical MRI evaluation of epilepsy. Future optimized quantitative methods may improve the diagnostic yield of this technique.

ABBREVIATIONS AI = asymmetry index; ASL = arterial spin labeling; CBF = cerebral blood flow; ECoG = electrocorticography; EZ = epileptogenic zone; FCD = focal cortical dysplasia; MEG = magnetoencephalography; MOGHE = mild malformation of cortical development with oligodendroglial hyperplasia; PDC = poorly defined case; SEEG = stereoelectroencephalography; SMA = supplementary motor area.

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Contributor Notes

Correspondence Roy W. R. Dudley: Montreal Children’s Hospital, Montréal, QC, Canada. roy.dudley@mcgill.ca.

INCLUDE WHEN CITING Published online December 25, 2020; DOI: 10.3171/2020.7.PEDS20397.

J.L. and P.T. contributed equally to this paper.

Disclosures Dr. Gilbert reports being an employee of Philips Healthcare. Dr. Moreau reports receiving clinical or research support for the study described (includes equipment or material) from the Canada First Research Excellence Fund awarded to McGill University for the Healthy Brains, Healthy Lives initiative; the Fonds de Recherche du Québec-Santé; and the Foundation of Stars.

  • 1

    Duncan JS, Winston GP, Koepp MJ, Ourselin S. Brain imaging in the assessment for epilepsy surgery. Lancet Neurol. 2016;15(4):420433.

  • 2

    Warsi NM, Lasry O, Farah A, 3-T intraoperative MRI (iMRI) for pediatric epilepsy surgery. Childs Nerv Syst. 2016;32(12):24152422.

  • 3

    Eryurt B, Oner AY, Ucar M, Presurgical evaluation of mesial temporal lobe epilepsy with multiple advanced MR techniques at 3T. J Neuroradiol. 2015;42(5):283290.

    • Search Google Scholar
    • Export Citation
  • 4

    Guo X, Xu S, Wang G, Asymmetry of cerebral blood flow measured with three-dimensional pseudocontinuous arterial spin-labeling MR imaging in temporal lobe epilepsy with and without mesial temporal sclerosis. J Magn Reson Imaging. 2015;42(5):13861397.

    • Search Google Scholar
    • Export Citation
  • 5

    Lim YM, Cho YW, Shamim S, Usefulness of pulsed arterial spin labeling MR imaging in mesial temporal lobe epilepsy. Epilepsy Res. 2008;82(2-3):183189.

    • Search Google Scholar
    • Export Citation
  • 6

    Liu HL, Kochunov P, Hou J, Perfusion-weighted imaging of interictal hypoperfusion in temporal lobe epilepsy using FAIR-HASTE: comparison with H2 15O PET measurements. Magn Reson Med. 2001;45(3):431435.

    • Search Google Scholar
    • Export Citation
  • 7

    Oner AY, Eryurt B, Ucar M, pASL versus DSC perfusion MRI in lateralizing temporal lobe epilepsy. Acta Radiol. 2015;56(4):477481.

  • 8

    Wolf RL, Alsop DC, Levy-Reis I, 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(7):13341341

    • Search Google Scholar
    • Export Citation
  • 9

    Blauwblomme T, Boddaert N, Chémaly N, Arterial spin labeling MRI: a step forward in non-invasive delineation of focal cortical dysplasia in children. Epilepsy Res. 2014;108(10):19321939.

    • Search Google Scholar
    • Export Citation
  • 10

    Alsop DC, Detre JA, Golay X, Recommended implementation of arterial spin-labeled perfusion MRI for clinical applications: a consensus of the ISMRM perfusion study group and the European consortium for ASL in dementia. Magn Reson Med. 2015;73(1):102116.

    • Search Google Scholar
    • Export Citation
  • 11

    Boudes E, Gilbert G, Leppert IR, Measurement of brain perfusion in newborns: pulsed arterial spin labeling (PASL) versus pseudo-continuous arterial spin labeling (pCASL). Neuroimage Clin. 2014;6:126133.

    • Search Google Scholar
    • Export Citation
  • 12

    Shaikh H, Lechpammer M, Jensen FE, Increased brain perfusion persists over the first month of life in term asphyxiated newborns treated with hypothermia: does it reflect activated angiogenesis? Transl Stroke Res. 2015;6(3):224233.

    • Search Google Scholar
    • Export Citation
  • 13

    Fischl B. FreeSurfer. Neuroimage. 2012;62(2):774781.

  • 14

    Jenkinson M, Bannister P, Brady M, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage. 2002;17(2):825841.

    • Search Google Scholar
    • Export Citation
  • 15

    Desikan RS, Ségonne F, Fischl B, An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage. 2006;31(3):968980.

    • Search Google Scholar
    • Export Citation
  • 16

    Baillet S. Magnetoencephalography for brain electrophysiology and imaging. Nat Neurosci. 2017;20(3):327339.

  • 17

    Blümcke I, Thom M, Aronica E, 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(1):158174.

    • Search Google Scholar
    • Export Citation
  • 18

    Schurr J, Coras R, Rössler K, Mild malformation of cortical development with oligodendroglial hyperplasia in frontal lobe epilepsy: a new clinico-pathological entity. Brain Pathol. 2017;27(1):2635.

    • Search Google Scholar
    • Export Citation
  • 19

    Bulacio JC, Jehi L, Wong C, Long-term seizure outcome after resective surgery in patients evaluated with intracranial electrodes. Epilepsia. 2012;53(10):17221730.

    • Search Google Scholar
    • Export Citation
  • 20

    Pearce MS, Salotti JA, Little MP, Radiation exposure from CT scans in childhood and subsequent risk of leukaemia and brain tumours: a retrospective cohort study. Lancet. 2012;380(9840):499505.

    • Search Google Scholar
    • Export Citation
  • 21

    Dangouloff-Ros V, Deroulers C, Foissac F, Arterial spin labeling to predict brain tumor grading in children: correlations between histopathologic vascular density and perfusion MR imaging. Radiology. 2016;281(2):553566.

    • Search Google Scholar
    • Export Citation
  • 22

    Noguchi T, Yoshiura T, Hiwatashi A, Perfusion imaging of brain tumors using arterial spin-labeling: correlation with histopathologic vascular density. AJNR Am J Neuroradiol. 2008;29(4):688693.

    • Search Google Scholar
    • Export Citation
  • 23

    Pendse N, Wissmeyer M, Altrichter S, Interictal arterial spin-labeling MRI perfusion in intractable epilepsy. J Neuroradiol. 2010;37(1):6063.

    • Search Google Scholar
    • Export Citation
  • 24

    Sierra-Marcos A, Carreño M, Setoain X, Accuracy of arterial spin labeling magnetic resonance imaging (MRI) perfusion in detecting the epileptogenic zone in patients with drug-resistant neocortical epilepsy: comparison with electrophysiological data, structural MRI, SISCOM and FDG-PET. Eur J Neurol. 2016;23(1):160167.

    • Search Google Scholar
    • Export Citation
  • 25

    Lee SM, Kwon S, Lee YJ. Diagnostic usefulness of arterial spin labeling in MR negative children with new onset seizures. Seizure. 2019;65:151158.

    • Search Google Scholar
    • Export Citation
  • 26

    Wintermark P, Lechpammer M, Warfield SK, Perfusion imaging of focal cortical dysplasia using arterial spin labeling: correlation with histopathological vascular density. J Child Neurol. 2013;28(11):14741482.

    • Search Google Scholar
    • Export Citation
  • 27

    Boscolo Galazzo I, Mattoli MV, Pizzini FB, Cerebral metabolism and perfusion in MR-negative individuals with refractory focal epilepsy assessed by simultaneous acquisition of (18)F-FDG PET and arterial spin labeling. Neuroimage Clin. 2016;11:648657.

    • Search Google Scholar
    • Export Citation
  • 28

    Pollock JM, Tan H, Kraft RA, Arterial spin-labeled MR perfusion imaging: clinical applications. Magn Reson Imaging Clin N Am. 2009;17(2):315338.

    • Search Google Scholar
    • Export Citation
  • 29

    Mastin ST, Drane WE, Gilmore RL, Prospective localization of epileptogenic foci: comparison of PET and SPECT with site of surgery and clinical outcome. Radiology. 1996;199(2):375380.

    • Search Google Scholar
    • Export Citation
  • 30

    Gaxiola-Valdez I, Singh S, Perera T, Seizure onset zone localization using postictal hypoperfusion detected by arterial spin labelling MRI. Brain. 2017;140(11):28952911.

    • Search Google Scholar
    • Export Citation
  • 31

    Rhondali O, André C, Pouyau A, Sevoflurane anesthesia and brain perfusion. Paediatr Anaesth. 2015;25(2):180185.

  • 32

    Levman J, MacDonald P, Lim AR, A pediatric structural MRI analysis of healthy brain development from newborns to young adults. Hum Brain Mapp. 2017;38(12):59315942.

    • Search Google Scholar
    • Export Citation

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