Neuropediatrics 2023; 54(03): 188-196
DOI: 10.1055/a-1959-9241
Original Article

Abnormal Spontaneous Blood Oxygenation Level Dependent Fluctuations in Children with Focal Cortical Dysplasias: Initial Findings in Surgically Confirmed Cases

1   Pediatric Radiology Department, AP-HP, Hôpital Universitaire Necker-Enfants Malades, Paris, France
2   Université de Paris, INSERM U1199, Paris, France
3   Université de Paris, Institut Imagine, Paris, France
4   Department of Radiology, Maastricht University Medical Center, Maastricht, the Netherlands
5   School of Mental Health and Neurosciences, Maastricht, the Netherlands
,
Jacobus F.A. Jansen
4   Department of Radiology, Maastricht University Medical Center, Maastricht, the Netherlands
5   School of Mental Health and Neurosciences, Maastricht, the Netherlands
,
Joost de Jong
4   Department of Radiology, Maastricht University Medical Center, Maastricht, the Netherlands
5   School of Mental Health and Neurosciences, Maastricht, the Netherlands
,
Alida A. Postma
4   Department of Radiology, Maastricht University Medical Center, Maastricht, the Netherlands
5   School of Mental Health and Neurosciences, Maastricht, the Netherlands
,
Christianne Hoeberigs
4   Department of Radiology, Maastricht University Medical Center, Maastricht, the Netherlands
,
Ludovic Fillon
1   Pediatric Radiology Department, AP-HP, Hôpital Universitaire Necker-Enfants Malades, Paris, France
2   Université de Paris, INSERM U1199, Paris, France
3   Université de Paris, Institut Imagine, Paris, France
,
Jennifer Boisgontier
1   Pediatric Radiology Department, AP-HP, Hôpital Universitaire Necker-Enfants Malades, Paris, France
2   Université de Paris, INSERM U1199, Paris, France
3   Université de Paris, Institut Imagine, Paris, France
,
Charles-Joris Roux
1   Pediatric Radiology Department, AP-HP, Hôpital Universitaire Necker-Enfants Malades, Paris, France
2   Université de Paris, INSERM U1199, Paris, France
3   Université de Paris, Institut Imagine, Paris, France
,
Raphael Levy
1   Pediatric Radiology Department, AP-HP, Hôpital Universitaire Necker-Enfants Malades, Paris, France
2   Université de Paris, INSERM U1199, Paris, France
3   Université de Paris, Institut Imagine, Paris, France
,
Pascale Varlet
6   Neuropathology Department, GHU Paris, Université de Paris, 1 rue Cabanis, Paris
,
Thomas Blauwblomme
7   Pediatric Neurosurgery Department, AP-HP, Hôpital Universitaire Necker-Enfants Malades, Paris, France
8   Université de Paris, INSERM U1129, Pediatric Epilepsies and Brain Plasticity, Paris, France
,
Monika Eisermann
8   Université de Paris, INSERM U1129, Pediatric Epilepsies and Brain Plasticity, Paris, France
9   Department of Clinical Neurophysiology, Hôpital Universitaire Necker-Enfants Malades, Paris, France
,
Emma Losito
8   Université de Paris, INSERM U1129, Pediatric Epilepsies and Brain Plasticity, Paris, France
10   Pediatric Neurology Department, Reference Center for Rare Epilepsies, Hôpital Universitaire Necker-Enfants Malades, Paris, France
,
Marie Bourgeois
7   Pediatric Neurosurgery Department, AP-HP, Hôpital Universitaire Necker-Enfants Malades, Paris, France
,
Catherine Chiron
8   Université de Paris, INSERM U1129, Pediatric Epilepsies and Brain Plasticity, Paris, France
10   Pediatric Neurology Department, Reference Center for Rare Epilepsies, Hôpital Universitaire Necker-Enfants Malades, Paris, France
11   Department of Nuclear Medicine, SHFJ-CEA, Orsay, France
,
Rima Nabbout
8   Université de Paris, INSERM U1129, Pediatric Epilepsies and Brain Plasticity, Paris, France
10   Pediatric Neurology Department, Reference Center for Rare Epilepsies, Hôpital Universitaire Necker-Enfants Malades, Paris, France
,
Nathalie Boddaert
1   Pediatric Radiology Department, AP-HP, Hôpital Universitaire Necker-Enfants Malades, Paris, France
2   Université de Paris, INSERM U1199, Paris, France
3   Université de Paris, Institut Imagine, Paris, France
,
Walter Backes
4   Department of Radiology, Maastricht University Medical Center, Maastricht, the Netherlands
5   School of Mental Health and Neurosciences, Maastricht, the Netherlands
› Author Affiliations
Funding This work was funded by the Alain Rahmouni research grant from the French Society of Radiology.

Abstract

Background Focal cortical dysplasias (FCD) are a frequent cause of drug-resistant epilepsy in children but are often undetected on structural magnetic resonance imaging (MRI). We aimed to measure and validate the variation of resting state functional MRI (rs-fMRI) blood oxygenation level dependent (BOLD) metrics in surgically proven FCDs in children, to assess the potential yield for detecting and understanding these lesions.

Methods We prospectively included pediatric patients with surgically proven FCD with inconclusive structural MRI and healthy controls, who underwent a ten-minute rs-fMRI acquired at 3T. Rs-fMRI data was pre-processed and maps of values of regional homogeneity (ReHo), degree centrality (DC), amplitude of low frequency fluctuations (ALFF) and fractional ALFF (fALFF) were calculated. The variations of BOLD metrics within the to-be-resected areas were analyzed visually, and quantitatively using lateralization indices. BOLD metrics variations were also analyzed in fluorodeoxyglucose-positron emission tomography (FDG-PET) hypometabolic areas.

Results We included 7 patients (range: 3–15 years) and 6 aged-matched controls (range: 6–17 years). ReHo lateralization indices were positive in the to-be-resected areas in 4/7 patients, and in 6/7 patients in the additional PET hypometabolic areas. These indices were significantly higher compared to controls in 3/7 and 4/7 patients, respectively. Visual analysis revealed a good spatial correlation between high ReHo areas and MRI structural abnormalities (when present) or PET hypometabolic areas. No consistent variation was seen using DC, ALFF, or fALFF.

Conclusion Resting-state fMRI metrics, noticeably increase in ReHo, may have potential to help detect MRI-negative FCDs in combination with other morphological and functional techniques, used in clinical practice and epilepsy-surgery screening.

Supplementary Material



Publication History

Received: 17 May 2022

Accepted: 07 October 2022

Accepted Manuscript online:
12 October 2022

Article published online:
27 December 2022

© 2022. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Wong-Kisiel LC, Blauwblomme T, Ho ML. et al. Challenges in managing epilepsy associated with focal cortical dysplasia in children. Epilepsy Res 2018; 145: 1-17
  • 2 Blumcke I, Spreafico R, Haaker G. et al; EEBB Consortium. Histopathological findings in brain tissue obtained during epilepsy surgery. N Engl J Med 2017; 377 (17) 1648-1656
  • 3 Jayalakshmi S, Nanda SK, Vooturi S. et al. Focal cortical dysplasia and refractory epilepsy: role of multimodality imaging and outcome of surgery. AJNR Am J Neuroradiol 2019; 40 (05) 892-898
  • 4 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
  • 5 Wilmshurst JM, Gaillard WD, Vinayan KP. et al. Summary of recommendations for the management of infantile seizures: task force report for the ILAE commission of pediatrics. Epilepsia 2015; 56 (08) 1185-1197
  • 6 Zijlmans M, Zweiphenning W, van Klink N. Changing concepts in presurgical assessment for epilepsy surgery. Nat Rev Neurol 2019; 15 (10) 594-606
  • 7 Chassoux F, Rodrigo S, Semah F. et al. FDG-PET improves surgical outcome in negative MRI Taylor-type focal cortical dysplasias. Neurology 2010; 75 (24) 2168-2175
  • 8 Boerwinkle VL, Cediel EG, Mirea L. et al. Network-targeted approach and postoperative resting-state functional magnetic resonance imaging are associated with seizure outcome. Ann Neurol 2019; 86 (03) 344-356
  • 9 Boerwinkle VL, Mohanty D, Foldes ST. et al. Correlating resting-state functional magnetic resonance imaging connectivity by independent component analysis-based epileptogenic zones with intracranial electroencephalogram localized seizure onset zones and surgical outcomes in prospective pediatric intractable epilepsy study. Brain Connect 2017; 7 (07) 424-442
  • 10 Zang Y, Jiang T, Lu Y, He Y, Tian L. Regional homogeneity approach to fMRI data analysis. Neuroimage 2004; 22 (01) 394-400
  • 11 Yang H, Long XY, Yang Y. et al. Amplitude of low frequency fluctuation within visual areas revealed by resting-state functional MRI. Neuroimage 2007; 36 (01) 144-152
  • 12 Zuo XN, Ehmke R, Mennes M. et al. Network centrality in the human functional connectome. Cereb Cortex 2012; 22 (08) 1862-1875
  • 13 Gupta L, Hofman PAM, Besseling RMH, Jansen JFA, Backes WH. Abnormal blood oxygen level-dependent fluctuations in focal cortical dysplasia and the perilesional zone: initial findings. AJNR Am J Neuroradiol 2018; 39 (07) 1310-1315
  • 14 Chen Z, An Y, Zhao B. et al. The value of resting-state functional magnetic resonance imaging for detecting epileptogenic zones in patients with focal epilepsy. PLoS One 2017; 12 (02) e0172094
  • 15 Chao-Gan Y, Yu-Feng Z. DPARSF: a MATLAB toolbox for “Pipeline” data analysis of resting-state fMRI. Front Syst Neurosci 2010; 4: 13
  • 16 Song XW, Dong ZY, Long XY. et al. REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PLoS One 2011; 6 (09) e25031
  • 17 Yan CG, Wang XD, Zuo XN, Zang YF. DPABI: data processing & analysis for (Resting-State) brain imaging. Neuroinformatics 2016; 14 (03) 339-351
  • 18 Wang X, Jiao D, Zhang X, Lin X. Altered degree centrality in childhood absence epilepsy: a resting-state fMRI study. J Neurol Sci 2017; 373: 274-279
  • 19 Warbrick T, Rosenberg J, Shah NJ. The relationship between BOLD fMRI response and the underlying white matter as measured by fractional anisotropy (FA): a systematic review. Neuroimage 2017; 153: 369-381
  • 20 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
  • 21 R Core Team (2022). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria; https://www.R-project.org/
  • 22 Leach JL, Awwad R, Greiner HM, Vannest JJ, Miles L, Mangano FT. Mesial temporal lobe morphology in intractable pediatric epilepsy: so-called hippocampal malrotation, associated findings, and relevance to presurgical assessment. J Neurosurg Pediatr 2016; 17 (06) 683-693
  • 23 Desarnaud S, Mellerio C, Semah F. et al. 18F-FDG PET in drug-resistant epilepsy due to focal cortical dysplasia type 2: additional value of electroclinical data and coregistration with MRI. Eur J Nucl Med Mol Imaging 2018; 45 (08) 1449-1460
  • 24 Pedersen M, Curwood EK, Vaughan DN, Omidvarnia AH, Jackson GD. Abnormal brain areas common to the focal epilepsies: multivariate pattern analysis of fMRI. Brain Connect 2016; 6 (03) 208-215
  • 25 Jiang L, Zuo XN. Regional homogeneity: a multimodal, multiscale neuroimaging marker of the human Connectome. Neuroscientist 2016; 22 (05) 486-505
  • 26 Nugent AC, Martinez A, D'Alfonso A, Zarate CA, Theodore WH. The relationship between glucose metabolism, resting-state fMRI BOLD signal, and GABAA-binding potential: a preliminary study in healthy subjects and those with temporal lobe epilepsy. J Cereb Blood Flow Metab 2015; 35 (04) 583-591
  • 27 Hunyadi B, Tousseyn S, Dupont P, Van Huffel S, De Vos M, Van Paesschen W. A prospective fMRI-based technique for localising the epileptogenic zone in presurgical evaluation of epilepsy. Neuroimage 2015; 113: 329-339
  • 28 Thornton RC, Rodionov R, Laufs H. et al. Imaging haemodynamic changes related to seizures: comparison of EEG-based general linear model, independent component analysis of fMRI and intracranial EEG. Neuroimage 2010; 53 (01) 196-205
  • 29 Zhang CH, Lu Y, Brinkmann B, Welker K, Worrell G, He B. Lateralization and localization of epilepsy related hemodynamic foci using presurgical fMRI. Clin Neurophysiol 2015; 126 (01) 27-38