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27-04-2024 | Epilepsy | Advanced Neuroimaging

Combined diffusion tensor imaging and quantitative susceptibility mapping to characterize normal-appearing white matter in self-limited epilepsy with centrotemporal spikes

Authors: Gaoqiang Xu, Yao Zhang, Xiaoxi Chen

Published in: Neuroradiology

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Abstract

Purpose

In brain development, Myelination is the characteristic feature of white matter maturation, which plays an important role in efficient information transmitting. The white matter abnormality has been reported to be associated with self-limited epilepsy with centrotemporal spikes (SeLECTS). This study aimed to detect the altered white matter region in the SeLECTS patients by the combination of diffusion tensor imaging (DTI) and quantitative susceptibility mapping (QSM) technique.

Methods

27 children with SeLECTS and 23 age- and gender-matched healthy children were enrolled. All participants were scanned with 3.0-T MRI to acquire the structure, diffusion and susceptibility-weighted data. The susceptibility and diffusion weighted data were processed to obtain quantitative susceptibility map and fraction anisotropy (FA) map. Then voxel-wise tract-based spatial statistics (TBSS) were used to analyze quantitative susceptibility and FA data.

Results

Both DTI and QSM revealed extensive white matter alterations in the frontal, parietal, and temporal lobes in SeLECTS patients. The overlapped region of DTI and QSM analyses was located in the fiber tracts of the corona radiata. The FA values in this overlapped region were negatively correlated with the magnetic susceptibility values.

Conclusion

Our results suggest that TBSS-based QSM can be employed as a novel approach for characterizing alterations in white matter in SeLECTS. And the combination of QSM and DTI can provide a more comprehensive evaluation of white matter integrity by utilizing different biophysical features.
Literature
1.
go back to reference Specchio N, Wirrell EC, Scheffer IE et al (2022) International league against epilepsy classification and definition of epilepsy syndromes with onset in childhood: position paper by the ilae task force on nosology and definitions. Epilepsia 63:1398–1442CrossRefPubMed Specchio N, Wirrell EC, Scheffer IE et al (2022) International league against epilepsy classification and definition of epilepsy syndromes with onset in childhood: position paper by the ilae task force on nosology and definitions. Epilepsia 63:1398–1442CrossRefPubMed
2.
go back to reference Dalla Bernardina B, Sgrò V, Caraballo R et al (1991) Sleep and benign partial epilepsies of childhood: EEG and evoked potentials study. Epilepsy Res Suppl 2:83–96PubMed Dalla Bernardina B, Sgrò V, Caraballo R et al (1991) Sleep and benign partial epilepsies of childhood: EEG and evoked potentials study. Epilepsy Res Suppl 2:83–96PubMed
3.
go back to reference Wirrell EC, Grossardt BR, Wong Kisiel LCL, Nickels KC (2011) 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 95:110–118CrossRefPubMedPubMedCentral Wirrell EC, Grossardt BR, Wong Kisiel LCL, Nickels KC (2011) 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 95:110–118CrossRefPubMedPubMedCentral
4.
go back to reference Kavros PM, Clarke T, Strug LJ, Halperin JM, Dorta NJ, Pal DK (2008) Attention impairment in rolandic epilepsy: systematic review. Epilepsia 49:1570–1580CrossRefPubMed Kavros PM, Clarke T, Strug LJ, Halperin JM, Dorta NJ, Pal DK (2008) Attention impairment in rolandic epilepsy: systematic review. Epilepsia 49:1570–1580CrossRefPubMed
5.
go back to reference Yung AW, Park YD, Cohen MJ, Garrison TN (2000) Cognitive and behavioral problems in children with centrotemporal spikes. Pediatr Neurol 23:391–395CrossRefPubMed Yung AW, Park YD, Cohen MJ, Garrison TN (2000) Cognitive and behavioral problems in children with centrotemporal spikes. Pediatr Neurol 23:391–395CrossRefPubMed
6.
go back to reference Kim SE, Lee JH, Chung HK et al (2014) Alterations in white matter microstructures and cognitive dysfunctions in benign childhood epilepsy with centrotemporal spikes. Eur J Neurol 21:708–717CrossRefPubMed Kim SE, Lee JH, Chung HK et al (2014) Alterations in white matter microstructures and cognitive dysfunctions in benign childhood epilepsy with centrotemporal spikes. Eur J Neurol 21:708–717CrossRefPubMed
7.
go back to reference Zhang Q, He Y, Qu T et al (2021) Delayed brain development of Rolandic epilepsy profiled by deep learning–based neuroanatomic imaging. Eur Radiol 31:9628–9637CrossRefPubMed Zhang Q, He Y, Qu T et al (2021) Delayed brain development of Rolandic epilepsy profiled by deep learning–based neuroanatomic imaging. Eur Radiol 31:9628–9637CrossRefPubMed
8.
go back to reference Pardoe HR, Berg AT, Archer JS, Fulbright RK, Jackson GD (2013) A neurodevelopmental basis for BECTS: evidence from structural MRI. Epilepsy Res 105:133–139CrossRefPubMedPubMedCentral Pardoe HR, Berg AT, Archer JS, Fulbright RK, Jackson GD (2013) A neurodevelopmental basis for BECTS: evidence from structural MRI. Epilepsy Res 105:133–139CrossRefPubMedPubMedCentral
9.
go back to reference Wilent WB, Contreras D (2005) Dynamics of excitation and inhibition underlying stimulus selectivity in rat somatosensory cortex. Nat Neurosci 8:1364–1370CrossRefPubMed Wilent WB, Contreras D (2005) Dynamics of excitation and inhibition underlying stimulus selectivity in rat somatosensory cortex. Nat Neurosci 8:1364–1370CrossRefPubMed
10.
go back to reference Lenroot RK, Giedd JN (2006) Brain development in children and adolescents: insights from anatomical magnetic resonance imaging. Neurosci Biobehav R 30:718–729CrossRef Lenroot RK, Giedd JN (2006) Brain development in children and adolescents: insights from anatomical magnetic resonance imaging. Neurosci Biobehav R 30:718–729CrossRef
11.
go back to reference Gogtay N, Giedd JN, Lusk L et al (2004) Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci 101:8174–8179CrossRefPubMedPubMedCentral Gogtay N, Giedd JN, Lusk L et al (2004) Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci 101:8174–8179CrossRefPubMedPubMedCentral
12.
go back to reference Ciumas C, Saignavongs M, Ilski F et al (2014) White matter development in children with benign childhood epilepsy with centro-temporal spikes. Brain 137:1095–1106CrossRefPubMed Ciumas C, Saignavongs M, Ilski F et al (2014) White matter development in children with benign childhood epilepsy with centro-temporal spikes. Brain 137:1095–1106CrossRefPubMed
13.
go back to reference Eluvathingal TJ, Hasan KM, Kramer L et al (2007) Quantitative diffusion tensor tractography of association and projection fibers in normally developing children and adolescents. Cereb Cortex 17:2760–2768CrossRefPubMed Eluvathingal TJ, Hasan KM, Kramer L et al (2007) Quantitative diffusion tensor tractography of association and projection fibers in normally developing children and adolescents. Cereb Cortex 17:2760–2768CrossRefPubMed
15.
go back to reference Xiao F, Chen Q, Yu X et al (2014) Hemispheric lateralization of microstructural white matter abnormalities in children with active benign childhood epilepsy with centrotemporal spikes (BECTS): a preliminary DTI study. J Neurol sci 336:171–179CrossRefPubMed Xiao F, Chen Q, Yu X et al (2014) Hemispheric lateralization of microstructural white matter abnormalities in children with active benign childhood epilepsy with centrotemporal spikes (BECTS): a preliminary DTI study. J Neurol sci 336:171–179CrossRefPubMed
16.
go back to reference Yu FF, Chiang FL, Stephens N et al (2019) Characterization of normal-appearing white matter in multiple sclerosis using quantitative susceptibility mapping in conjunction with diffusion tensor imaging. Neuroradiology 61:71–79CrossRefPubMed Yu FF, Chiang FL, Stephens N et al (2019) Characterization of normal-appearing white matter in multiple sclerosis using quantitative susceptibility mapping in conjunction with diffusion tensor imaging. Neuroradiology 61:71–79CrossRefPubMed
18.
go back to reference Rudko DA, Solovey I, Gati JS, Kremenchutzky M, Menon RS (2014) Multiple sclerosis: improved identification of diseaserelevant changes in gray and white matter by using susceptibilitybased MR imaging. Radiology 272:851–864CrossRefPubMed Rudko DA, Solovey I, Gati JS, Kremenchutzky M, Menon RS (2014) Multiple sclerosis: improved identification of diseaserelevant changes in gray and white matter by using susceptibilitybased MR imaging. Radiology 272:851–864CrossRefPubMed
19.
go back to reference Argyridis I, Li W, Johnson GA, Liu C (2013) Quantitative magnetic susceptibility of the developing mouse brain reveals microstructural changes in the white matter. Neuroimage 88:134–142CrossRefPubMed Argyridis I, Li W, Johnson GA, Liu C (2013) Quantitative magnetic susceptibility of the developing mouse brain reveals microstructural changes in the white matter. Neuroimage 88:134–142CrossRefPubMed
20.
go back to reference Li W, Avram AV, Wu B, Xiao X, Liu C (2014) Integrated Laplacianbased phase unwrapping and background phase removal for quantitative susceptibility mapping. NMR Biomed 27:219–227CrossRefPubMed Li W, Avram AV, Wu B, Xiao X, Liu C (2014) Integrated Laplacianbased phase unwrapping and background phase removal for quantitative susceptibility mapping. NMR Biomed 27:219–227CrossRefPubMed
21.
go back to reference Li W, Wu B, Avram AV, Liu C (2012) Magnetic susceptibility anisotropy of human brain in vivo and its molecular underpinnings. Neuroimage 59:2088–2097CrossRefPubMed Li W, Wu B, Avram AV, Liu C (2012) Magnetic susceptibility anisotropy of human brain in vivo and its molecular underpinnings. Neuroimage 59:2088–2097CrossRefPubMed
22.
go back to reference Smith SM, Jenkinson M, Johansen-Berg H et al (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31:1487–1505CrossRefPubMed Smith SM, Jenkinson M, Johansen-Berg H et al (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31:1487–1505CrossRefPubMed
23.
go back to reference Lebel C, Walker L, Leemans A, Phillips L, Beaulieu C (2008) Microstructural maturation of the human brain from childhood to adulthood. Neuroimage 40:1044–1055CrossRefPubMed Lebel C, Walker L, Leemans A, Phillips L, Beaulieu C (2008) Microstructural maturation of the human brain from childhood to adulthood. Neuroimage 40:1044–1055CrossRefPubMed
24.
25.
go back to reference Lebel C, Gee M, Camicioli R et al (2012) Diffusion tensor imaging of white matter tract evolution over the lifespan. Neuroimage 60:340–352CrossRefPubMed Lebel C, Gee M, Camicioli R et al (2012) Diffusion tensor imaging of white matter tract evolution over the lifespan. Neuroimage 60:340–352CrossRefPubMed
26.
go back to reference Govindan RM, Makki MI, Sundaram SK, Juhász C, Chugani HT (2008) Diffusion tensor analysis of temporal and extra-temporal lobe tracts in temporal lobe epilepsy. Epilepsy Res 80:30–41CrossRefPubMedPubMedCentral Govindan RM, Makki MI, Sundaram SK, Juhász C, Chugani HT (2008) Diffusion tensor analysis of temporal and extra-temporal lobe tracts in temporal lobe epilepsy. Epilepsy Res 80:30–41CrossRefPubMedPubMedCentral
27.
go back to reference Shu M, Yu C, Shi Q, Li Y, Niu K, Zhang S, Wang X (2021) Alterations in white matter integrity and asymmetry in patients with benign childhood epilepsy with centrotemporal spikes and childhood absence epilepsy: An automated fiber quantification tractography study. Epilepsy Behav 123:108235CrossRefPubMed Shu M, Yu C, Shi Q, Li Y, Niu K, Zhang S, Wang X (2021) Alterations in white matter integrity and asymmetry in patients with benign childhood epilepsy with centrotemporal spikes and childhood absence epilepsy: An automated fiber quantification tractography study. Epilepsy Behav 123:108235CrossRefPubMed
28.
go back to reference Thorn EL, Ostrowski LM, Chinappen DM et al (2020) Persistent abnormalities in Rolandic thalamocortical white matter circuits in childhood epilepsy with centrotemporal spikes. Epilepsia 61:2500–2508CrossRefPubMedPubMedCentral Thorn EL, Ostrowski LM, Chinappen DM et al (2020) Persistent abnormalities in Rolandic thalamocortical white matter circuits in childhood epilepsy with centrotemporal spikes. Epilepsia 61:2500–2508CrossRefPubMedPubMedCentral
29.
go back to reference Agarwal R, Kumar A, Tiwari VN, Chugani H (2016) Thalamic abnormalities in children with continuous spike-wave during slow-wave sleep: an F-18-fluorodeoxyglucose positron emission tomography perspective. Epilepsia 57:263–271CrossRefPubMed Agarwal R, Kumar A, Tiwari VN, Chugani H (2016) Thalamic abnormalities in children with continuous spike-wave during slow-wave sleep: an F-18-fluorodeoxyglucose positron emission tomography perspective. Epilepsia 57:263–271CrossRefPubMed
Metadata
Title
Combined diffusion tensor imaging and quantitative susceptibility mapping to characterize normal-appearing white matter in self-limited epilepsy with centrotemporal spikes
Authors
Gaoqiang Xu
Yao Zhang
Xiaoxi Chen
Publication date
27-04-2024
Publisher
Springer Berlin Heidelberg
Published in
Neuroradiology
Print ISSN: 0028-3940
Electronic ISSN: 1432-1920
DOI
https://doi.org/10.1007/s00234-024-03367-2