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Quantitative susceptibility mapping shows lower brain iron content in children with childhood epilepsy with centrotemporal spikes

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Japanese Journal of Radiology Aims and scope Submit manuscript

Abstract

Purpose

The dysregulation of brain iron homeostasis is closely relevant to a multitude of chronic neurological disorders. This study employed quantitative susceptibility mapping (QSM) to detect and compare whole-brain iron content between childhood epilepsy with centrotemporal spikes (CECTS) children and typically developing children.

Materials and methods

32 children with CECTS and 25 age- and gender-matched healthy children were enrolled. All participants were imaged with 3.0-T MRI to acquire the structural and susceptibility-weighted data. The susceptibility-weighted data were processed using STISuite toolbox to obtain QSM. The magnetic susceptibility difference between the two groups was compared using voxel-wise and region of interest methods. Multivariable linear regression, controlling for age, were employed to investigate the associations between the brain magnetic susceptibility and age at onset.

Results

Lower magnetic susceptibility was mainly observed in sensory- and motor-related brain regions in children with CECTS, including bilateral middle frontal gyrus, supplementary motor area, midcingulate cortex, paracentral lobule and precentral gyrus, the magnetic susceptibility of right paracentral lobule, right precuneus and left supplementary motor area were found to have positive correlation with the age at onset.

Conclusions

This study suggests that the potential iron deficiency in certain brain regions is associated with CECTS, which might be helpful for further illumination of potential pathogenesis mechanism of CECTS.

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Abbreviations

AAL:

Automated anatomical labeling

ADHD:

Attention-deficit/hyperactivity disorder

ALFF:

Amplitude of low-frequency fluctuation

CECTS:

Childhood epilepsy with centrotemporal spikes

EEG:

Electroencephalogram

FEW:

Family-wise error

HC:

Healthy controls

MNI:

Montreal Neurological Institute

QSM:

Quantitative susceptibility mapping

SMA:

Supplementary motor area

MRI:

Magnetic resonance imaging

ROI:

Region of interest

References

  1. Northcott E, Connolly AM, Berroya A, et al. Memory and phonological awareness in children with Benign Rolandic Epilepsy compared to a matched control group. Epilepsy Res. 2007;75:57–62.

    Article  PubMed  Google Scholar 

  2. Giordani B, Caveney AF, Laughrin D, et al. Cognition and behavior in children with benign epilepsy with centrotemporal spikes (bects). Epilepsy Res. 2006;70:89–94.

    Article  CAS  PubMed  Google Scholar 

  3. Nicolai J, Aldenkamp AP, Arends J, Weber JW, Vles JS. Cognitive and behavioral effects of nocturnal epileptiform discharges in children with benign childhood epilepsy with centrotemporal spikes. Epilepsy Behav. 2006;8:56–70.

    Article  PubMed  Google Scholar 

  4. Garcia-Ramos C, Jackson DC, Lin JJ, et al. Cognition and brain development in children with benign epilepsy with centrotemporal spikes. Epilepsia. 2015;56:1615–22.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Shakeri M, Datta AN, Malfait D, et al. Sub-cortical brain morphometry and its relationship with cognition in rolandic epilepsy. Epilepsy Res. 2017;138:39–45.

    Article  PubMed  Google Scholar 

  6. Tan G, Xiao F, Chen S, et al. Frequency-specific alterations in the amplitude and synchronization of resting-state spontaneous low-frequency oscillations in benign childhood epilepsy with centrotemporal spikes. Epilepsy Res. 2018;145:178–84.

    Article  PubMed  Google Scholar 

  7. Zeng H, Ramos CG, Nair VA, et al. Regional homogeneity (ReHo) changes in new onset versus chronic benign epilepsy of childhood with centrotemporal spikes (BECTS): A resting state fMRI study. Epilepsy Res. 2015;116:79–85.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Li R, Wang L, Chen H, et al. Abnormal dynamics of functional connectivity density in children with benign epilepsy with centrotemporal spikes. Brain Imaging Behav. 2019;13:985–94.

    Article  PubMed  Google Scholar 

  9. Xiao F, Chen Q, Yu X, et al. 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. 2014;336:171–9.

    Article  PubMed  Google Scholar 

  10. Ward RJ, Zucca FA, Duyn JH, Crichton RR, Zecca L. The role of iron in brain ageing and neurodegenerative disorders. Lancet Neurol. 2014;13:1045–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Ke Y, Ming Qian Z. Iron misregulation in the brain: a primary cause of neurodegenerative disorders. Lancet Neurol. 2003;2:246–53.

    Article  CAS  PubMed  Google Scholar 

  12. Zecca L, Youdim MB, Riederer P, Connor JR, Crichton RR. Iron, brain ageing and neurodegenerative disorders. Nat Rev Neurosci. 2004;25:863–73.

    Article  Google Scholar 

  13. Crichton RR, Dexter DT, Ward RJ. Brain iron metabolism and its perturbation in neurological diseases. J Neural Transm (Vienna). 2011;118:301–14.

    Article  CAS  PubMed  Google Scholar 

  14. Jin L, Wang J, Zhao L, et al. Decreased serum ceruloplasmin levels characteristically aggravate nigral iron deposition in Parkinson’s disease. Brain. 2011;134:50–8.

    Article  PubMed  Google Scholar 

  15. Zhu WZ, Zhong WD, Wang W, et al. (2009) Quantitative MR phase-corrected imaging to investigate increased brain iron deposition of patients with Alzheimer disease. Radiology. 2009;253:497–504.

    Article  PubMed  Google Scholar 

  16. Langkammer C, Liu T, Khalil M, et al. Quantitative susceptibility mapping in multiple sclerosis. Radiology. 2013;267:551–9.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Jang HN, Yoon HS, Lee EH. Prospective case control study of iron deficiency and the risk of febrile seizures in children in South Korea. BMC Pediatr. 2019;19:309–17.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Xu M, Guo Y, Cheng J, et al. Brain iron assessment in patients with First-episode schizophrenia using quantitative susceptibility mapping. Neuroimage Clin. 2021;31: 102736.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Faux NG, Rembach A, Wiley J, et al. An anemia of Alzheimer’s disease. Mol Psychiatry. 2014;19:1227–34.

    Article  CAS  PubMed  Google Scholar 

  20. Zhang Z, Liao W, Bernhardt B, et al. Brain iron redistribution in mesial temporal lobe epilepsy: a susceptibility-weighted magnetic resonance imaging study. BMC Neurosci. 2014;15:117–28.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Gorter JA, Mesquita AR, van Vliet EA, da Silva FH, Aronica E. Increased expression of ferritin, an iron-storage protein, in specific regions of the parahippocampal cortex of epileptic rats. Epilepsia. 2005;46:1371–9.

    Article  CAS  PubMed  Google Scholar 

  22. Wang Y, Liu T. Quantitative susceptibility mapping (QSM): decoding MRI data for a tissue magnetic biomarker. Magn Reson Med. 2015;73:82–101.

    Article  CAS  PubMed  Google Scholar 

  23. Haacke EM, Liu S, Buch S, et al. Quantitative susceptibility mapping: current status and future directions. Magn Reson Imaging. 2015;33:1–25.

    Article  PubMed  Google Scholar 

  24. Berg AT, Berkovic SF, Brodie MJ, et al. Revised terminology and concepts for organization of seizures and epilepsies: report of the ILAE commission on classification and terminology, 2005–2009. Epilepsia. 2010;51:676–85.

    Article  PubMed  Google Scholar 

  25. Li W, Avram AV, Wu B, Xiao X, Liu C. Integrated Laplacian-based phase unwrapping and background phase removal for quantitative susceptibility mapping. NMR Biomed. 2014;27:219–27.

    Article  PubMed  Google Scholar 

  26. Ashburner J, Friston KJ. Unified segmentation. Neuroimage. 2005;26:839–51.

    Article  PubMed  Google Scholar 

  27. Hare D, Ayton S, Bush A, Lei P. A delicate balance: Iron metabolism and diseases of the brain. Front Aging Neurosci. 2013;5:34.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Bilgic B, Pfefferbaum A, Rohlfing T, et al. MRI estimates of brain iron concentration in normal aging using quantitative susceptibility mapping. Neuroimage. 2012;59:2625–35.

    Article  CAS  PubMed  Google Scholar 

  29. Langkammer C, Krebs N, Goessler W, et al. Quantitative MR imaging of brain iron: a postmortem validation study. Radiology. 2011;257:455–62.

    Article  Google Scholar 

  30. Chen Y, Su S, Dai Y, et al. Quantitative susceptibility mapping reveals brain iron deficiency in children with attention-deficit/hyperactivity disorder: a whole-brain analysis. Eur Radiol. 2022;32:3726–33.

    Article  CAS  PubMed  Google Scholar 

  31. Tang S, Xu Y, Liu X, Chen Z, Zhou Y, Nie L, He L. Quantitative susceptibility mapping shows lower brain iron content in children with autism. Eur Radiol. 2021;31:2073–83.

    Article  CAS  PubMed  Google Scholar 

  32. Khattar N, Triebswetter C, Kiely M, et al. Investigation of the association between cerebral iron content and myelin content in normative aging using quantitative magnetic resonance neuroimaging. Neuroimage. 2021;239: 118267.

    Article  CAS  PubMed  Google Scholar 

  33. Zhang Q, He Y, Qu T, et al. Delayed brain development of Rolandic epilepsy profiled by deep learning-based neuroanatomic imaging. Eur Radiol. 2021;31:9628–37.

    Article  PubMed  Google Scholar 

  34. Cona G, Semenza C. Supplementary motor area as key structure for domain-general sequence processing: A unified account. Neurosci Biobehav Rev. 2017;72:28–42.

    Article  PubMed  Google Scholar 

  35. Zhu J, Xu C, Zhang X, et al. Altered topological properties of brain functional networks in drug-resistant epilepsy patients with vagus nerve stimulators. Seizure. 2021;92:149–54.

    Article  PubMed  Google Scholar 

  36. Qin Y, Jiang S, Zhang Q, et al. BOLD-fMRI activity informed by network variation of scalp EEG in juvenile myoclonic epilepsy. Neuroimage Clin. 2019;22: 101759.

    Article  PubMed  PubMed Central  Google Scholar 

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Funding

This study has received funding by Guizhou Provincial Science and Technology Projects (grant number [2020]1Y347 and [2020] 1Y346).

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Authors and Affiliations

  1. Department of Radiology, Affiliated Hospital of Zunyi Medical University, 149 Dalian Road, Huichuan District, Zunyi, 563003, Guizhou, China

    Gaoqiang Xu & Xiaoxi Chen

  2. The Public Experimental Center of Medicine, Affiliated Hospital of Zunyi Medical University, 149 Dalian Road, Huichuan District, Zunyi, Guizhou, China

    Yao Zhang

Authors
  1. Gaoqiang Xu
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  2. Xiaoxi Chen
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  3. Yao Zhang
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Correspondence to Gaoqiang Xu.

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The authors declare that they have no conflict of interest.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Xu, G., Chen, X. & Zhang, Y. Quantitative susceptibility mapping shows lower brain iron content in children with childhood epilepsy with centrotemporal spikes. Jpn J Radiol 41, 1344–1350 (2023). https://doi.org/10.1007/s11604-023-01464-5

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  • DOI: https://doi.org/10.1007/s11604-023-01464-5

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