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Brain structural changes and molecular analyses in children with benign epilepsy with centrotemporal spikes

Pediatric Research (2024)Cite this article

Abstract

Background

Benign epilepsy with centrotemporal spikes (BECTS) is a common childhood epilepsy syndrome, accompanied by behavioral problems and cognitive impairments. Previous studies of BECTS-related brain structures applied univariate analysis and showed inconsistent results. And neurotransmitter patterns associated with brain structural alterations were still unclear.

Methods

Structural images of twenty-one drug-naïve children with BECTS and thirty-five healthy controls (HCs) were scanned. Segmented gray matter volume (GMV) images were decomposed into independent components (ICs) using the source-based morphometry method. Then spatial correlation analyses were applied to examine possible relationships between GMV changes and neurotransmitter systems.

Results

Compared with HCs, drug-naïve children with BECTS showed increased volume in one GMV component (IC7), including bilateral precentral gyrus, bilateral supplementary motor area, left superior frontal cortex, bilateral middle/ inferior frontal cortex and bilateral anterior/ middle cingulate cortex. A positive correlation was observed between one GMV component (IC6) and seizure frequency. There were significantly positive correlations between abnormal GMV in IC7 and serotonergic, GABAergic and glutamatergic systems.

Conclusion

These findings provided further evidence of changed GMV in drug-naïve children with BECTS related to their behavioral problems and cognitive impairments, and associated neurotransmitters which could help to better understand neurobiological mechanisms and underlying molecular mechanisms of BECTS.

Impact

  • The article provides further evidence of changed gray matter volume in drug-naïve children with BECTS related to their behavioral problems and cognitive impairments as well as associated neurotransmitters.

  • Most literature to date has applied univariate analysis and showed inconsistent results, and neurotransmitter patterns associated with brain structural alterations were still unclear. Therefore, this article uses multivariate method and JuSpace toolbox to fill the gap.

  • Significantly increased gray matter volume was found in drug-naïve children with BECTS compared with healthy controls.

  • Abnormal gray matter volume was significantly correlated with clinical data and specific neurotransmitters.

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Fig. 1: Spatial map of IC7 showing significant differences between BECTS and HCs group.
Fig. 2: Functional annotation associated with IC7.
Fig. 3: Correlation between loading coefficients of IC6 and seizure frequency in BECTS group.
Fig. 4: Spatial correlations between IC7 and neurotransmitter maps.

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Data availability

The datasets generated and/or analyzed during this study are available from the corresponding author on reasonable request.

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Acknowledgements

The authors acknowledge and thank wholeheartedly the participants of this study. We truly appreciate the patience of study participants for their valuable information, cooperation, and participation. This study was financially supported by the National Natural Science Foundation of China under (grant No. 82270696); Shaanxi Key Research and Development Program (grant No.2023-YBSF-673); Shaanxi Provincial Key Laboratory of Integrated Acupuncture and Medication (grant No. KF2219); Young Outstanding Scientific and Technological Talent of Guizhou Province (grant No. Qiankehepingtairencai[2021]5620), Key Basic Research Program of Guizhou Province (grant No. Qiankehejichu-ZK[2022]zhongdian 051), Talent Program for Future Famous Clinical Doctors of Zunyi Medical University (grant No. rc220211205), and Science and Technology Program of Xi’an (grant No.23YXYJ0004). The authors would like to express their gratitude for the support of these projects.

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Author notes

  1. These authors contributed equally: Heng Liu, Duoli Chen.

Authors and Affiliations

  1. Department of Radiology, The Seventh People’s Hospital of Chongqing, The Central Hospital Affiliated to Chongqing University of Technology, Chongqing, China

    Heng Liu & Hong Lu

  2. Department of Radiology, The Affiliated Hospital of Zunyi Medical University, Zunyi, China

    Heng Liu

  3. School of Life Science and Technology, Xidian University, Xi’an, Shaanxi, China

    Duoli Chen, Chengxiang Liu & Peng Liu

  4. Department of Medical Imaging, Chongqing Traditional Chinese Medicine Hospital, Chongqing, China

    Hua Yang

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Contributions

Heng Liu, Hua Yang and Hong Lu were responsible for conception and design of the study; Duoli Chen, Chengxiang Liu and Peng Liu assisted with data analysis and interpretation of findings; Duoli Chen and Peng Liu drafted the manuscript. All authors critically reviewed the content and approved the final version for publication.

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Correspondence to Heng Liu, Hua Yang or Hong Lu.

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Liu, H., Chen, D., Liu, C. et al. Brain structural changes and molecular analyses in children with benign epilepsy with centrotemporal spikes. Pediatr Res (2024). https://doi.org/10.1038/s41390-024-03118-2

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