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Structural plasticity of the contralesional hippocampus and its subfields in patients with glioma

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Abstract

Objectives

To characterize the structural plasticity of the contralesional hippocampus and its subfields in patients with unilateral glioma.

Methods

3D T1-weighted MRI images were collected from 55 patients with tumors infiltrating the left (HipL, n = 27) or right (HipR, n = 28) hippocampus, along with 30 age- and sex-matched healthy controls (HC). Gray matter volume differences of the contralesional hippocampal regions and three control regions (superior frontal gyrus, caudate nucleus, and superior occipital gyrus) were evaluated using voxel-based morphometry (VBM) analyses. Volumetric differences in the hippocampus and its subregional volume were measured using the FreeSurfer software.

Results

Compared with HC, patients with unilateral hippocampal glioma exhibited significantly larger gray matter volume in the contralesional hippocampus and parahippocampal regions (cluster = 571 voxels for HipL; cluster 1 = 538 voxels and cluster 2 = 88 voxels for HipR; family-wise error corrected p < 0.05). No significant alterations were found in control regions. Volumetric analyses showed the same trend in the contralesional hippocampal subregions for both patient groups, including the CA1 head, CA3 head, hippocampus amygdala transition area (HATA), fimbria, and the granule cell molecular layer of the dentate gyrus head (GC-ML-DG head). Notably, the differences of the contralesional HATA (HipL: η2 = 0.418, corrected p = 0.002; HipR: η2 = 0.313, corrected p = 0.052) and fimbria (HipL: η2 = 0.450, corrected p < 0.001; HipR: η2 = 0.358, corrected p = 0.012) still held after the Bonferroni correction.

Conclusions

Our findings provide evidence for macrostructural plasticity of the contralateral hippocampus in patients with unilateral hippocampal glioma. Specifically, HATA and fimbria exhibit great potential in this process.

Key Points

• Glioma infiltration of the hippocampal regions induces a significant increase in gray matter volume on the contralateral side.

• Specifically, the HATA and fimbria regions exhibit favorable plastic potential in the process of lesion-induced structural remolding.

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Abbreviations

CA:

Cornu ammonis area

DG:

Dentate gyrus

GC-ML-DG:

The granule cell molecular layer of the dentate gyrus

GM:

Gray matter

HATA:

Hippocampus amygdala transition area

HC:

Healthy controls

HipL/R:

Patients with tumors infiltrating the left/right hippocampus

IDH:

Isocitrate dehydrogenase

LGG:

Lower-grade glioma

MANCOVA:

Multivariate analysis of covariance

MNI:

Montreal Neurological Institute

ROI:

Region of interest

TFCE-FWE:

Threshold-free cluster enhancement family-wise error

TIV:

Total intracranial volume

VBG:

Virtual brain grafting

VBM:

Voxel-based morphometry

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Acknowledgements

The authors thank Prof. Ahmed M. Radwan and his team for their open-source code base, as well as the healthy volunteers and patients for their participation.

Funding

This study has received funding from the Postgraduate Research & Practice Innovation Program of Jiangsu Province (No. SJCX21_0643), the Jiangsu Provincial Medical Innovation Team (No. CXTDA2017050), and Jiangsu Provincial Health Commission (M2021003).

Author information

Author notes

  1. Dongming Liu and Jiu Chen have contributed equally to this work (joint first authors).

Authors and Affiliations

  1. Department of Neurosurgery, The Affiliated Brain Hospital of Nanjing Medical University, No.264, Guangzhou Road, Gulou District, Nanjing, 210029, Jiangsu, China

    Dongming Liu, Honglin Ge, Zhen Yan, Bei Luo, Xinhua Hu, Kun Yang, Yong Liu, Wenbin Zhang & Hongyi Liu

  2. Institute of Neuropsychiatry, The Affiliated Brain Hospital of Nanjing Medical University, Fourth Clinical College of Nanjing Medical University, Nanjing, 210029, Jiangsu, China

    Jiu Chen

  3. Institute of Brain Sciences, The Affiliated Brain Hospital of Nanjing Medical University, Nanjing, 210029, Jiangsu, China

    Jiu Chen, Xinhua Hu, Wenbin Zhang & Hongyi Liu

  4. Department of Radiology, The Affiliated Brain Hospital of Nanjing Medical University, Nanjing, Jiangsu, China

    Chaoyong Xiao

Authors
  1. Dongming Liu
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Corresponding authors

Correspondence to Wenbin Zhang or Hongyi Liu.

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Guarantor

The scientific guarantor of this publication is Prof. Hongyi Liu.

Conflict of interest

The authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article.

Statistics and biometry

No complex statistical methods were necessary for this paper.

Informed consent

Written informed consent was obtained from all subjects (patients) in this study.

Ethical approval

Institutional Review Board approval was obtained.

Methodology

• retrospective

• case–control study

• performed at one institution

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Liu, D., Chen, J., Ge, H. et al. Structural plasticity of the contralesional hippocampus and its subfields in patients with glioma. Eur Radiol 33, 6107–6115 (2023). https://doi.org/10.1007/s00330-023-09582-4

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  • DOI: https://doi.org/10.1007/s00330-023-09582-4

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