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Altered whole-brain functional network in patients with frontal low-grade gliomas: a resting-state functional MRI study

  • Advanced Neuroimaging
  • Published:
Neuroradiology Aims and scope Submit manuscript

Abstract

Purpose

Gliomas are the most common primary brain tumor. Currently, topological alterations of whole-brain functional network caused by gliomas are not fully understood. The work here clarified the topological reorganization of the functional network in patients with unilateral frontal low-grade gliomas (LGGs).

Methods

A total of 45 patients with left frontal LGGs, 19 with right frontal LGGs, and 25 healthy controls (HCs) were enrolled. All the resting-state functional MRI (rs-fMRI) images of the subjects were preprocessed to construct the functional network matrix, which was used for graph theoretical analysis. A two-sample t-test was conducted to clarify the differences in global and nodal network metrics between patients and HCs. A network-based statistic approach was used to identify the altered specific pairs of regions in which functional connectivity in patients with LGGs.

Results

The local efficiency, clustering coefficient, characteristic path length, and normalized characteristic path length of patients with unilateral frontal LGGs were significantly lower than HCs, while there were no significant differences of global efficiency and small-worldness between patients and HCs. Compared with the HCs, betweenness centrality, degree centrality, and nodal efficiency of several brain nodes were changed significantly in patients. Around the tumor and its adjacent areas, the inter- and intra-hemispheric connections were significantly decreased in patients with left frontal LGGs.

Conclusion

The patients with unilateral frontal LGGs have altered global and nodal network metrics and decreased inter- and intra-hemispheric connectivity. These topological alterations may be involved in functional impairment and compensation of patients.

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Data Availability

The anonymized imaging database can be obtained after the reasonable request is evaluated and approved by the Ethics Committee of Huashan hospital, Fudan University.

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Funding

This work was supported by the National Natural Science Foundation of China (82372048), Research Startup Fund of Huashan Hospital, Fudan University (2021QD035), Shanghai Sailing Program (22YF1405000), Shanghai Municipal Commission of Science and Technology (22TS1400900, 23S31904100, 22ZR1409500, and 22S31905300), and Greater Bay Area Institute of Precision Medicine (Guangzhou) (KCH2310094).

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Authors and Affiliations

  1. Department of Radiology, Huashan Hospital, Fudan University, Shanghai, China

    Kun Lv, Yue Hu, Xin Cao, Junyan Fu, Daoying Geng & Jun Zhang

  2. Shanghai Engineering Research Center of Intelligent Imaging for Critical Brain Diseases, Shanghai, China

    Kun Lv, Xin Cao, Junyan Fu, Daoying Geng & Jun Zhang

  3. Institute of Functional and Molecular Medical Imaging, Fudan University, Shanghai, China

    Kun Lv, Xin Cao, Junyan Fu, Daoying Geng & Jun Zhang

  4. Department of Radiology, Affiliated Hospital of Nantong University, Nantong, Jiangsu Province, China

    Yue Hu

  5. Department of Neurosurgery, Huashan Hospital, Fudan University, Shanghai, China

    Yongsheng Xie

  6. Academy for Engineering and Technology, Fudan University, Shanghai, China

    Hongyi Chen, Daoying Geng & Jun Zhang

  7. Department of Pathology, Huashan Hospital, Fudan University, Shanghai, China

    Ji Xiong

  8. Department of Radiology, Shanghai Chest Hospital, Shanghai Jiao Tong University, 241 West Huaihai Road, Shanghai, China

    Li Zhu

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  1. Kun Lv
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  2. Yue Hu
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  3. Xin Cao
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  4. Yongsheng Xie
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  8. Li Zhu
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Corresponding authors

Correspondence to Li Zhu, Daoying Geng or Jun Zhang.

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The authors declare that they have no conflict of interest.

Ethics approval

All procedures performed in the 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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Informed consent was obtained from all individual participants included in the study.

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Kun Lv and Yue Hu contributed equally to this work.

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Lv, K., Hu, Y., Cao, X. et al. Altered whole-brain functional network in patients with frontal low-grade gliomas: a resting-state functional MRI study. Neuroradiology 66, 775–784 (2024). https://doi.org/10.1007/s00234-024-03300-7

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  • DOI: https://doi.org/10.1007/s00234-024-03300-7

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