Structure-Function Decoupling: A Novel Perspective for Understanding the Radiation-Induced Brain Injury in Patients With Nasopharyngeal Carcinoma

Ya-Fei Kang; Rui-Ting Chen; Hao Ding; Li Li; Jian-Ming Gao; Li-Zhi Liu; You-Ming Zhang

doi:10.3389/fnins.2022.915164

Structure-Function Decoupling: A Novel Perspective for Understanding the Radiation-Induced Brain Injury in Patients With Nasopharyngeal Carcinoma

Front Neurosci. 2022 Jul 4:16:915164. doi: 10.3389/fnins.2022.915164. eCollection 2022.

Authors

Ya-Fei Kang¹, Rui-Ting Chen², Hao Ding^{3

4}, Li Li⁵, Jian-Ming Gao⁶, Li-Zhi Liu⁵, You-Ming Zhang^{2

7}

Affiliations

¹ Shaanxi Provincial Key Research Center of Child Mental and Behavioral Health, School of Psychology, Shaanxi Normal University, Xi'an, China.
² Department of Radiology, Xiangya Hospital, Central South University, Changsha, China.
³ Department of Radiology, Affiliated Hospital of Guilin Medical University, Guilin, China.
⁴ Department of Radiology, The First Affiliated Hospital of Guangxi Medical University, Nanning, China.
⁵ State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Sun Yat-sen University Cancer Center, Guangzhou, China.
⁶ State Key Laboratory of Oncology in South China, Department of Radiation Oncology, Collaborative Innovation Center for Cancer Medicine, Sun Yat-sen University Cancer Center, Guangzhou, China.
⁷ National Clinical Research Center for Geriatric Diseases, Xiangya Hospital, Central South University, Changsha, China.

Abstract

Radiation-induced functional and structural brain alterations are well documented in patients with nasopharyngeal carcinoma (NPC), followed by radiotherapy (RT); however, alterations in structure-function coupling remain largely unknown. Herein, we aimed to assess radiation-induced structure-function decoupling and its importance in predicting radiation encephalopathy (RE). We included 62 patients with NPC (22 patients in the pre-RT cohort, 18 patients in the post-RT-RE_+ve cohort, and 22 patients in the post-RT-RE_-ve cohort). A metric of regional homogeneity (ReHo)/voxel-based morphometry (VBM) was used to detect radiation-induced structure-function decoupling, which was then used as a feature to construct a predictive model for RE. Compared with the pre-RT group, patients in the post-RT group (which included post-RT-RE_+ve and post-RT-RE_-ve) showed higher ReHo/VBM coupling values in the substantia nigra (SN), the putamen, and the bilateral thalamus and lower values in the brain stem, the cerebellum, the bilateral medial temporal lobes (MTLs), the bilateral insula, the right precentral and postcentral gyri, the medial prefrontal cortex (MPFC), and the left inferior parietal lobule (IPL). In the post-RT group, negative correlations were observed between maximum dosage of RT (MDRT) to the ipsilateral temporal lobe and ReHo/VBM values in the ipsilateral middle temporal gyrus (MTG). Moreover, structure-function decoupling in the bilateral superior temporal gyrus (STG), the bilateral precentral and postcentral gyri, the paracentral lobules, the right precuneus and IPL, and the right MPFC exhibited excellent predictive performance (accuracy = 88.0%) in identifying patients likely to develop RE. These findings show that ReHo/VBM may be a novel effective imaging metric that reflects the neural mechanism underlying RE in patients with NPC.

Keywords: ReHo/VBM; individual prediction; nasopharyngeal carcinoma; radiation encephalopathy; structure–function coupling.