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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.

Radiation encephalopathy (RE) is an important potential complication in patients with nasopharyngeal carcinoma (NPC) who undergo radiotherapy (RT) that can affect the quality of life. However, a functional imaging biomarker of pre-symptomatic RE has not yet been established. This study aimed to assess radiation-induced gray matter functional alterations and explore fractional amplitude of low-frequency fluctuation (fALFF) as an imaging biomarker for predicting or diagnosing RE in patients with NPC. A total of 60 patients with NPC were examined, 21 in the pre-RT cohort and 39 in the post-RT cohort. Patients in the post-RT cohort were further divided into two subgroups according to the occurrence of RE in follow-up: post-RT non−RE (n = 21) and post-RT REprovedinfollow−up (n = 18). Surface-based and volume-based fALFF were used to detect radiation-induced functional alterations. Functional derived features were then adopted to construct a predictive model for the diagnosis of RE. We observed that surface-based fALFF could sensitively detect radiation-induced functional alterations in the intratemporal brain regions (such as the hippocampus and superior temporal gyrus), as well as the extratemporal regions (such as the insula and prefrontal lobe); however, no significant intergroup differences were observed using volume-based fALFF. No significant correlation between fALFF and radiation dose to the ipsilateral temporal lobe was observed. Support vector machine (SVM) analysis revealed that surface-based fALFF in the bilateral superior temporal gyri and left insula exhibited impressive performance (accuracy = 80.49%) in identifying patients likely to develop RE. We conclude that surface-based fALFF may serve as a sensitive imaging biomarker in the prediction of RE.

Radiation encephalopathy (RE) is one of the most severe complications in nasopharyngeal carcinoma (NPC) patients after radiotherapy (RT). However, the morphological alteration of early RE is insufficiently investigated. We aimed to investigate the cortical thickness and surface area alterations in NPC patients with or without RE in the follow-up. A total of 168 NPC patients each underwent a single scan and analysis at various times either Pre-RT (n = 56) or Post-RT (n = 112). We further divided the Post-RT NPC patients into three groups based on the time of the analysis following RT (Post-RTwithin 6 months and Post-RT7-12 months) or whether RE signs were detected in the analysis (Post-RTRE proved in follow-up). We confined the vertex-wise analyses of the cortical thickness and surface area to the bilateral temporal lobes. Interestingly, we revealed a gradual increase in the cortical surface area of the temporal lobe with increasing time after RT within the Post-RTRE proved in follow-up group, consistent with the between-group findings, which showed a significant increase in cortical surface area in the Post-RTRE proved in follow-up group relative to the Pre-RT group and the Post-RTwithin 6 months group. By contrast, such a trend was not observed in the cortical thickness findings. We concluded that the cortical surface area, rather than cortical thickness, may serve as a potential biomarker for early diagnosis of RE.