Structure–Function Decoupling: A Novel Perspective for Understanding the Radiation-Induced Brain Injury in Patients With Nasopharyngeal Carcinoma
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–functio...
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| Veröffentlicht in: | Frontiers in neuroscience Jg. 16; S. 915164 |
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| Sprache: | Englisch |
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Frontiers Media S.A
04.07.2022
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| 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. |
|---|---|
| AbstractList | 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-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-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-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. |
| Author | Ding, Hao Chen, Rui-ting Li, Li Gao, Jian-ming Liu, Li-zhi Kang, Ya-fei Zhang, You-ming |
| AuthorAffiliation | 5 State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Sun Yat-sen University Cancer Center , Guangzhou , China 1 Shaanxi Provincial Key Research Center of Child Mental and Behavioral Health, School of Psychology, Shaanxi Normal University , Xi’an , China 3 Department of Radiology, Affiliated Hospital of Guilin Medical University , Guilin , China 7 National Clinical Research Center for Geriatric Diseases, Xiangya Hospital, Central South University , Changsha , China 2 Department of Radiology, Xiangya Hospital, Central South University , Changsha , China 4 Department of Radiology, The First Affiliated Hospital of Guangxi Medical University , Nanning , 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 |
| AuthorAffiliation_xml | – name: 3 Department of Radiology, Affiliated Hospital of Guilin Medical University , Guilin , China – name: 5 State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Sun Yat-sen University Cancer Center , Guangzhou , China – name: 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 – name: 2 Department of Radiology, Xiangya Hospital, Central South University , Changsha , China – name: 4 Department of Radiology, The First Affiliated Hospital of Guangxi Medical University , Nanning , China – name: 7 National Clinical Research Center for Geriatric Diseases, Xiangya Hospital, Central South University , Changsha , China – name: 1 Shaanxi Provincial Key Research Center of Child Mental and Behavioral Health, School of Psychology, Shaanxi Normal University , Xi’an , China |
| Author_xml | – sequence: 1 givenname: Ya-fei surname: Kang fullname: Kang, Ya-fei – sequence: 2 givenname: Rui-ting surname: Chen fullname: Chen, Rui-ting – sequence: 3 givenname: Hao surname: Ding fullname: Ding, Hao – sequence: 4 givenname: Li surname: Li fullname: Li, Li – sequence: 5 givenname: Jian-ming surname: Gao fullname: Gao, Jian-ming – sequence: 6 givenname: Li-zhi surname: Liu fullname: Liu, Li-zhi – sequence: 7 givenname: You-ming surname: Zhang fullname: Zhang, You-ming |
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| Cites_doi | 10.1016/s0166-2236(02)02231-2 10.1371/journal.pone.0144556 10.1038/nn.2538 10.1016/j.asr.2003.09.051 10.1155/2021/4793517 10.1186/s12885-020-06957-4 10.1371/journal.pone.0036529 10.1016/j.actaastro.2004.05.068 10.1073/pnas.1219562110 10.1007/s11682-019-00145-0 10.1093/schbul/sbx051 10.1002/cam4.1291 10.1016/s0273-1177(99)01013-3 10.1002/hbm.23852 10.1007/s00234-014-1338-y 10.1097/SPC.0000000000000055 10.1016/j.neuroimage.2003.12.030 10.1097/MD.0000000000004275 10.1080/13548506.2014.967703 10.3389/fnins.2018.00599 10.1073/pnas.0811168106 10.1002/mus.23530 10.3389/fnins.2021.692575 10.1093/neuonc/nox211 10.1038/s41562-017-0260-9 10.1371/journal.pone.0067488 10.1016/j.neuron.2020.06.006 10.1523/JNEUROSCI.2709-12.2012 10.1097/j.pain.0000000000000951 10.1097/WNR.0000000000000813 10.1523/JNEUROSCI.21-06-02186.2001 10.1016/j.neuroscience.2020.07.005 10.1097/j.pain.0000000000000615 10.1038/s41467-021-25184-4 10.1146/annurev.neuro.27.070203.144130 10.3389/fonc.2021.687127 10.4103/jcrt.JCRT_551_18 10.1016/j.ijrobp.2009.06.080 10.1093/jjco/hyu062 10.1002/hbm.24834 10.1007/s11682-017-9801-0 10.1016/j.nicl.2017.02.025 |
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| SubjectTerms | individual prediction nasopharyngeal carcinoma Neuroscience radiation encephalopathy ReHo/VBM structure–function coupling |
| Title | Structure–Function Decoupling: A Novel Perspective for Understanding the Radiation-Induced Brain Injury in Patients With Nasopharyngeal Carcinoma |
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