State-specific GluCEST alterations in insular subregions are associated with depression and plasma inflammatory biomarker levels in patients with inflammatory bowel disease
Background: Depression commonly co-occurs with inflammatory bowel disease (IBD). Abnormal glutamate levels in the insula and altered plasma inflammatory biomarkers are observed in IBD and depression. However, the changes in glutamate concentrations in insular subregions in IBD and their relationship...
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Elsevier
2025-01-01
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| Series: | NeuroImage: Clinical |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2213158224001542 |
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| author | Lixue Xu Jun Lu Minsi Zhou Haiyun Shi Jing Zheng Tianxin Cheng Hui Xu Dawei Yang Xingwang Yong Fang Xu Chenyue Xu Yan Dang Zhan Wang Siying Zhu Chunsaier Wang Peng Li Zhenchang Wang Jing Wu Yi Zhang Zhenghan Yang |
| author_facet | Lixue Xu Jun Lu Minsi Zhou Haiyun Shi Jing Zheng Tianxin Cheng Hui Xu Dawei Yang Xingwang Yong Fang Xu Chenyue Xu Yan Dang Zhan Wang Siying Zhu Chunsaier Wang Peng Li Zhenchang Wang Jing Wu Yi Zhang Zhenghan Yang |
| author_sort | Lixue Xu |
| collection | DOAJ |
| description | Background: Depression commonly co-occurs with inflammatory bowel disease (IBD). Abnormal glutamate levels in the insula and altered plasma inflammatory biomarkers are observed in IBD and depression. However, the changes in glutamate concentrations in insular subregions in IBD and their relationship with depression and inflammatory markers remain unclear. This study aimed to investigate differences in glutamate concentrations in insular subregions between IBD patients and healthy controls (HCs) and their correlation with depression scores and inflammatory markers. Methods: Forty-two IBD patients (19 active, IBD-A; 23 in remission, IBD-R) and 46 HCs underwent glutamate chemical exchange saturation transfer (GluCEST) magnetic resonance imaging. Blood samples from 37 IBD patients were collected for plasma inflammatory biomarker analysis. GluCEST indices in insular subregions were measured. The Hospital Anxiety and Depression Scale (HADS-D) was used to estimate depression symptoms. Whole-brain voxel-based analysis using one-way ANOVA explored between-group differences in GluCEST indices within the insula. FDR-corrected partial correlation analysis evaluated the relationships between GluCEST, depression symptoms, and inflammatory factors. Results: GluCEST indices decreased in IBD patients in the left dorsal dysgranular subregion of the insula (dId) (uncorrected p < 0.001, cluster-level FWE-corrected p < 0.05). GluCEST indices in the left dId showed a significant positive correlation with HADS-D in IBD-R (FDR corrected q < 0.05). Additionally, GluCEST indices in the left dId were negatively correlated with CXCL9 (FDR corrected q < 0.05). Conclusion: State-specific GluCEST alterations in the left dId are a cerebral metabolic feature of IBD. These changes are associated with depression and inflammatory biomarkers, suggesting that the brain-immune-gut axis might underlie depression in IBD patients. |
| format | Article |
| id | doaj-art-1b46bf2b2b9949368d8206eb00660766 |
| institution | DOAJ |
| issn | 2213-1582 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage: Clinical |
| spelling | doaj-art-1b46bf2b2b9949368d8206eb006607662025-08-20T02:52:31ZengElsevierNeuroImage: Clinical2213-15822025-01-014510371310.1016/j.nicl.2024.103713State-specific GluCEST alterations in insular subregions are associated with depression and plasma inflammatory biomarker levels in patients with inflammatory bowel diseaseLixue Xu0Jun Lu1Minsi Zhou2Haiyun Shi3Jing Zheng4Tianxin Cheng5Hui Xu6Dawei Yang7Xingwang Yong8Fang Xu9Chenyue Xu10Yan Dang11Zhan Wang12Siying Zhu13Chunsaier Wang14Peng Li15Zhenchang Wang16Jing Wu17Yi Zhang18Zhenghan Yang19Department of Radiology, Beijing Friendship Hospital, Capital Medical University, No. 95 Yongan Road, Beijing 100050, ChinaDepartment of Radiology, Beijing Friendship Hospital, Capital Medical University, No. 95 Yongan Road, Beijing 100050, ChinaDepartment of Gastroenterology, Beijing Friendship Hospital, Capital Medical University, No. 95 Yongan Road, Beijing 100050, ChinaDepartment of Gastroenterology, Beijing Friendship Hospital, Capital Medical University, No. 95 Yongan Road, Beijing 100050, ChinaDepartment of Radiology, Beijing Friendship Hospital, Capital Medical University, No. 95 Yongan Road, Beijing 100050, ChinaDepartment of Radiology, Beijing Friendship Hospital, Capital Medical University, No. 95 Yongan Road, Beijing 100050, ChinaDepartment of Radiology, Beijing Friendship Hospital, Capital Medical University, No. 95 Yongan Road, Beijing 100050, ChinaDepartment of Radiology, Beijing Friendship Hospital, Capital Medical University, No. 95 Yongan Road, Beijing 100050, ChinaKey Laboratory for Biomedical Engineering of Ministry of Education, Department of Biomedical Engineering, College of Biomedical Engineering & Instrument Science, Zhejiang University, Hangzhou, Zhejiang, 310058, ChinaDepartment of Gastroenterology, Beijing Friendship Hospital, Capital Medical University, No. 95 Yongan Road, Beijing 100050, ChinaDepartment of Gastroenterology, Beijing Friendship Hospital, Capital Medical University, No. 95 Yongan Road, Beijing 100050, ChinaDepartment of Gastroenterology, Beijing Friendship Hospital, Capital Medical University, No. 95 Yongan Road, Beijing 100050, ChinaDepartment of Gastroenterology, Beijing Friendship Hospital, Capital Medical University, No. 95 Yongan Road, Beijing 100050, ChinaDepartment of Gastroenterology, Beijing Friendship Hospital, Capital Medical University, No. 95 Yongan Road, Beijing 100050, ChinaDepartment of Gastroenterology, Beijing Friendship Hospital, Capital Medical University, No. 95 Yongan Road, Beijing 100050, ChinaDepartment of Gastroenterology, Beijing Friendship Hospital, Capital Medical University, No. 95 Yongan Road, Beijing 100050, ChinaDepartment of Radiology, Beijing Friendship Hospital, Capital Medical University, No. 95 Yongan Road, Beijing 100050, ChinaDepartment of Gastroenterology, Beijing Friendship Hospital, Capital Medical University, No. 95 Yongan Road, Beijing 100050, ChinaKey Laboratory for Biomedical Engineering of Ministry of Education, Department of Biomedical Engineering, College of Biomedical Engineering & Instrument Science, Zhejiang University, Hangzhou, Zhejiang, 310058, China; Corresponding authors.Department of Radiology, Beijing Friendship Hospital, Capital Medical University, No. 95 Yongan Road, Beijing 100050, China; Corresponding authors.Background: Depression commonly co-occurs with inflammatory bowel disease (IBD). Abnormal glutamate levels in the insula and altered plasma inflammatory biomarkers are observed in IBD and depression. However, the changes in glutamate concentrations in insular subregions in IBD and their relationship with depression and inflammatory markers remain unclear. This study aimed to investigate differences in glutamate concentrations in insular subregions between IBD patients and healthy controls (HCs) and their correlation with depression scores and inflammatory markers. Methods: Forty-two IBD patients (19 active, IBD-A; 23 in remission, IBD-R) and 46 HCs underwent glutamate chemical exchange saturation transfer (GluCEST) magnetic resonance imaging. Blood samples from 37 IBD patients were collected for plasma inflammatory biomarker analysis. GluCEST indices in insular subregions were measured. The Hospital Anxiety and Depression Scale (HADS-D) was used to estimate depression symptoms. Whole-brain voxel-based analysis using one-way ANOVA explored between-group differences in GluCEST indices within the insula. FDR-corrected partial correlation analysis evaluated the relationships between GluCEST, depression symptoms, and inflammatory factors. Results: GluCEST indices decreased in IBD patients in the left dorsal dysgranular subregion of the insula (dId) (uncorrected p < 0.001, cluster-level FWE-corrected p < 0.05). GluCEST indices in the left dId showed a significant positive correlation with HADS-D in IBD-R (FDR corrected q < 0.05). Additionally, GluCEST indices in the left dId were negatively correlated with CXCL9 (FDR corrected q < 0.05). Conclusion: State-specific GluCEST alterations in the left dId are a cerebral metabolic feature of IBD. These changes are associated with depression and inflammatory biomarkers, suggesting that the brain-immune-gut axis might underlie depression in IBD patients.http://www.sciencedirect.com/science/article/pii/S2213158224001542Brain-immune-gut axisGlutamate chemical exchange saturated transferDepressionPlasma inflammatory biomarkerInflammatory bowel disease |
| spellingShingle | Lixue Xu Jun Lu Minsi Zhou Haiyun Shi Jing Zheng Tianxin Cheng Hui Xu Dawei Yang Xingwang Yong Fang Xu Chenyue Xu Yan Dang Zhan Wang Siying Zhu Chunsaier Wang Peng Li Zhenchang Wang Jing Wu Yi Zhang Zhenghan Yang State-specific GluCEST alterations in insular subregions are associated with depression and plasma inflammatory biomarker levels in patients with inflammatory bowel disease NeuroImage: Clinical Brain-immune-gut axis Glutamate chemical exchange saturated transfer Depression Plasma inflammatory biomarker Inflammatory bowel disease |
| title | State-specific GluCEST alterations in insular subregions are associated with depression and plasma inflammatory biomarker levels in patients with inflammatory bowel disease |
| title_full | State-specific GluCEST alterations in insular subregions are associated with depression and plasma inflammatory biomarker levels in patients with inflammatory bowel disease |
| title_fullStr | State-specific GluCEST alterations in insular subregions are associated with depression and plasma inflammatory biomarker levels in patients with inflammatory bowel disease |
| title_full_unstemmed | State-specific GluCEST alterations in insular subregions are associated with depression and plasma inflammatory biomarker levels in patients with inflammatory bowel disease |
| title_short | State-specific GluCEST alterations in insular subregions are associated with depression and plasma inflammatory biomarker levels in patients with inflammatory bowel disease |
| title_sort | state specific glucest alterations in insular subregions are associated with depression and plasma inflammatory biomarker levels in patients with inflammatory bowel disease |
| topic | Brain-immune-gut axis Glutamate chemical exchange saturated transfer Depression Plasma inflammatory biomarker Inflammatory bowel disease |
| url | http://www.sciencedirect.com/science/article/pii/S2213158224001542 |
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