Brain structural alterations in MDD patients with gastrointestinal symptoms: Evidence from the REST-meta-MDD project,Progress in Neuro-Psychopharmacology and Biological Psychiatry

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Brain structural alterations in MDD patients with gastrointestinal symptoms: Evidence from the REST-meta-MDD project
Progress in Neuro-Psychopharmacology and Biological Psychiatry ( IF 5.3 ) Pub Date : 2021-06-11 , DOI: 10.1016/j.pnpbp.2021.110386
Peng-Hong Liu ₁ , Yan Li ₂ , Ai-Xia Zhang ₃ , Ning Sun ₁ , Gai-Zhi Li ₁ , Xiao Chen ₄ , Tong-Jian Bai ₅ , Qi-Jing Bo ₆ , Guan-Mao Chen ₇ , Ning-Xuan Chen ₄ , Tao-Lin Chen ₈ , Wei Chen ₉ , Chang Cheng ₁₀ , Yu-Qi Cheng ₁₁ , Xi-Long Cui ₁₀ , Jia Duan ₁₂ , Yi-Ru Fang ₁₃ , Qi-Yong Gong ₁₄ , Wen-Bin Guo ₁₀ , Zheng-Hua Hou ₁₅ , Lan Hu ₁₅ , Li Kuang ₁₅ , Feng Li ₅ , Kai-Ming Li ₁₆ , Tao Li ₈ , Yan-Song Liu ₁₇ , Zhe-Ning Liu ₁₀ , Yi-Cheng Long ₁₀ , Qing-Hua Luo ₁₅ , Hua-Qing Meng ₁₅ , Dai-Hui Peng ₁₃ , Hai-Tang Qiu ₁₅ , Jiang Qiu ₁₈ , Yue-Di Shen ₁₉ , Yu-Shu Shi ₈ , Fei Wang ₁₂ , Kai Wang ₅ , Li Wang ₂₀ , Xiang Wang ₁₀ , Ying Wang ₇ , Xiao-Ping Wu ₂₁ , Xin-Ran Wu ₁₈ , Chun-Ming Xie ₂₂ , Guang-Rong Xie ₁₀ , Hai-Yan Xie ₂₃ , Peng Xie ₂₄ , Xiu-Feng Xu ₆ , Hong Yang ₂₅ , Jian Yang ₂₆ , Jia-Shu Yao ₉ , Shu-Qiao Yao ₁₀ , Ying-Ying Yin ₂₇ , Yong-Gui Yuan ₂₇ , Hong Zhang ₂₁ , Lei Zhang ₄ , Zhi-Jun Zhang ₂₂ , Ru-Bai Zhou ₁₃ , Yi-Ting Zhou ₈ , Jun-Juan Zhu ₁₃ , Chao-Jie Zou ₁₁ , Tian-Mei Si ₂₀ , Xi-Nian Zuo ₂₈ , Chao-Gan Yan ₂₉ , Ke-Rang Zhang ₃

Affiliation

Department of Psychiatry, First Hospital of Shanxi Medical University, Taiyuan 030001, China; Department of First Clinical Medicine, Shanxi Medical University, Taiyuan 030001, China.
Department of Clinical Medicine, Fenyang College of Shanxi Medical University, 032200, China.
Department of Psychiatry, First Hospital of Shanxi Medical University, Taiyuan 030001, China.
CAS Key Laboratory of Behavioral Science, Institute of Psychology, Beijing 100054, China; Department of Psychology, University of Chinese Academy of Sciences, Beijing 100054, China.
Anhui Medical University, Hefei, Anhui 230022, China.
Beijing Anding Hospital, Capital Medical University, Beijing 100054, China.
The First Affiliated Hospital of Jinan University, Guangzhou, Guangdong 510630, China.
Mental Health Center, West China Hospital, Sichuan University Chengdu, Sichuan 610041, China.
Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang 310012, China.
The Institute of Mental Health, Second Xiangya Hospital of Central South University, Changsha, Hunan 410008, China.
First Affiliated Hospital of Kunming Medical University, Kunming, Yunnan 650221, China.
Department of Psychiatry, First Affiliated Hospital, China Medical University, Shenyang, Liaoning 110001, China.
Department of Psychiatry, Shanghai Jiao Tong University School of Medicine, Shanghai 200240, China.
Department of Radiology, Huaxi MR Research Center,West China Hospital of Sichuan University, Chengdu, Sichuan 610041, China; Psychoradiology Research Unit of Chinese Academy of Medical Sciences, West China Hospital of Sichuan University, Chengdu, Sichuan 610041, China.
Department of Psychiatry, The First Affiliated Hospital of Chongqing Medical University, Chongqing 400016, China.
Department of Radiology, Huaxi MR Research Center,West China Hospital of Sichuan University, Chengdu, Sichuan 610041, China.
Department of Clinical Psychology, Suzhou Psychiatric Hospital, The Affiliated Guangji Hospital of Soochow University, Suzhou, Jiangsu 215137, China.
Faculty of Psychology, Southwest University, Chongqing 400716, China.
Department of Diagnostics, Affiliated Hospital, Hangzhou Normal University Medical School, Hangzhou, Zhejiang 311121, China.
National Clinical Research Center for Mental Disorders, Peking University Sixth Hospital, Beijing 100191, China; Key Laboratory of Mental Health, Ministry of Health, Peking University, Beijing 100191, China.
Xi'an Central Hospital, Xi'an, Shannxi 710003, China.
Department of Neurology, Affiliated ZhongDa Hospital of Southeast University, Nanjing, Jiangsu 210009, China.
Department of Psychiatry, The Fourth Affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou, Zhejiang 310058, China.
Institute of Neuroscience, Chongqing Medical University, Chongqing 400016, China; Chongqing Key Laboratory of Neurobiology, Chongqing, 400016, China; Department of Neurology, The First Affiliated Hospital of Chongqing Medical University, Chongqing, 400016, China.
Department of Radiology, The First Affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou, Zhejiang 310058, China.
The First Affiliated Hospital of Xi'an Jiaotong University, Shaanxi 710061, China.
Department of Psychosomatics and Psychiatry, Zhongda Hospital, School of Medicine, Southeast University, Nanjing, Jiangsu 210096, China.
CAS Key Laboratory of Behavioral Science, Institute of Psychology, Beijing 100054, China; Department of Psychology, University of Chinese Academy of Sciences, Beijing 100054, China; Magnetic Resonance Imaging Research Center and Research Center for Lifespan Development of Mind and Brain (CLIMB), Institute of Psychology, Chinese Academy of Sciences, Beijing 100054, China.
CAS Key Laboratory of Behavioral Science, Institute of Psychology, Beijing 100054, China; Department of Psychology, University of Chinese Academy of Sciences, Beijing 100054, China; Magnetic Resonance Imaging Research Center and Research Center for Lifespan Development of Mind and Brain (CLIMB), Institute of Psychology, Chinese Academy of Sciences, Beijing 100054, China; Department of Child and Adolescent Psychiatry, NYU Langone Medical Center School of Medicine, New York, NY 10016, USA.

Objective

While gastrointestinal (GI) symptoms are very common in patients with major depressive disorder (MDD), few studies have investigated the neural basis behind these symptoms. In this study, we sought to elucidate the neural basis of GI symptoms in MDD patients by analyzing the changes in regional gray matter volume (GMV) and gray matter density (GMD) in brain structure.

Method

Subjects were recruited from 13 clinical centers and categorized into three groups, each of which is based on the presence or absence of GI symptoms: the GI symptoms group (MDD patients with at least one GI symptom), the non-GI symptoms group (MDD patients without any GI symptoms), and the healthy control group (HCs). Structural magnetic resonance images (MRI) were collected of 335 patients in the GI symptoms group, 149 patients in the non-GI symptoms group, and 446 patients in the healthy control group. The 17-item Hamilton Depression Rating Scale (HAMD-17) was administered to all patients. Correlation analysis and logistic regression analysis were used to determine if there was a correlation between the altered brain regions and the clinical symptoms.

Results

There were significantly higher HAMD-17 scores in the GI symptoms group than that of the non-GI symptoms group (P < 0.001). Both GMV and GMD were significant different among the three groups for the bilateral superior temporal gyrus, bilateral middle temporal gyrus, left lingual gyrus, bilateral caudate nucleus, right Fusiform gyrus and bilateral Thalamus (GRF correction, cluster-P < 0.01, voxel-P < 0.001). Compared to the HC group, the GI symptoms group demonstrated increased GMV and GMD in the bilateral superior temporal gyrus, and the non-GI symptoms group demonstrated an increased GMV and GMD in the right superior temporal gyrus, right fusiform gyrus and decreased GMV in the right Caudate nucleus (GRF correction, cluster-P < 0.01, voxel-P < 0.001). Compared to the non-GI symptoms group, the GI symptoms group demonstrated significantly increased GMV and GMD in the bilateral thalamus, as well as decreased GMV in the bilateral superior temporal gyrus and bilateral insula lobe (GRF correction, cluster-P < 0.01, voxel-P < 0.001). While these changed brain areas had significantly association with GI symptoms (P < 0.001), they were not correlated with depressive symptoms (P > 0.05). Risk factors for gastrointestinal symptoms in MDD patients (p < 0.05) included age, increased GMD in the right thalamus, and decreased GMV in the bilateral superior temporal gyrus and left Insula lobe.

Conclusion

MDD patients with GI symptoms have more severe depressive symptoms. MDD patients with GI symptoms exhibited larger GMV and GMD in the bilateral thalamus, and smaller GMV in the bilateral superior temporal gyrus and bilateral insula lobe that were correlated with GI symptoms, and some of them and age may contribute to the presence of GI symptoms in MDD patients.

中文翻译：

伴有胃肠道症状的 MDD 患者的脑结构改变：来自 REST-meta-MDD 项目的证据

客观的

虽然胃肠道 (GI) 症状在重度抑郁症 (MDD) 患者中非常常见，但很少有研究调查这些症状背后的神经基础。在这项研究中，我们试图通过分析大脑结构中区域灰质体积 (GMV) 和灰质密度 (GMD) 的变化来阐明 MDD 患者胃肠道症状的神经基础。

方法

受试者从 13 个临床中心招募并分为三组，每组根据是否存在胃肠道症状：胃肠道症状组（患有至少一种胃肠道症状的 MDD 患者）、非胃肠道症状组（MDD没有任何胃肠道症状的患者）和健康对照组（HCs）。收集了胃肠道症状组335例患者、非胃肠道症状组149例患者和健康对照组446例患者的结构磁共振图像（MRI）。对所有患者进行了 17 项汉密尔顿抑郁评定量表 (HAMD-17)。相关性分析和逻辑回归分析用于确定大脑区域改变与临床症状之间是否存在相关性。

结果

胃肠道症状组HAMD-17评分显着高于非胃肠道症状组（P <0.001）。双侧颞上回、双侧颞中回、左舌回、双侧尾状核、右梭状回和双侧丘脑三组间GMV和GMD均存在显着差异（GRF校正，簇-P <0.01，体素-P < 0.001)。与HC组相比，胃肠道症状组双侧颞上回GMV和GMD升高，非胃肠道症状组右侧颞上回、右侧梭状回GMV和GMD升高，右侧颞上回GMV降低。右尾状核（GRF 校正，簇-P < 0.01，体素- P < 0.001）。与非胃肠道症状组相比，胃肠道症状组双侧丘脑 GMV 和 GMD 显着增加，双侧颞上回和双侧岛叶 GMV 降低（GRF 校正，cluster -P < 0.01，voxel - P < 0.001)。虽然这些改变的脑区与胃肠道症状有显着相关性（P < 0.001），但与抑郁症状无关（P > 0.05）。MDD患者胃肠道症状的危险因素包括年龄、右侧丘脑GMD增加、双侧颞上回和左侧岛叶GMV降低。