Alterations of gut microbiota are associated with brain structural changes in the spectrum of Alzheimer's disease: the SILCODE study in Hainan cohort

Beiqi He; Can Sheng; Xianfeng Yu; Liang Zhang; Feng Chen; Ying Han

doi:10.3389/fnagi.2023.1216509

Alterations of gut microbiota are associated with brain structural changes in the spectrum of Alzheimer's disease: the SILCODE study in Hainan cohort

Front Aging Neurosci. 2023 Jul 14:15:1216509. doi: 10.3389/fnagi.2023.1216509. eCollection 2023.

Authors

Beiqi He¹, Can Sheng², Xianfeng Yu³, Liang Zhang¹, Feng Chen⁴, Ying Han^{1

3

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Affiliations

¹ School of Biomedical Engineering, Hainan University, Haikou, China.
² Department of Neurology, The Affiliated Hospital of Jining Medical University, Jining, China.
³ Department of Neurology, Xuanwu Hospital of Capital Medical University, Beijing, China.
⁴ Department of Radiology, Hainan General Hospital (Hainan Affiliated Hospital of Hainan Medical University), Haikou, China.
⁵ Center of Alzheimer's Disease, Beijing Institute for Brain Disorders, Beijing, China.
⁶ National Clinical Research Center for Geriatric Disorders, Beijing, China.

Abstract

Background: The correlation between gut microbiota and Alzheimer's disease (AD) is increasingly being recognized by clinicians. However, knowledge about the gut-brain-cognition interaction remains largely unknown.

Methods: One hundred and twenty-seven participants, including 35 normal controls (NCs), 62 with subjective cognitive decline (SCD), and 30 with cognitive impairment (CI), were included in this study. The participants underwent neuropsychological assessments and fecal microbiota analysis through 16S ribosomal RNA (rRNA) Illumina Miseq sequencing technique. Structural MRI data were analyzed for cortical anatomical features, including thickness, sulcus depth, fractal dimension, and Toro's gyrification index using the SBM method. The association of altered gut microbiota among the three groups with structural MRI metrics and cognitive function was evaluated. Furthermore, co-expression network analysis was conducted to investigate the gut-brain-cognition interactions.

Results: The abundance of Lachnospiraceae, Lachnospiracea_incertae_sedis, Fusicatenibacter, and Anaerobutyricum decreased with cognitive ability. Rikenellaceae, Odoribacteraceae, and Alistipes were specifically enriched in the CI group. Mediterraneibacter abundance was correlated with changes in brain gray matter and cerebrospinal fluid volume (p = 0.0214, p = 0.0162) and significantly with changes in cortical structures in brain regions, such as the internal olfactory area and the parahippocampal gyrus. The three colonies enriched in the CI group were positively correlated with cognitive function and significantly associated with changes in cortical structure related to cognitive function, such as the precuneus and syrinx gyrus.

Conclusion: This study provided evidence that there was an inner relationship among the altered gut microbiota, brain atrophy, and cognitive decline. Targeting the gut microbiota may be a novel therapeutic strategy for early AD.

Keywords: 16S ribosomal RNA; Alzheimer's disease; brain structural; gut microbiota; magnetic resonance imaging.

Grants and funding

This study was supported by STI2030-Major Projects (2022ZD0211800), the National Natural Science Foundation of China (Grant No. 82020108013), the Sino-German Cooperation Grant (M-0759), the Science and Technology Development Plan Project of Shandong Medical and Health (Grant No. 202203070774), and the Doctoral Research Fund Project in the Affiliated Hospital of Jining Medical University (Grant No. 2022-BS-02).