Association of aberrant brain network dynamics with gut microbial composition uncovers disrupted brain-gut-microbiome interactions in irritable bowel syndrome: Preliminary findings

Study information

Reviewed Marked as Reviewed by Svetlana up on 2025-4-17

study design

case-control

Citation

PMID PubMed identifier for scientific articles.

36905309

DOI Digital object identifier for electronic documents.

https://doi.org/10.1111/ene.15776

URI Uniform resource identifier for web resources.

Authors

Yang L, Liu G, Li S, Yao C, Zhao Z, Chen N, Zhang P, Shang Y, Wang Y, Zhang D, Tian X, Zhang J, Yao Z, Hu B

Journal

European journal of neurology

Year

2023

Keywords:

brain-gut-microbiome axis, dynamic functional connectivity, gut microbiome, irritable bowel syndrome, resting-state functional MRI

BACKGROUND AND PURPOSE: Growing evidence suggests that abnormalities in brain-gut-microbiome (BGM) interactions are involved in the pathogenesis of irritable bowel syndrome (IBS). Our study aimed to explore alterations in dynamic functional connectivity (DFC), the gut microbiome and the bidirectional interaction in the BGM. METHODS: Resting-state functional magnetic resonance imaging (rs-fMRI), fecal samples and clinical chacteristics were collected from 33 IBS patients and 32 healthy controls. We performed a systematic DFC analysis on rs-fMRI. The gut microbiome was analyzed by 16S rRNA gene sequencing. Associations between DFC characteristics and microbial alterations were explored. RESULTS: In the DFC analysis, four dynamic functional states were identified. IBS patients exhibited increased mean dwell and fraction time in State 4, and reduced transitions from State 3 to State 1. Aberrant temporal properties in State 4 were only evident when choosing a short window (36 s or 44 s). Decreased functional connectivity (FC) variability was found in State 1 and State 3 in IBS patients, two of which (independent component [IC]51-IC91, IC46-IC11) showed significant correlations with clinical characteristics. Additionally, we identified nine significantly differential abundances in microbial composition. We also found that IBS-related microbiota were associated with aberrant FC variability, although these exploratory results were obtained at an uncorrected threshold of significance. CONCLUSIONS: Although future studies are needed to confirm our results, the findings not only provide a new insight into the dysconnectivity hypothesis in IBS from a dynamic perspective, but also establish a possible link between DFC and the gut microbiome, which lays the foundation for future research on disrupted BGM interactions.

Experiment 1

Edit History Delete

Flag for review

Your review change was submittedDuplicate this Experiment Add a new Signature

Reviewed Marked as Reviewed by Svetlana up on 2025-4-17

Curated date: 2025/04/13

Curator: Aiyshaaaa

Revision editor(s): Aiyshaaaa

Subjects

Location of subjects: China

Host species Species from which microbiome was sampled. Contact us to have more species added.: Homo sapiens

Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology: Feces Cow dung,Cow pat,Droppings,Dung,Excrement,Excreta,Faeces,Fecal material,Fecal matter,Fewmet,Frass,Guano,Matières fécales@fr,Merde@fr,Ordure,Partie de la merde@fr,Piece of shit,Porción de mierda@es,Portion of dung,Portion of excrement,Portion of faeces,Portion of fecal material,Portion of fecal matter,Portion of feces,Portion of guano,Portion of scat,Portionem cacas,Scat,Spoor,Spraint,Stool,Teil der fäkalien@de,Feces,feces

Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology: Irritable bowel syndrome [X]Psychogenic IBS,Adaptive colitis,Colitides, Mucous,Colitis, Mucous,Colon spasm,Colon, Irritable,Functional bowel disease,IBD,IBS,IBS - Irritable bowel syndrome,IC - Irritable colon,Irritable bowel,Irritable bowel - IBS,irritable bowel syndrome,Irritable Bowel Syndromes,Irritable Colon,irritable colon,Irritable colon (disorder),Irritable colon - Irritable bowel syndrome,Irritable colon syndrome,Membranous colitis,Mucous Colitides,Mucous colitis,mucus colitis,Nervous colitis,Psychogenic IBS,psychogenic IBS,Spastic colitis,Spastic colon,spastic colon,Syndrome, Irritable Bowel,Syndromes, Irritable Bowel,Irritable bowel syndrome

Group 0 name Corresponds to the control (unexposed) group for case-control studies: Healthy Controls (HC)

Group 1 name Corresponds to the case (exposed) group for case-control studies: IBS patients (Irritable Bowel Syndrome)

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group: Patients who have been diagnosed with irritable bowel syndrome (IBS)

Group 0 sample size Number of subjects in the control (unexposed) group: 32

Group 1 sample size Number of subjects in the case (exposed) group: 33

Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any): 1 month

Lab analysis

Sequencing type: 16S

16S variable region One or more hypervariable region(s) of the bacterial 16S gene: V3-V4

Sequencing platform Manufacturer and experimental platform used for quantifying microbial abundance: Illumina

Statistical Analysis

Data transformation Data transformation applied to microbial abundance measurements prior to differential abundance testing (if any).: raw counts

Statistical test: DESeq2

Significance threshold p-value or FDR threshold used for differential abundance testing (if any): 0.05

MHT correction Have statistical tests be corrected for multiple hypothesis testing (MHT)?: Yes

Matched on Factors on which subjects have been matched on in a case-control study: age, sex

Alpha Diversity

Pielou Quantifies how equal the community is numerically: unchanged

Shannon Estimator of species richness and species evenness: more weight on species richness: decreased

Richness Number of species: unchanged

Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample: unchanged

Signature 1

Edit History Delete

Flag for review

Your review change was submitted

Reviewed Marked as Reviewed by Svetlana up on 2025-4-17

Curated date: 2025/04/13

Curator: Aiyshaaaa

Revision editor(s): Aiyshaaaa

Source: Fig-5c and Table-S3

Description: Relative abundance in gut microbiota at genus and family level between healthy controls and irritable bowel syndrome patients

Abundance in Group 1: increased abundance in IBS patients (Irritable Bowel Syndrome)

NCBI	Quality Control	Links
Anaerostipes
Erysipelotrichaceae
Ruminococcus
Streptococcus

Revision editor(s): Aiyshaaaa

Signature 2

Edit History Delete

Flag for review

Your review change was submitted

Reviewed Marked as Reviewed by Svetlana up on 2025-4-17

Curated date: 2025/04/13

Curator: Aiyshaaaa

Revision editor(s): Aiyshaaaa

Source: Fig-5c and Table-S3

Description: Relative abundance in gut microbiota at genus and family level between healthy controls and irritable bowel syndrome patients

Abundance in Group 1: decreased abundance in IBS patients (Irritable Bowel Syndrome)

NCBI	Quality Control	Links
Barnesiellaceae
Oscillospira
Rikenellaceae
Christensenellaceae
Oscillospiraceae

Revision editor(s): Aiyshaaaa