Cerebral small vessel disease burden is associated with decreased abundance of gut Barnesiella intestinihominis bacterium in the Framingham Heart Study

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Reviewed Marked as Reviewed by Folakunmi on 2024-1-23
study design
cross-sectional observational, not case-control
Citation
PMID PubMed identifier for scientific articles.
37604954
DOI Digital object identifier for electronic documents.
https://doi.org/10.1038/s41598-023-40872-5
URI
Authors
Fongang B, Satizabal C, Kautz TF, Wadop YN, Muhammad JAS, Vasquez E, Mathews J, Gireud-Goss M, Saklad AR, Himali J, Beiser A, Cavazos JE, Mahaney MC, Maestre G, DeCarli C, Shipp EL, Vasan RS, Seshadri S
Journal
Scientific reports
Year
2023
A bidirectional communication exists between the brain and the gut, in which the gut microbiota influences cognitive function and vice-versa. Gut dysbiosis has been linked to several diseases, including Alzheimer's disease and related dementias (ADRD). However, the relationship between gut dysbiosis and markers of cerebral small vessel disease (cSVD), a major contributor to ADRD, is unknown. In this cross-sectional study, we examined the connection between the gut microbiome, cognitive, and neuroimaging markers of cSVD in the Framingham Heart Study (FHS). Markers of cSVD included white matter hyperintensities (WMH), peak width of skeletonized mean diffusivity (PSMD), and executive function (EF), estimated as the difference between the trail-making tests B and A. We included 972 FHS participants with MRI scans, neurocognitive measures, and stool samples and quantified the gut microbiota composition using 16S rRNA sequencing. We used multivariable association and differential abundance analyses adjusting for age, sex, BMI, and education level to estimate the association between gut microbiota and WMH, PSMD, and EF measures. Our results suggest an increased abundance of Pseudobutyrivibrio and Ruminococcus genera was associated with lower WMH and PSMD (p values < 0.001), as well as better executive function (p values < 0.01). In addition, in both differential and multivariable analyses, we found that the gram-negative bacterium Barnesiella intestinihominis was strongly associated with markers indicating a higher cSVD burden. Finally, functional analyses using PICRUSt implicated various KEGG pathways, including microbial quorum sensing, AMP/GMP-activated protein kinase, phenylpyruvate, and β-hydroxybutyrate production previously associated with cognitive performance and dementia. Our study provides important insights into the association between the gut microbiome and cSVD, but further studies are needed to replicate the findings.

Experiment 1


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Reviewed Marked as Reviewed by Folakunmi on 2024-1-23

Curated date: 2023/10/08

Curator: Sinmisoluwa Adesanya

Revision editor(s): Sinmisoluwa Adesanya, Folakunmi

Subjects

Location of subjects
United States of America
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
Cerebral small vessel disease genetic cerebral small vessel disease,small vessel cerebrovascular disease,Cerebral small vessel disease,cerebral small vessel disease
Group 0 name Corresponds to the control (unexposed) group for case-control studies
Lower burden (Healthy)
Group 1 name Corresponds to the case (exposed) group for case-control studies
High burden (Unhealthy)
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Participants with Cerebral small vessel disease that were tested using the PSMD marker
Group 0 sample size Number of subjects in the control (unexposed) group
674
Group 1 sample size Number of subjects in the case (exposed) group
108
Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any)
unspecified

Lab analysis

Sequencing type
16S
16S variable region One or more hypervariable region(s) of the bacterial 16S gene
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).
relative abundances
Statistical test
MaAsLin2
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, body mass index, time, education level, sex

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Chao1 Abundance-based estimator of species richness
unchanged
Simpson Estimator of species richness and species evenness: more weight on species evenness
unchanged

Signature 1

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Reviewed Marked as Reviewed by Folakunmi on 2024-1-23

Curated date: 2023/10/14

Curator: Sinmisoluwa Adesanya

Revision editor(s): Peace Sandy, Folakunmi, Sinmisoluwa Adesanya, Chinelsy, Welile

Source: Table S4, S5, S6

Description: Difference between the gut microbiome of patients with cSVD marker PSMD and the Lower burden (Healthy) group at phylum, genus and species rank

Abundance in Group 1: increased abundance in High burden (Unhealthy)

NCBI Quality ControlLinks
Christensenella   
Clostridium ruminantium   
Enterocloster aldenensis   
Oscillospira   
Oscillospira guilliermondii   
Erysipelotrichaceae   

Revision editor(s): Peace Sandy, Folakunmi, Sinmisoluwa Adesanya, Chinelsy, Welile

Signature 2

EditHistoryDelete
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Reviewed Marked as Reviewed by Folakunmi on 2024-1-23

Curated date: 2023/10/14

Curator: Sinmisoluwa Adesanya

Revision editor(s): Sinmisoluwa Adesanya, Chinelsy, Peace Sandy, Folakunmi

Source: Table S4, S5, S6

Description: Difference between the gut microbiome of patients with cSVD marker PSMD and the Lower burden (Healthy) group at phylum, genus and species rank

Abundance in Group 1: decreased abundance in High burden (Unhealthy)

NCBI Quality ControlLinks
Candidatus Poribacteria   
Clostridium   
Methanobrevibacter   
Victivallis   

Revision editor(s): Sinmisoluwa Adesanya, Chinelsy, Peace Sandy, Folakunmi

Experiment 2


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Reviewed Marked as Reviewed by Folakunmi on 2024-1-23

Curated date: 2023/10/15

Curator: Sinmisoluwa Adesanya

Revision editor(s): Sinmisoluwa Adesanya, Folakunmi

Differences from previous experiment shown

Subjects

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Participants with Cerebral small vessel disease that were tested using the WMH marker
Group 0 sample size Number of subjects in the control (unexposed) group
832
Group 1 sample size Number of subjects in the case (exposed) group
136

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Chao1 Abundance-based estimator of species richness
unchanged
Simpson Estimator of species richness and species evenness: more weight on species evenness
unchanged

Signature 1

EditHistoryDelete
Flag for review
Your review change was submitted
Reviewed Marked as Reviewed by Folakunmi on 2024-1-23

Curated date: 2023/10/15

Curator: Sinmisoluwa Adesanya

Revision editor(s): Sinmisoluwa Adesanya, Chinelsy, Folakunmi

Source: Table S4, S5, S6

Description: Difference between the gut microbiome of patients with cSVD marker PSMD and the Lower burden (Healthy) group at phylum, genus and species rank

Abundance in Group 1: increased abundance in High burden (Unhealthy)

NCBI Quality ControlLinks
Christensenella   
Enterocloster aldenensis   
Pseudomonadota   

Revision editor(s): Sinmisoluwa Adesanya, Chinelsy, Folakunmi

Signature 2

EditHistoryDelete
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Your review change was submitted
Reviewed Marked as Reviewed by Folakunmi on 2024-1-23

Curated date: 2023/10/15

Curator: Sinmisoluwa Adesanya

Revision editor(s): Sinmisoluwa Adesanya, Chinelsy, Folakunmi, Welile

Source: Table S4, S5, S6

Description: Difference between the gut microbiome of patients with cSVD marker PSMD and the Lower burden (Healthy) group at phylum, genus and species rank

Abundance in Group 1: decreased abundance in High burden (Unhealthy)

NCBI Quality ControlLinks
Actinomycetota   
Anaerosinus   
Bacillota   
Bacteroidia   
Barnesiella   
Barnesiella intestinihominis   
Candidatus Parcubacteria   
Catenibacterium   
Catenibacterium mitsuokai   
Clostridium   
Clostridium ruminantium   
Lachnotalea glycerini   
Methanobrevibacter   
Oscillospira   
Ruminococcus   
[Ruminococcus] lactaris   
Erysipelotrichaceae   

Revision editor(s): Sinmisoluwa Adesanya, Chinelsy, Folakunmi, Welile

Experiment 3


EditHistoryDelete
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Your review change was submittedDuplicate this ExperimentAdd a new Signature
Reviewed Marked as Reviewed by Folakunmi on 2024-1-23

Curated date: 2023/10/15

Curator: Sinmisoluwa Adesanya

Revision editor(s): Sinmisoluwa Adesanya, Folakunmi

Differences from previous experiment shown

Subjects

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Participants with Cerebral small vessel disease that were tested using the EF marker
Group 0 sample size Number of subjects in the control (unexposed) group
822
Group 1 sample size Number of subjects in the case (exposed) group
121

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Chao1 Abundance-based estimator of species richness
unchanged
Simpson Estimator of species richness and species evenness: more weight on species evenness
unchanged

Signature 1

EditHistoryDelete
Flag for review
Your review change was submitted
Reviewed Marked as Reviewed by Folakunmi on 2024-1-23

Curated date: 2023/10/15

Curator: Sinmisoluwa Adesanya

Revision editor(s): Sinmisoluwa Adesanya, Chinelsy, Folakunmi

Source: Table S4, S5, S6

Description: Difference between the gut microbiome of patients with cSVD marker PSMD and the Lower burden (Healthy) group at phylum, genus and species rank

Abundance in Group 1: increased abundance in High burden (Unhealthy)

NCBI Quality ControlLinks
Catenibacterium   
Clostridium ruminantium   
Collinsella   
Collinsella aerofaciens   
Enterocloster aldenensis   
Enterocloster lavalensis   

Revision editor(s): Sinmisoluwa Adesanya, Chinelsy, Folakunmi

Signature 2

EditHistoryDelete
Flag for review
Your review change was submitted
Reviewed Marked as Reviewed by Folakunmi on 2024-1-23

Curated date: 2023/10/15

Curator: Sinmisoluwa Adesanya

Revision editor(s): Sinmisoluwa Adesanya, Chinelsy, Folakunmi

Source: Table S4, S5, S6

Description: Difference between the gut microbiome of patients with cSVD marker PSMD and the Lower burden (Healthy) group at phylum, genus and species rank

Abundance in Group 1: decreased abundance in High burden (Unhealthy)

NCBI Quality ControlLinks
Alistipes   
Bacillota   
Candidatus Parcubacteria   
Methanobrevibacter   
Ruminococcus   
[Ruminococcus] lactaris   

Revision editor(s): Sinmisoluwa Adesanya, Chinelsy, Folakunmi

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