Visceral adiposity in postmenopausal women is associated with a pro-inflammatory gut microbiome and immunogenic metabolic endotoxemia

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Reviewed Marked as Reviewed by Svetlana up on 2024-12-14
study design
cross-sectional observational, not case-control
Citation
PMID PubMed identifier for scientific articles.
39367431
DOI Digital object identifier for electronic documents.
10.1186/s40168-024-01901-1
URI
https://pubmed.ncbi.nlm.nih.gov/39367431/
Authors
Gaber M, Wilson AS, Millen AE, Hovey KM, LaMonte MJ, Wactawski-Wende J, Ochs-Balcom HM, Cook KL
Journal
Microbiome
Year
2024
Keywords:
Aging, Inflammation, Leaky gut, Lipopolysaccharide, Menopause, Metabolic endotoxemia, Microbiome, Obesity, Women’s Health Initiative
BACKGROUND: Obesity, and in particular abdominal obesity, is associated with an increased risk of developing a variety of chronic diseases. Obesity, aging, and menopause are each associated with differential shifts in the gut microbiome. Obesity causes chronic low-grade inflammation due to increased lipopolysaccharide (LPS) levels which is termed "metabolic endotoxemia." We examined the association of visceral adiposity tissue (VAT) area, circulating endotoxemia markers, and the gut bacterial microbiome in a cohort of aged postmenopausal women. METHODS: Fifty postmenopausal women (mean age 78.8 ± 5.3 years) who had existing adipose measurements via dual x-ray absorptiometry (DXA) were selected from the extremes of VAT: n = 25 with low VAT area (45.6 ± 12.5 cm2) and n = 25 with high VAT area (177.5 ± 31.3 cm2). Dietary intake used to estimate the Healthy Eating Index (HEI) score was assessed with a food frequency questionnaire. Plasma LPS, LPS-binding protein (LBP), anti-LPS antibodies, anti-flagellin antibodies, and anti-lipoteichoic acid (LTA) antibodies were measured by ELISA. Metagenomic sequencing was performed on fecal DNA. Female C57BL/6 mice consuming a high-fat or low-fat diet were treated with 0.4 mg/kg diet-derived fecal isolated LPS modeling metabolic endotoxemia, and metabolic outcomes were measured after 6 weeks. RESULTS: Women in the high VAT group showed increased Proteobacteria abundance and a lower Firmicutes/Bacteroidetes ratio. Plasma LBP concentration was positively associated with VAT area. Plasma anti-LPS, anti-LTA, and anti-flagellin IgA antibodies were significantly correlated with adiposity measurements. Women with high VAT showed significantly elevated LPS-expressing bacteria compared to low VAT women. Gut bacterial species that showed significant associations with both adiposity and inflammation (anti-LPS IgA and LBP) were Proteobacteria (Escherichia coli, Shigella spp., and Klebsiella spp.) and Veillonella atypica. Healthy eating index (HEI) scores negatively correlated with % body fat and anti-LPS IgA antibodies levels. Preclinical murine model showed that high-fat diet-fed mice administered a low-fat diet fecal-derived LPS displayed reduced body weight, decreased % body fat, and improved glucose tolerance test parameters when compared with saline-injected or high-fat diet fecal-derived LPS-treated groups consuming a high-fat diet. CONCLUSIONS: Increased VAT in postmenopausal women is associated with elevated gut Proteobacteria abundance and immunogenic metabolic endotoxemia markers. Low-fat diet-derived fecal-isolated LPS improved metabolic parameters in high-fat diet-fed mice giving mechanistic insights into potential pro-health signaling mediated by under-acylated LPS isoforms. Video Abstract.

Experiment 1


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Reviewed Marked as Reviewed by Svetlana up on 2024-12-14

Curated date: 2024/10/24

Curator: Vandana Maddi

Revision editor(s): Vandana Maddi, KateRasheed

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
Visceral adipose tissue measurement Visceral adipose tissue measurement,visceral adipose tissue measurement
Group 0 name Corresponds to the control (unexposed) group for case-control studies
Low Visceral Adiposity Tissue (VAT) group (Control/Unexposed group).
Group 1 name Corresponds to the case (exposed) group for case-control studies
High Visceral Adiposity Tissue (VAT) group (Case/Exposed group)
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
The high visceral adiposity tissue (VAT) group represents women with elevated visceral adipose tissue, which is associated with pro-inflammatory gut microbiome characteristics and metabolic endotoxemia
Group 0 sample size Number of subjects in the control (unexposed) group
25
Group 1 sample size Number of subjects in the case (exposed) group
25
Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any)
3 months

Lab analysis

Sequencing type
WMS
16S variable region One or more hypervariable region(s) of the bacterial 16S gene
Not specified
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
Mann-Whitney (Wilcoxon)
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)?
No
Matched on Factors on which subjects have been matched on in a case-control study
age, 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

Signature 1

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Curated date: 2024/10/24

Curator: Vandana Maddi

Revision editor(s): Vandana Maddi, KateRasheed

Source: Fig. 3E, Fig. 4b

Description: Differential abundant taxa between women with Low Visceral Adiposity Tissue and High Visceral Adiposity Tissue

Abundance in Group 1: increased abundance in High Visceral Adiposity Tissue (VAT) group (Case/Exposed group)

NCBI Quality ControlLinks
Emergencia   
Klebsiella   
Parabacteroides   
Parasutterella   
Pseudomonadota   
Shigella   
uncultured Burkholderia sp.   

Revision editor(s): Vandana Maddi, KateRasheed

Signature 2

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Reviewed Marked as Reviewed by ChiomaBlessing on 2024-11-28

Curated date: 2024/10/24

Curator: Vandana Maddi

Revision editor(s): Vandana Maddi, KateRasheed

Source: Fig. 4b

Description: Differential abundant taxa between women with Low Visceral Adiposity Tissue and High Visceral Adiposity Tissue

Abundance in Group 1: decreased abundance in High Visceral Adiposity Tissue (VAT) group (Case/Exposed group)

NCBI Quality ControlLinks
Anaerostipes   
Barnesiella   
Desulfovibrio   
Intestinimonas   
Massiliimalia   
Negativibacillus   

Revision editor(s): Vandana Maddi, KateRasheed

Experiment 2


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Reviewed Marked as Reviewed by Svetlana up on 2024-12-14

Curated date: 2024/10/24

Curator: Vandana Maddi

Revision editor(s): Vandana Maddi, KateRasheed

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
Low Visceral Adiposity Tissue (VAT) group with Lipopolysaccharide (LPS)-containing bacteria
Group 1 name Corresponds to the case (exposed) group for case-control studies
High Visceral Adiposity Tissue (VAT) group with Lipopolysaccharide (LPS)-containing bacteria
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
High Visceral Adiposity Tissue (VAT) group with Lipopolysaccharide (LPS)-containing bacteria represents women with elevated visceral adipose tissue having LPS-containing bacteria as defined by lpxA and lpxB gene expression.

Lab analysis

Statistical Analysis

Signature 1

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Reviewed Marked as Reviewed by Svetlana up on 2024-12-14

Curated date: 2024/10/24

Curator: Vandana Maddi

Revision editor(s): Vandana Maddi, KateRasheed

Source: Fig. 6E

Description: Differential abundant taxa between women with Low Visceral Adiposity Tissue and High Visceral Adiposity Tissue with LPS-containing bacteria

Abundance in Group 1: increased abundance in High Visceral Adiposity Tissue (VAT) group with Lipopolysaccharide (LPS)-containing bacteria

NCBI Quality ControlLinks
Pseudomonadota   

Revision editor(s): Vandana Maddi, KateRasheed

Signature 2

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Reviewed Marked as Reviewed by Svetlana up on 2024-12-14

Curated date: 2024/10/24

Curator: Vandana Maddi

Revision editor(s): Vandana Maddi, KateRasheed

Source: Fig. 6B

Description: Differential abundant taxa between women with Low Visceral Adiposity Tissue and High Visceral Adiposity Tissue with LPS-containing bacteria

Abundance in Group 1: decreased abundance in High Visceral Adiposity Tissue (VAT) group with Lipopolysaccharide (LPS)-containing bacteria

NCBI Quality ControlLinks
Alistipes   

Revision editor(s): Vandana Maddi, KateRasheed

Experiment 3


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Your review change was submittedDuplicate this ExperimentAdd a new Signature
Reviewed Marked as Reviewed by ChiomaBlessing on 2024-11-28

Curated date: 2024/10/24

Curator: Vandana Maddi

Revision editor(s): Vandana Maddi, KateRasheed

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
Low Visceral Adiposity Tissue (VAT) group (Control/Unexposed group).
Group 1 name Corresponds to the case (exposed) group for case-control studies
High Visceral Adiposity Tissue (VAT) group (Case/Exposed group)
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
The high visceral adiposity tissue (VAT) group represents women with elevated visceral adipose tissue, which is associated with pro-inflammatory gut microbiome characteristics and metabolic endotoxemia

Lab analysis

Statistical Analysis

Statistical test
LEfSe
LDA Score above Threshold for the linear discriminant analysis (LDA) score for studies using the popular LEfSe tool
2

Alpha Diversity

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

Signature 1

EditHistoryDelete
Flag for review
Your review change was submitted
Reviewed Marked as Reviewed by ChiomaBlessing on 2024-11-28

Curated date: 2024/10/24

Curator: Vandana Maddi

Revision editor(s): Vandana Maddi, KateRasheed

Source: Fig. 4D

Description: Differential abundant taxa between women with Low Visceral Adiposity Tissue and High Visceral Adiposity Tissue using LEfSe

Abundance in Group 1: increased abundance in High Visceral Adiposity Tissue (VAT) group (Case/Exposed group)

NCBI Quality ControlLinks
uncultured Burkholderia sp.   
Parasutterella excrementihominis   
Bacteroides ovatus   
Phocaeicola vulgatus   
Parabacteroides distasonis   
uncultured Paraburkholderia sp.   

Revision editor(s): Vandana Maddi, KateRasheed

Signature 2

EditHistoryDelete
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Your review change was submitted
Reviewed Marked as Reviewed by ChiomaBlessing on 2024-11-28

Curated date: 2024/10/24

Curator: Vandana Maddi

Revision editor(s): Vandana Maddi, KateRasheed

Source: Fig. 4D

Description: Differential abundant taxa between women with Low Visceral Adiposity Tissue and High Visceral Adiposity Tissue using LEfSe

Abundance in Group 1: decreased abundance in High Visceral Adiposity Tissue (VAT) group (Case/Exposed group)

NCBI Quality ControlLinks
Xylanibacter rarus   
Victivallis vadensis   
Intestinimonas massiliensis (ex Afouda et al. 2020)   
Negativibacillus massiliensis   
uncultured Bifidobacterium sp.   
Bacteroides timonensis   
Bacteroides cellulosilyticus   
Barnesiella intestinihominis   
uncultured Firmicutes bacterium   

Revision editor(s): Vandana Maddi, KateRasheed

Experiment 4


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Reviewed Marked as Reviewed by Svetlana up on 2024-12-14

Curated date: 2024/10/24

Curator: Vandana Maddi

Revision editor(s): Vandana Maddi, KateRasheed

Differences from previous experiment shown

Subjects

Lab analysis

Statistical Analysis

Statistical test
Pearson Correlation
LDA Score above Threshold for the linear discriminant analysis (LDA) score for studies using the popular LEfSe tool
Not specified

Alpha Diversity

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

Signature 1

EditHistoryDelete
Flag for review
Your review change was submitted
Reviewed Marked as Reviewed by Svetlana up on 2024-12-14

Curated date: 2024/10/24

Curator: Vandana Maddi

Revision editor(s): Vandana Maddi, KateRasheed

Source: Figure 4C + Within text (Under 'Results' section, Paragraph 4, Line 2)

Description: Differential abundant taxa between women with Low Visceral Adiposity Tissue and High Visceral Adiposity Tissue using Pearson Heatmap

Abundance in Group 1: increased abundance in High Visceral Adiposity Tissue (VAT) group (Case/Exposed group)

NCBI Quality ControlLinks
Dorea longicatena DSM 13814   
Parabacteroides distasonis ATCC 8503   
Roseburia intestinalis L1-82   
unclassified Shigella   

Revision editor(s): Vandana Maddi, KateRasheed

Signature 2

EditHistoryDelete
Flag for review
Your review change was submitted
Reviewed Marked as Reviewed by ChiomaBlessing on 2024-11-28

Curated date: 2024/10/24

Curator: Vandana Maddi

Revision editor(s): Vandana Maddi, KateRasheed

Source: Figure 4C + Within text (Under 'Results' section, Paragraph 4, Line 2)

Description: Differential abundant taxa between women with Low Visceral Adiposity Tissue and High Visceral Adiposity Tissue using Pearson heatmap

Abundance in Group 1: decreased abundance in High Visceral Adiposity Tissue (VAT) group (Case/Exposed group)

NCBI Quality ControlLinks
Alistipes shahii WAL 8301   
Anaerostipes hadrus ATCC 29173 = JCM 17467   
Blautia wexlerae DSM 19850   
Clostridiaceae bacterium AF42-6   
Clostridiaceae bacterium OF09-1   
Lachnospiraceae bacterium AM21-21   
Lachnospiraceae bacterium AM26-1LB   
Lachnospiraceae bacterium GAM79   
Lachnospiraceae bacterium OF09-33XD   
Negativibacillus massiliensis   
Ruminococcaceae bacterium AM28-23LB   

Revision editor(s): Vandana Maddi, KateRasheed

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