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Weighted Gene Co-Expression Network Analysis Identifies a Functional Guild and Metabolite Cluster Mediating the Relationship between Mucosal Inflammation and Adherence to the Mediterranean Diet in Ulcerative Colitis.

ABSTRACT: Diet influences the pathogenesis and clinical course of inflammatory bowel disease (IBD). The Mediterranean diet (MD) is linked to reductions in inflammatory biomarkers and alterations in microbial taxa and metabolites associated with health. We aimed to identify features of the gut microbiome that mediate the relationship between the MD and fecal calprotectin (FCP) in ulcerative colitis (UC). Weighted gene co-expression network analysis (WGCNA) was used to identify modules of co-abundant microbial taxa and metabolites correlated with the MD and FCP. The features considered were gut microbial taxa, serum metabolites, dietary components, short-chain fatty acid and bile acid profiles in participants that experienced an increase (n = 13) or decrease in FCP (n = 16) over eight weeks. WGCNA revealed ten modules containing sixteen key features that acted as key mediators between the MD and FCP. Three taxa (Faecalibacterium prausnitzii, Dorea longicatena, Roseburia inulinivorans) and a cluster of four metabolites (benzyl alcohol, 3-hydroxyphenylacetate, 3-4-hydroxyphenylacetate and phenylacetate) demonstrated a strong mediating effect (ACME: -1.23, p = 0.004). This study identified a novel association between diet, inflammation and the gut microbiome, providing new insights into the underlying mechanisms of how a MD may influence IBD. See clinicaltrials.gov (NCT04474561).

SUBMITTER: Strauss JC

PROVIDER: S-EPMC10138710 | biostudies-literature | 2023 Apr

REPOSITORIES: biostudies-literature

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Weighted Gene Co-Expression Network Analysis Identifies a Functional Guild and Metabolite Cluster Mediating the Relationship between Mucosal Inflammation and Adherence to the Mediterranean Diet in Ulcerative Colitis.

Strauss Jaclyn C JC Haskey Natasha N Ramay Hena R HR Ghosh Tarini Shankar TS Taylor Lorian M LM Yousuf Munazza M Ohland Christina C McCoy Kathy D KD Ingram Richard J M RJM Ghosh Subrata S Panaccione Remo R Raman Maitreyi M

International journal of molecular sciences 20230415 8

Diet influences the pathogenesis and clinical course of inflammatory bowel disease (IBD). The Mediterranean diet (MD) is linked to reductions in inflammatory biomarkers and alterations in microbial taxa and metabolites associated with health. We aimed to identify features of the gut microbiome that mediate the relationship between the MD and fecal calprotectin (FCP) in ulcerative colitis (UC). Weighted gene co-expression network analysis (WGCNA) was used to identify modules of co-abundant microb ...[more]

PMID: 37108484

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Project description:ObjectiveThe pathogenesis of UC relates to gut microbiota dysbiosis. We postulate that alterations in the viral community populating the intestinal mucosa play an important role in UC pathogenesis. This study aims to characterise the mucosal virome and their functions in health and UC.DesignDeep metagenomics sequencing of virus-like particle preparations and bacterial 16S rRNA sequencing were performed on the rectal mucosa of 167 subjects from three different geographical regions in China (UC=91; healthy controls=76). Virome and bacteriome alterations in UC mucosa were assessed and correlated with patient metadata. We applied partition around medoids clustering algorithm and classified mucosa viral communities into two clusters, referred to as mucosal virome metacommunities 1 and 2.ResultsIn UC, there was an expansion of mucosa viruses, particularly Caudovirales bacteriophages, and a decrease in mucosa Caudovirales diversity, richness and evenness compared with healthy controls. Altered mucosal virome correlated with intestinal inflammation. Interindividual dissimilarity between mucosal viromes was higher in UC than controls. Escherichia phage and Enterobacteria phage were more abundant in the mucosa of UC than controls. Compared with metacommunity 1, metacommunity 2 was predominated by UC subjects and displayed a significant loss of various viral species. Patients with UC showed substantial abrogation of diverse viral functions, whereas multiple viral functions, particularly functions of bacteriophages associated with host bacteria fitness and pathogenicity, were markedly enriched in UC mucosa. Intensive transkingdom correlations between mucosa viruses and bacteria were significantly depleted in UC.ConclusionWe demonstrated for the first time that UC is characterised by substantial alterations of the mucosa virobiota with functional distortion. Enrichment of Caudovirales bacteriophages, increased phage/bacteria virulence functions and loss of viral-bacterial correlations in the UC mucosa highlight that mucosal virome may play an important role in UC pathogenesis.

Project description:BackgroundThe Mediterranean diet pattern (MDP) is believed to improve health and promote balanced inflammation and metabolism. While unknown, compelling evidence suggests that MDP could benefit patients with inflammatory bowel disease (IBD). We aimed to evaluate the level of diet adherence, diet quality, and nutritional adequacy of the MDP in patients with Ulcerative Colitis (UC).MethodsAdult participants (n = 32) with quiescent UC were randomized to follow a MDP (n = 18) or Canadian Habitual Diet (CHD) (n = 14) for 12 weeks. The MDP participants received tailored nutrition education from a Registered Dietitian. Demographic, clinical data, medical history, and quality of life were assessed with the Short Inflammatory Bowel Disease Questionnaire (SIBDQ), dietary adherence with the Mediterranean Diet Serving Score (MDSS), diet quality via the Healthy Eating Index-2015 (HEI-2015), and dietary intake (ASA-24) were completed at baseline and week 12.ResultsParticipants' diets were analyzed (MDP n = 15, CHD n = 13). The MDP (n = 10, 67%) achieved a high level of adherence (MDSS score between 16 and 24) vs. CHD (n = 3), (p = 0.030). HEI-2015 significantly increased from baseline to week 12 (p = 0.007) in the MDP and was significantly higher at week 12 compared to the CHD (p = 0.0001). The SIBDQ (bowel domain) showed reductions in the passage of large amounts of gas (p = 0.01) and improvements in tenesmus (p = 0.03) in the MDP. Despite enhanced diet quality and adherence in the MDP, females had inadequate intakes of calcium, iron, vitamin D, vitamin E, and choline and males had inadequate intakes of fiber, vitamin D, vitamin E, and choline. No adverse events were reported.ConclusionWith nutrition education, high adherence to the MDP was achieved without an increase in bowel symptoms. Following the MDP led to a higher diet quality; however, nutritional inadequacies were identified. Tailored dietary education focusing on nutrients of concern when following the MDP is recommended to ensure nutritional adequacy.Clinical trial registration[www.ClinicalTrials.gov], identifier [NCT03053713].

Dataset Information

Weighted Gene Co-Expression Network Analysis Identifies a Functional Guild and Metabolite Cluster Mediating the Relationship between Mucosal Inflammation and Adherence to the Mediterranean Diet in Ulcerative Colitis.

Publications

Weighted Gene Co-Expression Network Analysis Identifies a Functional Guild and Metabolite Cluster Mediating the Relationship between Mucosal Inflammation and Adherence to the Mediterranean Diet in Ulcerative Colitis.

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