Dialister -driven succinate accumulation is associated with disease activity and postoperative recurrence in Crohn's disease

Succinate, a metabolite produced by both the gut microbiota and the host, has emerged as a key player in chronic inflammation. In patients with Crohn's disease (CD), increased succinate in the intestinal lumen correlates with both dysbiosis and greater disease activity. To investigate circulati...

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Autores: Boronat-Toscano, Albert|||0000-0003-2650-156X, Queipo-Ortuño, Maribel|||0000-0002-2867-0845, Monfort-Ferré, Diandra|||0000-0003-3832-4249, Suau, Roger|||0000-0003-3754-4768, Vañó-Segarra, Irene, Valldosera, Gemma, Cepero, Claudia, Astiarraga, Brenno|||0000-0003-2216-8974, Clua-Ferré, Laura, Plaza-Andrade, Isaac, Aranega-Martín, Lucía, Cabrinety, Lidia, Abadia de Barbarà, Carme, Castellano, Daniel|||0000-0002-9106-0687, Moliné, Alicia, Caro, Aleidis|||0000-0001-6151-3879, Domènech, Eugeni|||0000-0002-2315-7196, Sánchez Herrero, José Francisco|||0000-0001-6771-4807, Benaiges-Fernandez, Robert|||0000-0003-4691-8290, Fernández-Veledo, Sonia|||0000-0003-2906-3788, Vendrell, Joan|||0000-0002-6994-6115, Sumoy, Lauro|||0000-0003-0005-4618, Manyé, Josep|||0000-0002-3121-8016, Menacho, Margarita, Serena, Carolina|||0000-0003-2251-0856
Tipo de recurso: artículo
Fecha de publicación:2025
País:España
Institución:Universitat Autònoma de Barcelona
Repositorio:Dipòsit Digital de Documents de la UAB
Idioma:inglés
OAI Identifier:oai:dnet:uabarcelona_::2d50ed12b5cc7c002723826725f1ffa4
Acceso en línea:https://ddd.uab.cat/record/327818
https://dx.doi.org/urn:doi:10.3748/wjg.v31.i45.112618
Access Level:acceso abierto
Palabra clave:Crohn's disease
Succinate
Dialister
Biomarker
Postoperative recurrence
Inflammatory bowel diseases
Succinic acid
Gut microbiota
Prevotella
Escherichia coli
Descripción
Sumario:Succinate, a metabolite produced by both the gut microbiota and the host, has emerged as a key player in chronic inflammation. In patients with Crohn's disease (CD), increased succinate in the intestinal lumen correlates with both dysbiosis and greater disease activity. To investigate circulating succinate as a biomarker of CD activity and its associations with gut microbiota, immune, and clinical features. This study with the prospective inclusion of patients with CD in remission, active CD, and non-inflammatory bowel disease controls matched by age, sex, and body mass index. Remission was defined as Harvey-Bradshaw index < 6, C-reactive protein < 0.4 mg/dL, fecal calprotectin < 250 μg/g, and endoscopic activity index Simple Endoscopic Score for CD < 6. Faecal microbiota profiling was performed using 16S rRNA gene sequencing, and demographic, clinical, and treatment variables were recorded along with blood samples (C-reactive protein and succinate) and stool samples. Results: Succinate levels were significantly elevated in active CD patients compared to inactive patients and non-inflammatory bowel disease controls. These increases were associated with higher Harvey-Bradshaw Index scores, increased expression of the succinate receptor 1 in immune cells, and enrichment of the succinate-producing genus Prevotella and the pro-inflammatory phylum Proteobacteria. Conversely, succinate levels negatively correlated with Odoribacter, a known succinate consumer. Interestingly, Dialister, a slow succinate consumer, was enriched in both active and inactive CD patients and was associated with impaired circulating succinate clearance and increased disease activity as well as postoperative recurrence in a validation cohort. Functional microbial analyses revealed upregulation of fumarate reductase and succinate transporters, alongside reduced NADH dehydrogenase expression, indicating disrupted succinate metabolism. Conclusion: These findings highlight succinate as a promising biomarker for CD activity and progression, suggesting that targeting succinate metabolism or key microbial taxa may offer novel therapeutic opportunities.