Gut microbiota drives colon cancer risk associated with diet: a comparative analysis of meat-based and pesco-vegetarian diets - Alimentation, Microbiote, Pathologies Encéphaliques et Métaboliques
Journal Articles Microbiome Year : 2024

Gut microbiota drives colon cancer risk associated with diet: a comparative analysis of meat-based and pesco-vegetarian diets

Carlotta de Filippo
  • Function : Author
Sofia Chioccioli
  • Function : Author
Niccolò Meriggi
  • Function : Author
Antonio Dario Troise
  • Function : Author
Francesco Vitali
  • Function : Author
Mariela Mejia Monroy
  • Function : Author
Serdar Özsezen
  • Function : Author
Katia Tortora
  • Function : Author
Aurélie Balvay
  • Function : Author
Claire Maudet
  • Function : Author
Nathalie Naud
  • Function : Author
Edwin Fouché
  • Function : Author
Charline Buisson
  • Function : Author
Jacques Dupuy
  • Function : Author
Valérie Bézirard
  • Function : Author
Sylvie Chevolleau
  • Function : Author
Valérie Tondereau
  • Function : Author
Vassilia Theodorou
  • Function : Author
Claire Maslo
  • Function : Author
Perrine Aubry
  • Function : Author
Camille Etienne
  • Function : Author
Lisa Giovannelli
  • Function : Author
Vincenzo Longo
  • Function : Author
Andrea Scaloni
  • Function : Author
Duccio Cavalieri
  • Function : Author
Jildau Bouwman
  • Function : Author
Fabrice Pierre
  • Function : Author
Françoise Guéraud
  • Function : Author
Giovanna Caderni
  • Function : Author

Abstract

Background Colorectal cancer (CRC) risk is strongly affected by dietary habits with red and processed meat increasing risk, and foods rich in dietary fibres considered protective. Dietary habits also shape gut microbiota, but the role of the combination between diet, the gut microbiota, and the metabolite profile on CRC risk is still missing an unequivocal characterisation.

Methods

To investigate how gut microbiota affects diet-associated CRC risk, we fed Apc-mutated PIRC rats and azoxymethane (AOM)-induced rats the following diets: a high-risk red/processed meat-based diet (MBD), a normalised risk diet (MBD with α-tocopherol, MBDT), a low-risk pesco-vegetarian diet (PVD), and control diet. We then conducted faecal microbiota transplantation (FMT) from PIRC rats to germ-free rats treated with AOM and fed a standard diet for 3 months. We analysed multiple tumour markers and assessed the variations in the faecal microbiota using 16S rRNA gene sequencing together with targeted-and untargeted-metabolomics analyses.

Results

In both animal models, the PVD group exhibited significantly lower colon tumorigenesis than the MBD ones, consistent with various CRC biomarkers. Faecal microbiota and its metabolites also revealed significant dietdependent profiles. Intriguingly, when faeces from PIRC rats fed these diets were transplanted into germ-free rats, those transplanted with MBD faeces developed a higher number of preneoplastic lesions together with distinctive diet-related bacterial and metabolic profiles. PVD determines a selection of nine taxonomic markers mainly belonging to Lachnospiraceae and Prevotellaceae families exclusively associated with at least two different animal models, and within these, four taxonomic markers were shared across all the three animal models. An inverse correlation between nonconjugated bile acids and bacterial genera mainly belonging to the Lachnospiraceae and Prevotellaceae families (representative of the PVD group) was present, suggesting a potential mechanism of action for the protective effect of these genera against CRC.

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Dates and versions

hal-04717263 , version 1 (01-10-2024)

Identifiers

Cite

Carlotta de Filippo, Sofia Chioccioli, Niccolò Meriggi, Antonio Dario Troise, Francesco Vitali, et al.. Gut microbiota drives colon cancer risk associated with diet: a comparative analysis of meat-based and pesco-vegetarian diets. Microbiome, 2024, 12 (1), pp.180. ⟨10.1186/s40168-024-01900-2⟩. ⟨hal-04717263⟩
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