Exclusive enteral nutrition initiates individual protective microbiome changes to induce remission in pediatric Crohn's disease

Cell Host Microbe. 2024 Nov 13;32(11):2019-2034.e8. doi: 10.1016/j.chom.2024.10.001. Epub 2024 Oct 25.

Abstract

Exclusive enteral nutrition (EEN) is a first-line therapy for pediatric Crohn's disease (CD), but protective mechanisms remain unknown. We established a prospective pediatric cohort to characterize the function of fecal microbiota and metabolite changes of treatment-naive CD patients in response to EEN (German Clinical Trials DRKS00013306). Integrated multi-omics analysis identified network clusters from individually variable microbiome profiles, with Lachnospiraceae and medium-chain fatty acids as protective features. Bioorthogonal non-canonical amino acid tagging selectively identified bacterial species in response to medium-chain fatty acids. Metagenomic analysis identified high strain-level dynamics in response to EEN. Functional changes in diet-exposed fecal microbiota were further validated using gut chemostat cultures and microbiota transfer into germ-free Il10-deficient mice. Dietary model conditions induced individual patient-specific strain signatures to prevent or cause inflammatory bowel disease (IBD)-like inflammation in gnotobiotic mice. Hence, we provide evidence that EEN therapy operates through explicit functional changes of temporally and individually variable microbiome profiles.

Keywords: EEN; FMT; bacterial strain dynamics; exclusive enteral nutrition; ex vivo gut chemostat model; fiber; medium-chain fatty acids; metagenomics; microbiome; multi-omics data integration; pediatric Crohn’s disease.

MeSH terms

  • Adolescent
  • Animals
  • Bacteria / classification
  • Bacteria / genetics
  • Child
  • Clostridiales
  • Crohn Disease* / microbiology
  • Crohn Disease* / therapy
  • Disease Models, Animal
  • Enteral Nutrition*
  • Fatty Acids / metabolism
  • Feces* / microbiology
  • Female
  • Gastrointestinal Microbiome*
  • Germ-Free Life
  • Humans
  • Interleukin-10 / genetics
  • Interleukin-10 / metabolism
  • Male
  • Metagenomics
  • Mice
  • Mice, Inbred C57BL
  • Prospective Studies
  • Remission Induction

Substances

  • Interleukin-10
  • Fatty Acids

Supplementary concepts

  • Pediatric Crohn's disease