Association of gut microbiome with immune microenvironment in surgically treated colorectal cancer patients

Pathology. 2024 Jun;56(4):528-539. doi: 10.1016/j.pathol.2024.01.010. Epub 2024 Mar 26.

Abstract

This study explored the relationship between faecal microbiota distribution and local or systemic immune response in patients with colorectal cancer (CRC). The study population included 114 surgically treated CRC patients. Faeces were analysed using 16S rRNA gene sequencing. The immune score in tumour microenvironment was evaluated using CD3 and CD8 immunohistochemistry. Genetic alterations, microsatellite instability status and five systemic inflammatory markers were also analysed. Thirty of 114 (26.3%) CRC patients were categorised as the 'immune type' with a high density of T-cells. The immune type CRC cases showed lower angiolymphatic invasion and longer overall survival. Of the 123 selected bacterial species, Bacteroides fragilis and Collinsella aerofaciens were prevalent in immune CRC cases, whereas Odoribacter splanchnicus and Phascolarctobacterium succinatutens were prevalent in non-immune CRC patients. Bacteroides fragilis was associated with shorter disease free survival in univariable and multivariable survival analyses. Regarding systemic immunity, a high prevalence of C. aerofaciens was associated with a high modified Glasgow prognostic score. This study revealed a potential relationship among the gut microbiome, immune microenvironment, and disease progression in patients with CRC. Our findings suggest that abundant B. fragilis in patients with CRC is associated with a 'cold immune' tumour microenvironment.

Keywords: Colorectal cancer; microbiota; systemic inflammatory markers; tumour microenvironment; tumour-infiltrating lymphocytes.

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Bacteroides fragilis / immunology
  • Colorectal Neoplasms* / immunology
  • Colorectal Neoplasms* / microbiology
  • Colorectal Neoplasms* / pathology
  • Colorectal Neoplasms* / surgery
  • Feces / microbiology
  • Female
  • Gastrointestinal Microbiome*
  • Humans
  • Male
  • Middle Aged
  • Prognosis
  • RNA, Ribosomal, 16S / genetics
  • Tumor Microenvironment* / immunology

Substances

  • RNA, Ribosomal, 16S