Surgical Treatment for Colorectal Cancer Partially Restores Gut Microbiome and Metabolome Traits

Hirotsugu Shiroma, Satoshi Shiba, Pande Putu Erawijantari, Hiroyuki Takamaru, Masayoshi Yamada, Taku Sakamoto, Yukihide Kanemitsu, Sayaka Mizutani, Tomoyoshi Soga, Yutaka Saito, Tatsuhiro Shibata, Shinji Fukuda, Shinichi Yachida, Takuji Yamada

Research output: Contribution to journalArticlepeer-review

Abstract

Accumulating evidence indicates that the gut microbiome and metabolites are associated with colorectal cancer (CRC). However, the influence of surgery for CRC treatment on the gut microbiome and metabolites and how it relates to CRC risk in postoperative CRC patients remain partially understood. Here, we collected 170 fecal samples from 85 CRC patients pre- and approximately 1 year postsurgery and performed shotgun metagenomic sequencing and capillary electrophoresis- time of flight mass spectrometry-based metabolomics analyses to characterize alterations between pre- and postsurgery. We determined that the relative abundance of 114 species was altered postsurgery (P<0.005). CRC-associated species, such as Fusobacterium nucleatum, were decreased postsurgery. On the other hand, Clostridium scindens, carcinogenesis-associated deoxycholate (DCA)-producing species, and its biotransformed genes (bai operon) were increased postsurgery. The concentration of 60 fecal metabolites was also altered postsurgery (P<0.005). Two bile acids, cholate and DCA, were increased postsurgery. We developed methods to estimate postoperative CRC risk based on the gut microbiome and metabolomic compositions using a random forest machine-learning algorithm that classifies large adenoma or early-stage CRC and healthy controls from publicly available data sets. We applied methods to preoperative samples and then compared the estimated CRC risk between the two groups according to the presence of large adenoma or tumors 5 years postsurgery (P<0.05). Overall, our results show that the gut microbiome and metabolites dynamically change from pre- to postsurgery. In postoperative CRC patients, potential CRC risk derived from gut microbiome and metabolites still remains, which indicates the importance of followup assessments.

Original languageEnglish
Article numbere00018-22
JournalmSystems
Volume7
Issue number2
DOIs
Publication statusPublished - 2022 Apr

Keywords

  • colorectal cancer
  • human gut microbiome
  • metabolomics
  • metagenomics
  • surgery

ASJC Scopus subject areas

  • Microbiology
  • Ecology, Evolution, Behavior and Systematics
  • Biochemistry
  • Physiology
  • Modelling and Simulation
  • Molecular Biology
  • Genetics
  • Computer Science Applications

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