Basic Study
Copyright ©The Author(s) 2024. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Jul 21, 2024; 30(27): 3336-3355
Published online Jul 21, 2024. doi: 10.3748/wjg.v30.i27.3336
Distinct gut microbiomes in Thai patients with colorectal polyps
Thoranin Intarajak, Wandee Udomchaiprasertkul, Ahmad Nuruddin Khoiri, Sawannee Sutheeworapong, Kanthida Kusonmano, Weerayuth Kittichotirat, Chinae Thammarongtham, Supapon Cheevadhanarak
Thoranin Intarajak, Bioinformatics Unit, Chulabhorn Royal Academy, Lak Si 10210, Bangkok, Thailand
Thoranin Intarajak, Ahmad Nuruddin Khoiri, Kanthida Kusonmano, Weerayuth Kittichotirat, Bioinformatics and Systems Biology Program, School of Bioresources and Technology, and School of Information Technology, King Mongkut’s University of Technology Thonburi, Bang Khun Thian 10150, Bangkok, Thailand
Thoranin Intarajak, Sawannee Sutheeworapong, Kanthida Kusonmano, Weerayuth Kittichotirat, Supapon Cheevadhanarak, Systems Biology and Bioinformatics Unit, Pilot Plant Development and Training Institute, King Mongkut’s University of Technology Thonburi, Bang Khun Thian 10150, Bangkok, Thailand
Wandee Udomchaiprasertkul, Molecular Genomic Research Laboratory, Chulabhorn Royal Academy, Lak Si 10210, Bangkok, Thailand
Chinae Thammarongtham, National Center for Genetic Engineering and Biotechnology, King Mongkut's University of Technology Thonburi, Bang Khun Thian 10150, Bangkok, Thailand
Supapon Cheevadhanarak, School of Bioresources and Technology, King Mongkut’s University of Technology Thonburi, Bank Khun Thian 10150, Bangkok, Thailand
Supapon Cheevadhanarak, Fungal Biotechnology Unit, Pilot Plant Development and Training Institute, King Mongkut’s University of Technology Thonburi, Bang Khun Thian 10150, Bangkok, Thailand
Author contributions: Cheevadhanarak S, Sutheeworapong S, Thammarongtham C, Intarajak T and Udomchaiprasertkul W contributed to conceptualization; Cheevadhanarak S, Kusonmano K, Intarajak T and Udomchaiprasertkul W contributed to methodology; Sutheeworapong S, Intarajak T and Khoiri AN contributed to software; Intarajak T, Kittichotirat W and Khoiri AN contributed to validation; Intarajak T and Khoiri AN contributed to formal analysis; Cheevadhanarak S, Intarajak T and Udomchaiprasertkul W contributed to investigation, resources, data curation and writing — original draft preparation; Cheevadhanarak S, Thammarongtham C, Kusonmano K, Khoiri AN, Intarajak T and Udomchaiprasertkul W contributed to writing — review and editing; Intarajak T, contributed to visualization; Cheevadhanarak S, Thammarongtham C, Sutheeworapong S, Kusonmano K and Kittichotirat W contributed to supervision; Intarajak T and Kittichotirat W contributed to project administration and funding acquisition; All authors gave final approval of the version of the article to be published.
Supported by Chulabhorn Royal Academy (Fundamental Fund: Fiscal year 2022 by National Science Research and Innovation Fund), No. FRB650039/0240 Project Code 165422.
Institutional review board statement: The study protocol was reviewed and approved by the Ethical Committee of Chulabhorn Research Institute and the Institutional Review Boards of Chulabhorn Royal Academy (Project Code 045/2563).
Informed consent statement: Informed consent was obtained from all participants involved in the study.
Conflict-of-interest statement: All the authors report no relevant conflicts of interest for this article.
Data sharing statement: Raw sequence data have been deposited in the SRA database under accession number PRJNA940282.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Supapon Cheevadhanarak, PhD, Associate Professor, School of Bioresources and Technology, King Mongkut’s University of Technology Thonburi, 49 Soi Thian Thale 25, Bang Khun Thian Chai Thale Road, Bank Khun Thian 10150, Bangkok, Thailand. supapon.che@mail.kmutt.ac.th
Received: February 21, 2024
Revised: April 30, 2024
Accepted: May 31, 2024
Published online: July 21, 2024
Processing time: 140 Days and 23.4 Hours
Abstract
BACKGROUND

Colorectal polyps that develop via the conventional adenoma-carcinoma sequence [e.g., tubular adenoma (TA)] often progress to malignancy and are closely associated with changes in the composition of the gut microbiome. There is limited research concerning the microbial functions and gut microbiomes associated with colorectal polyps that arise through the serrated polyp pathway, such as hyperplastic polyps (HP). Exploration of microbiome alterations associated with HP and TA would improve the understanding of mechanisms by which specific microbes and their metabolic pathways contribute to colorectal carcinogenesis.

AIM

To investigate gut microbiome signatures, microbial associations, and microbial functions in HP and TA patients.

METHODS

Full-length 16S rRNA sequencing was used to characterize the gut microbiome in stool samples from control participants without polyps [control group (CT), n = 40], patients with HP (n = 52), and patients with TA (n = 60). Significant differences in gut microbiome composition and functional mechanisms were identified between the CT group and patients with HP or TA. Analytical techniques in this study included differential abundance analysis, co-occurrence network analysis, and differential pathway analysis.

RESULTS

Colorectal cancer (CRC)-associated bacteria, including Streptococcus gallolyticus (S. gallolyticus), Bacteroides fragilis, and Clostridium symbiosum, were identified as characteristic microbial species in TA patients. Mediterraneibacter gnavus, associated with dysbiosis and gastrointestinal diseases, was significantly differentially abundant in the HP and TA groups. Functional pathway analysis revealed that HP patients exhibited enrichment in the sulfur oxidation pathway exclusively, whereas TA patients showed dominance in pathways related to secondary metabolite biosynthesis (e.g., mevalonate); S. gallolyticus was a major contributor. Co-occurrence network and dynamic network analyses revealed co-occurrence of dysbiosis-associated bacteria in HP patients, whereas TA patients exhibited co-occurrence of CRC-associated bacteria. Furthermore, the co-occurrence of SCFA-producing bacteria was lower in TA patients than HP patients.

CONCLUSION

This study revealed distinct gut microbiome signatures associated with pathways of colorectal polyp development, providing insights concerning the roles of microbial species, functional pathways, and microbial interactions in colorectal carcinogenesis.

Keywords: Gut microbiome; Colorectal adenoma; Hyperplastic polyp; Full-length 16s rRNA; Microbial correlation networks; Predicted functional mechanisms

Core Tip: This study identified gut microbiome signatures and metabolic pathways associated with two types of colorectal polyps. It is the first report of enrichment in the sulfur oxidation pathway among patients with hyperplastic polyps (HP) and the involvement of Streptococcus gallolyticus in the secondary metabolite biosynthesis pathway among patients with tubular adenoma (TA). Additionally, analysis of microbial associations in the gut microbiomes of HP and TA patients revealed a decrease in the co-occurrence of short chain fatty acid-producing bacteria. Conversely, there was an increase in the co-occurrence of dysbiosis and colorectal cancer-associated bacteria.