Surgical Treatment for Colorectal Cancer Partially Restores Gut Microbiome and Metabolome Traits
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 unders...
| Main Authors: | , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2022-04-01
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| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/msystems.00018-22 |
| _version_ | 1817991208520122368 |
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| author | 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 |
| author_facet | 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 |
| author_sort | Hirotsugu Shiroma |
| collection | DOAJ |
| description | 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 follow-up assessments. IMPORTANCE The gut microbiome and metabolites are associated with CRC progression and carcinogenesis. Postoperative CRC patients are reported to be at an increased CRC risk; however, how gut microbiome and metabolites are related to CRC risk in postoperative patients remains only partially understood. In this study, we investigated the influence of surgical CRC treatment on the gut microbiome and metabolites. We found that the CRC-associated species Fusobacterium nucleatum was decreased postsurgery, whereas carcinogenesis-associated DCA and its producing species and genes were increased postsurgery. We developed methods to estimate postoperative CRC risk based on the gut microbiome and metabolomic compositions. We applied methods to compare the estimated CRC risk between two groups according to the presence of large adenoma or tumors after 5 years postsurgery. To our knowledge, this study is the first report on differences between pre- and postsurgery using metagenomics and metabolomics data analysis. Our methods might be used for CRC risk assessment in postoperative patients. |
| first_indexed | 2024-04-14T01:10:13Z |
| format | Article |
| id | doaj.art-527d37b8bbb74bb59b0a5dc473fa1321 |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-04-14T01:10:13Z |
| publishDate | 2022-04-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-527d37b8bbb74bb59b0a5dc473fa13212022-12-22T02:21:07ZengAmerican Society for MicrobiologymSystems2379-50772022-04-017210.1128/msystems.00018-22Surgical Treatment for Colorectal Cancer Partially Restores Gut Microbiome and Metabolome TraitsHirotsugu Shiroma0Satoshi Shiba1Pande Putu Erawijantari2Hiroyuki Takamaru3Masayoshi Yamada4Taku Sakamoto5Yukihide Kanemitsu6Sayaka Mizutani7Tomoyoshi Soga8Yutaka Saito9Tatsuhiro Shibata10Shinji Fukuda11Shinichi Yachida12Takuji Yamada13School of Life Science and Technology, Tokyo Institute of Technology, Tokyo, JapanDivision of Cancer Genomics, National Cancer Center Research Institute, Tokyo, JapanSchool of Life Science and Technology, Tokyo Institute of Technology, Tokyo, JapanEndoscopy Division, National Cancer Center Hospital, Tokyo, JapanEndoscopy Division, National Cancer Center Hospital, Tokyo, JapanEndoscopy Division, National Cancer Center Hospital, Tokyo, JapanDepartment of Colorectal Surgery, National Cancer Center Hospital, Tokyo, JapanSchool of Life Science and Technology, Tokyo Institute of Technology, Tokyo, JapanInstitute for Advanced Biosciences, Keio University, Yamagata, JapanEndoscopy Division, National Cancer Center Hospital, Tokyo, JapanDivision of Cancer Genomics, National Cancer Center Research Institute, Tokyo, JapanInstitute for Advanced Biosciences, Keio University, Yamagata, JapanDivision of Cancer Genomics, National Cancer Center Research Institute, Tokyo, JapanSchool of Life Science and Technology, Tokyo Institute of Technology, Tokyo, JapanABSTRACT 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 follow-up assessments. IMPORTANCE The gut microbiome and metabolites are associated with CRC progression and carcinogenesis. Postoperative CRC patients are reported to be at an increased CRC risk; however, how gut microbiome and metabolites are related to CRC risk in postoperative patients remains only partially understood. In this study, we investigated the influence of surgical CRC treatment on the gut microbiome and metabolites. We found that the CRC-associated species Fusobacterium nucleatum was decreased postsurgery, whereas carcinogenesis-associated DCA and its producing species and genes were increased postsurgery. We developed methods to estimate postoperative CRC risk based on the gut microbiome and metabolomic compositions. We applied methods to compare the estimated CRC risk between two groups according to the presence of large adenoma or tumors after 5 years postsurgery. To our knowledge, this study is the first report on differences between pre- and postsurgery using metagenomics and metabolomics data analysis. Our methods might be used for CRC risk assessment in postoperative patients.https://journals.asm.org/doi/10.1128/msystems.00018-22colorectal cancersurgerymetagenomicshuman gut microbiomemetabolomics |
| spellingShingle | 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 Surgical Treatment for Colorectal Cancer Partially Restores Gut Microbiome and Metabolome Traits mSystems colorectal cancer surgery metagenomics human gut microbiome metabolomics |
| title | Surgical Treatment for Colorectal Cancer Partially Restores Gut Microbiome and Metabolome Traits |
| title_full | Surgical Treatment for Colorectal Cancer Partially Restores Gut Microbiome and Metabolome Traits |
| title_fullStr | Surgical Treatment for Colorectal Cancer Partially Restores Gut Microbiome and Metabolome Traits |
| title_full_unstemmed | Surgical Treatment for Colorectal Cancer Partially Restores Gut Microbiome and Metabolome Traits |
| title_short | Surgical Treatment for Colorectal Cancer Partially Restores Gut Microbiome and Metabolome Traits |
| title_sort | surgical treatment for colorectal cancer partially restores gut microbiome and metabolome traits |
| topic | colorectal cancer surgery metagenomics human gut microbiome metabolomics |
| url | https://journals.asm.org/doi/10.1128/msystems.00018-22 |
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