Clostridium butyricum potentially improves inflammation and immunity through alteration of the microbiota and metabolism of gastric cancer patients after gastrectomy

BackgroundGastrectomy is the most effective treatment to improve the clinical survival rate of patients with gastric cancer. However, the pathophysiological changes caused by gastrectomy have seriously affected the postoperative recovery.MethodsIn the present trial, Ataining (containing C. butyricum...

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Main Authors: Wenjie Cao, Cihua Zheng, Xuan Xu, Rui Jin, Feng Huang, Meng Shi, Zhipeng He, Yufeng Luo, Lulin Liu, Zhaoxia Liu, Jing Wei, Xiaorong Deng, Tingtao Chen
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-11-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2022.1076245/full
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author Wenjie Cao
Cihua Zheng
Xuan Xu
Rui Jin
Feng Huang
Meng Shi
Zhipeng He
Yufeng Luo
Lulin Liu
Zhaoxia Liu
Jing Wei
Xiaorong Deng
Tingtao Chen
Tingtao Chen
author_facet Wenjie Cao
Cihua Zheng
Xuan Xu
Rui Jin
Feng Huang
Meng Shi
Zhipeng He
Yufeng Luo
Lulin Liu
Zhaoxia Liu
Jing Wei
Xiaorong Deng
Tingtao Chen
Tingtao Chen
author_sort Wenjie Cao
collection DOAJ
description BackgroundGastrectomy is the most effective treatment to improve the clinical survival rate of patients with gastric cancer. However, the pathophysiological changes caused by gastrectomy have seriously affected the postoperative recovery.MethodsIn the present trial, Ataining (containing C. butyricum, CGMCC0313.1) was applied in patients after gastrectomy to investigate the effect of C. butyricum on the early postoperative recovery by monitoring the inflammatory immune response with blood indicators, detecting the gut microbiota with high-throughput sequencing, and analyzing the short-chain fatty acids (SCFAs) with targeted metabolomics. This study is registered with the number ChiCTR2000040915.ResultsOur outcomes revealed that C. butyricum had significantly reduced the number of Leucocyte (P < 0.001), the percentage of Neutrophil (P < 0.001), the expression of IL-1β (P < 0.01), IL-6 (P < 0.05), and TNF-α (P < 0.01), while markedly enhanced the immunity indexes (immunoglobulin and lymphocyte) (P < 0.05) and nutrition indexes (albumin and total protein) (P < 0.05). In addition, the use of the C. butyricum greatly enriched the relative abundance of beneficial bacteria Bacteroides, Faecalibacterium and Gemmiger, while the abundance of pathogenic Streptococcus, Desulfovibrio and Actinomyces were markedly decreased at genus level. We also observed significant up-regulation of SCFAs, including acetic acid, propionic acid, butyric acid and isobutyric acid, after C. butyricum administration in patients receiving gastrectomy.ConclusionTherefore, evidence supported that oral administration of C. butyricum after gastrectomy can reduce early postoperative inflammation, enhance immune ability, restore intestinal microbiota eubiosis, increase intestinal SCFAs, reduce the occurrence of postoperative complications, and ultimately promote the early recovery of the patient.Clinical trial registrationhttp://www.chictr.org.cn/, identifier (ChiCTR2000040915).
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spelling doaj.art-1c2b7d5b891a468a9e9d002bde7bdb8b2022-12-22T04:39:11ZengFrontiers Media S.A.Frontiers in Immunology1664-32242022-11-011310.3389/fimmu.2022.10762451076245Clostridium butyricum potentially improves inflammation and immunity through alteration of the microbiota and metabolism of gastric cancer patients after gastrectomyWenjie Cao0Cihua Zheng1Xuan Xu2Rui Jin3Feng Huang4Meng Shi5Zhipeng He6Yufeng Luo7Lulin Liu8Zhaoxia Liu9Jing Wei10Xiaorong Deng11Tingtao Chen12Tingtao Chen13Department of Gastrointestinal Surgery, The Second Affiliated Hospital of Nanchang University, Nanchang, ChinaDepartment of Gastrointestinal Surgery, The Second Affiliated Hospital of Nanchang University, Nanchang, ChinaHuanKui Academy, Nanchang University, Nanchang, ChinaQueen Mary College, Nanchang University, Nanchang, ChinaDepartment of Gastrointestinal Surgery, The Second Affiliated Hospital of Nanchang University, Nanchang, ChinaDepartment of Gastrointestinal Surgery, The Second Affiliated Hospital of Nanchang University, Nanchang, ChinaDepartment of Gastrointestinal Surgery, The Second Affiliated Hospital of Nanchang University, Nanchang, ChinaDepartment of Gastrointestinal Surgery, The Second Affiliated Hospital of Nanchang University, Nanchang, ChinaDepartment of Gastrointestinal Surgery, The Second Affiliated Hospital of Nanchang University, Nanchang, ChinaDepartment of Obstetrics and Gynecology, The Second Affiliated Hospital of Nanchang University, Nanchang, ChinaNational Engineering Research Center for Bioengineering Drugs and the Technologies, Institute of Translational Medicine, Nanchang University, Nanchang, ChinaDepartment of Gastrointestinal Surgery, The Second Affiliated Hospital of Nanchang University, Nanchang, ChinaDepartment of Gastrointestinal Surgery, The Second Affiliated Hospital of Nanchang University, Nanchang, ChinaNational Engineering Research Center for Bioengineering Drugs and the Technologies, Institute of Translational Medicine, Nanchang University, Nanchang, ChinaBackgroundGastrectomy is the most effective treatment to improve the clinical survival rate of patients with gastric cancer. However, the pathophysiological changes caused by gastrectomy have seriously affected the postoperative recovery.MethodsIn the present trial, Ataining (containing C. butyricum, CGMCC0313.1) was applied in patients after gastrectomy to investigate the effect of C. butyricum on the early postoperative recovery by monitoring the inflammatory immune response with blood indicators, detecting the gut microbiota with high-throughput sequencing, and analyzing the short-chain fatty acids (SCFAs) with targeted metabolomics. This study is registered with the number ChiCTR2000040915.ResultsOur outcomes revealed that C. butyricum had significantly reduced the number of Leucocyte (P < 0.001), the percentage of Neutrophil (P < 0.001), the expression of IL-1β (P < 0.01), IL-6 (P < 0.05), and TNF-α (P < 0.01), while markedly enhanced the immunity indexes (immunoglobulin and lymphocyte) (P < 0.05) and nutrition indexes (albumin and total protein) (P < 0.05). In addition, the use of the C. butyricum greatly enriched the relative abundance of beneficial bacteria Bacteroides, Faecalibacterium and Gemmiger, while the abundance of pathogenic Streptococcus, Desulfovibrio and Actinomyces were markedly decreased at genus level. We also observed significant up-regulation of SCFAs, including acetic acid, propionic acid, butyric acid and isobutyric acid, after C. butyricum administration in patients receiving gastrectomy.ConclusionTherefore, evidence supported that oral administration of C. butyricum after gastrectomy can reduce early postoperative inflammation, enhance immune ability, restore intestinal microbiota eubiosis, increase intestinal SCFAs, reduce the occurrence of postoperative complications, and ultimately promote the early recovery of the patient.Clinical trial registrationhttp://www.chictr.org.cn/, identifier (ChiCTR2000040915).https://www.frontiersin.org/articles/10.3389/fimmu.2022.1076245/fullGastric cancerClostridium butyricumSCFAsgut microbiotagastrectomy
spellingShingle Wenjie Cao
Cihua Zheng
Xuan Xu
Rui Jin
Feng Huang
Meng Shi
Zhipeng He
Yufeng Luo
Lulin Liu
Zhaoxia Liu
Jing Wei
Xiaorong Deng
Tingtao Chen
Tingtao Chen
Clostridium butyricum potentially improves inflammation and immunity through alteration of the microbiota and metabolism of gastric cancer patients after gastrectomy
Frontiers in Immunology
Gastric cancer
Clostridium butyricum
SCFAs
gut microbiota
gastrectomy
title Clostridium butyricum potentially improves inflammation and immunity through alteration of the microbiota and metabolism of gastric cancer patients after gastrectomy
title_full Clostridium butyricum potentially improves inflammation and immunity through alteration of the microbiota and metabolism of gastric cancer patients after gastrectomy
title_fullStr Clostridium butyricum potentially improves inflammation and immunity through alteration of the microbiota and metabolism of gastric cancer patients after gastrectomy
title_full_unstemmed Clostridium butyricum potentially improves inflammation and immunity through alteration of the microbiota and metabolism of gastric cancer patients after gastrectomy
title_short Clostridium butyricum potentially improves inflammation and immunity through alteration of the microbiota and metabolism of gastric cancer patients after gastrectomy
title_sort clostridium butyricum potentially improves inflammation and immunity through alteration of the microbiota and metabolism of gastric cancer patients after gastrectomy
topic Gastric cancer
Clostridium butyricum
SCFAs
gut microbiota
gastrectomy
url https://www.frontiersin.org/articles/10.3389/fimmu.2022.1076245/full
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