Characterization of the blood and neutrophil‐specific microbiomes and exploration of potential bacterial biomarkers for sepsis in surgical patients

Abstract Introduction Recent studies have demonstrated the presence of a circulating microbiome in the blood of healthy subjects and chronic inflammatory patients. However, our knowledge regarding the blood microbiome and its potential roles in surgical patients remains very limited. The objective o...

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Main Authors: Chenyang Wang, Qiurong Li, Chun Tang, Xiaofan Zhao, Qin He, Xingming Tang, Jianan Ren
Format: Article
Language:English
Published: Wiley 2021-12-01
Series:Immunity, Inflammation and Disease
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Online Access:https://doi.org/10.1002/iid3.483
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author Chenyang Wang
Qiurong Li
Chun Tang
Xiaofan Zhao
Qin He
Xingming Tang
Jianan Ren
author_facet Chenyang Wang
Qiurong Li
Chun Tang
Xiaofan Zhao
Qin He
Xingming Tang
Jianan Ren
author_sort Chenyang Wang
collection DOAJ
description Abstract Introduction Recent studies have demonstrated the presence of a circulating microbiome in the blood of healthy subjects and chronic inflammatory patients. However, our knowledge regarding the blood microbiome and its potential roles in surgical patients remains very limited. The objective of this study was to determine the blood microbial landscape in surgical patients and to explore its potential associations with postoperative sepsis. Materials and Methods 2825 patients who underwent surgical treatments were screened for enrollment and 204 cases were recruited in this study. The patients were sub‐grouped into noninfected, infected, sepsis, and septic shock according to postoperative clinical manifestations. A total of 222 blood samples were obtained for neutrophil isolation, DNA extraction and high‐throughput sequencing, quantitative proteomics analysis, and flow cytometric analyses. Results Blood and neutrophils in surgical patients and healthy controls contained highly diverse microbiomes, mainly comprising Proteobacteria, Actinobacteria, Firmicutes and Bacteroidetes. The majority (80.7%–91.5%) of the microbiomes were composed of gut‐associated bacteria. The microbiomes in septic patients were significantly distinct from those of healthy controls, and marked differences in microbiome composition were observed between sepsis and septic shock groups. Several specific bacterial genera, including Flavobacterium, Agrococcus, Polynucleobacter, and Acidovorax, could distinguish patients with septic shock from those with sepsis, with higher area under curve values. Moreover, Agrococcus, Polynucleobacter, and Acidovorax were positively associated with the sequential (sepsis‐related) organ failure assessment scores and/or acute physiology and chronic health examination scores in septic shock patients. The proteins involved in bactericidal activities of neutrophils were downregulated in septic patients. Conclusions We present evidence identifying significant changes of blood and neutrophil‐specific microbiomes across various stages of sepsis, which might be associated with the progression of sepsis after surgical treatments. Several certain bacterial genera in blood microbiome could have potential as microbial markers for early detection of sepsis.
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spelling doaj-art-fe4d4f827f864d5ba0adca3ac9c32b632025-08-20T02:46:35ZengWileyImmunity, Inflammation and Disease2050-45272021-12-01941343135710.1002/iid3.483Characterization of the blood and neutrophil‐specific microbiomes and exploration of potential bacterial biomarkers for sepsis in surgical patientsChenyang Wang0Qiurong Li1Chun Tang2Xiaofan Zhao3Qin He4Xingming Tang5Jianan Ren6Research Institute of General Surgery, Jinling Hospital Medical School of Nanjing University Nanjing ChinaResearch Institute of General Surgery, Jinling Hospital Medical School of Nanjing University Nanjing ChinaResearch Institute of General Surgery, Jinling Hospital Medical School of Nanjing University Nanjing ChinaResearch Institute of General Surgery, Jinling Hospital Medical School of Nanjing University Nanjing ChinaResearch Institute of General Surgery, Jinling Hospital Medical School of Nanjing University Nanjing ChinaResearch Institute of General Surgery, Jinling Hospital Medical School of Nanjing University Nanjing ChinaResearch Institute of General Surgery, Jinling Hospital Medical School of Nanjing University Nanjing ChinaAbstract Introduction Recent studies have demonstrated the presence of a circulating microbiome in the blood of healthy subjects and chronic inflammatory patients. However, our knowledge regarding the blood microbiome and its potential roles in surgical patients remains very limited. The objective of this study was to determine the blood microbial landscape in surgical patients and to explore its potential associations with postoperative sepsis. Materials and Methods 2825 patients who underwent surgical treatments were screened for enrollment and 204 cases were recruited in this study. The patients were sub‐grouped into noninfected, infected, sepsis, and septic shock according to postoperative clinical manifestations. A total of 222 blood samples were obtained for neutrophil isolation, DNA extraction and high‐throughput sequencing, quantitative proteomics analysis, and flow cytometric analyses. Results Blood and neutrophils in surgical patients and healthy controls contained highly diverse microbiomes, mainly comprising Proteobacteria, Actinobacteria, Firmicutes and Bacteroidetes. The majority (80.7%–91.5%) of the microbiomes were composed of gut‐associated bacteria. The microbiomes in septic patients were significantly distinct from those of healthy controls, and marked differences in microbiome composition were observed between sepsis and septic shock groups. Several specific bacterial genera, including Flavobacterium, Agrococcus, Polynucleobacter, and Acidovorax, could distinguish patients with septic shock from those with sepsis, with higher area under curve values. Moreover, Agrococcus, Polynucleobacter, and Acidovorax were positively associated with the sequential (sepsis‐related) organ failure assessment scores and/or acute physiology and chronic health examination scores in septic shock patients. The proteins involved in bactericidal activities of neutrophils were downregulated in septic patients. Conclusions We present evidence identifying significant changes of blood and neutrophil‐specific microbiomes across various stages of sepsis, which might be associated with the progression of sepsis after surgical treatments. Several certain bacterial genera in blood microbiome could have potential as microbial markers for early detection of sepsis.https://doi.org/10.1002/iid3.483blood microbiomehigh‐throughput sequencingneutrophil‐specific microbiomesepsisseptic shock
spellingShingle Chenyang Wang
Qiurong Li
Chun Tang
Xiaofan Zhao
Qin He
Xingming Tang
Jianan Ren
Characterization of the blood and neutrophil‐specific microbiomes and exploration of potential bacterial biomarkers for sepsis in surgical patients
Immunity, Inflammation and Disease
blood microbiome
high‐throughput sequencing
neutrophil‐specific microbiome
sepsis
septic shock
title Characterization of the blood and neutrophil‐specific microbiomes and exploration of potential bacterial biomarkers for sepsis in surgical patients
title_full Characterization of the blood and neutrophil‐specific microbiomes and exploration of potential bacterial biomarkers for sepsis in surgical patients
title_fullStr Characterization of the blood and neutrophil‐specific microbiomes and exploration of potential bacterial biomarkers for sepsis in surgical patients
title_full_unstemmed Characterization of the blood and neutrophil‐specific microbiomes and exploration of potential bacterial biomarkers for sepsis in surgical patients
title_short Characterization of the blood and neutrophil‐specific microbiomes and exploration of potential bacterial biomarkers for sepsis in surgical patients
title_sort characterization of the blood and neutrophil specific microbiomes and exploration of potential bacterial biomarkers for sepsis in surgical patients
topic blood microbiome
high‐throughput sequencing
neutrophil‐specific microbiome
sepsis
septic shock
url https://doi.org/10.1002/iid3.483
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