Clinical Risk Factors and Microbiological and Intestinal Characteristics of Carbapenemase-Producing Enterobacteriaceae Colonization and Subsequent Infection

ABSTRACT Gastrointestinal colonization with carbapenem-resistant Enterobacteriaceae (CRE) is always a prerequisite for the development of translocated infections. Here, we sought to screen for fecal carriage of CRE and identify the risk factors for CRE colonization as well as subsequent translocated...

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Main Authors: Wenli Yuan, Jiali Xu, Lin Guo, Yonghong Chen, Jinyi Gu, Huan Zhang, Chenghang Yang, Qiuping Yang, Shuwen Deng, Longlong Zhang, Qiongfang Deng, Zi Wang, Bin Ling, Deyao Deng
Format: Article
Language:English
Published: American Society for Microbiology 2022-12-01
Series:Microbiology Spectrum
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Online Access:https://journals.asm.org/doi/10.1128/spectrum.01906-21
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author Wenli Yuan
Jiali Xu
Lin Guo
Yonghong Chen
Jinyi Gu
Huan Zhang
Chenghang Yang
Qiuping Yang
Shuwen Deng
Longlong Zhang
Qiongfang Deng
Zi Wang
Bin Ling
Deyao Deng
author_facet Wenli Yuan
Jiali Xu
Lin Guo
Yonghong Chen
Jinyi Gu
Huan Zhang
Chenghang Yang
Qiuping Yang
Shuwen Deng
Longlong Zhang
Qiongfang Deng
Zi Wang
Bin Ling
Deyao Deng
author_sort Wenli Yuan
collection DOAJ
description ABSTRACT Gastrointestinal colonization with carbapenem-resistant Enterobacteriaceae (CRE) is always a prerequisite for the development of translocated infections. Here, we sought to screen for fecal carriage of CRE and identify the risk factors for CRE colonization as well as subsequent translocated pneumonia in critically ill patients admitted to the intensive care unit (ICU) of a university hospital in China. We further focused on the intestinal flora composition and fecal metabolic profiles in CRE rectal colonization and translocated infection patients. Animal models of gastrointestinal colonization with a carbapenemase-producing Klebsiella pneumoniae (carbapenem-resistant K. pneumoniae [CRKP]) clinical isolate expressing green fluorescent protein (GFP) were established, and systemic infection was subsequently traced using an in vivo imaging system (IVIS). The intestinal barrier, inflammatory factors, and infiltrating immune cells were further investigated. In this study, we screened 54 patients hospitalized in the ICU with CRE rectal colonization, and 50% of the colonized patients developed CRE-associated pneumonia, in line with the significantly high mortality rate. Upon multivariate analysis, risk factors associated with subsequent pneumonia caused by CRE in patients with fecal colonization included enteral feeding and carbapenem exposure. Furthermore, CRKP colonization and translocated infection influenced the diversity and community composition of the intestinal microbiome. Downregulated propionate and butyrate probably play important and multiangle roles in regulating immune cell infiltration, inflammatory factor expression, and mucus and intestinal epithelial barrier integrity. Although the risk factors and intestinal biomarkers for subsequent infections among CRE-colonized patients were explored, further work is needed to elucidate the complicated mechanisms. IMPORTANCE Carbapenem-resistant Enterobacteriaceae have emerged as a major threat to modern medicine, and the spread of carbapenem-resistant Enterobacteriaceae is a clinical and public health problem. Gastrointestinal colonization by potential pathogens is always a prerequisite for the development of translocated infections, and there is a growing need to assess clinical risk factors and microbiological and intestinal characteristics to prevent the development of clinical infection by carbapenem-resistant Enterobacteriaceae.
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spelling doaj.art-0e4d7537cd64457dad7b3adae2dc66202022-12-22T03:03:13ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-12-0110610.1128/spectrum.01906-21Clinical Risk Factors and Microbiological and Intestinal Characteristics of Carbapenemase-Producing Enterobacteriaceae Colonization and Subsequent InfectionWenli Yuan0Jiali Xu1Lin Guo2Yonghong Chen3Jinyi Gu4Huan Zhang5Chenghang Yang6Qiuping Yang7Shuwen Deng8Longlong Zhang9Qiongfang Deng10Zi Wang11Bin Ling12Deyao Deng13Department of Clinical Laboratory, The Affiliated Hospital of Yunnan University (The Second Hospital of Yunnan Province), Kunming, Yunnan Province, ChinaDepartment of Clinical Laboratory, The Affiliated Hospital of Yunnan University (The Second Hospital of Yunnan Province), Kunming, Yunnan Province, ChinaIntensive Care Union, The Affiliated Hospital of Yunnan University (The Second Hospital of Yunnan Province), Kunming, Yunnan Province, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources, Key Laboratory for Microbial Resources of the Ministry of Education, School of Life Sciences, Yunnan University, Kunming, Yunnan Province, ChinaDepartment of Clinical Laboratory, The Affiliated Hospital of Yunnan University (The Second Hospital of Yunnan Province), Kunming, Yunnan Province, ChinaDepartment of Clinical Laboratory, The Affiliated Hospital of Yunnan University (The Second Hospital of Yunnan Province), Kunming, Yunnan Province, ChinaIntensive Care Union, The Affiliated Hospital of Yunnan University (The Second Hospital of Yunnan Province), Kunming, Yunnan Province, ChinaDepartment of Clinical Laboratory, The Affiliated Hospital of Yunnan University (The Second Hospital of Yunnan Province), Kunming, Yunnan Province, ChinaDepartment of Clinical Laboratory, The Affiliated Hospital of Yunnan University (The Second Hospital of Yunnan Province), Kunming, Yunnan Province, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources, Key Laboratory for Microbial Resources of the Ministry of Education, School of Life Sciences, Yunnan University, Kunming, Yunnan Province, ChinaIntensive Care Union, The Affiliated Hospital of Yunnan University (The Second Hospital of Yunnan Province), Kunming, Yunnan Province, ChinaDepartment of Clinical Pharmacy, The Affiliated Hospital of Yunnan University (The Second Hospital of Yunnan Province), Kunming, Yunnan Province, ChinaIntensive Care Union, The Affiliated Hospital of Yunnan University (The Second Hospital of Yunnan Province), Kunming, Yunnan Province, ChinaDepartment of Clinical Laboratory, The Affiliated Hospital of Yunnan University (The Second Hospital of Yunnan Province), Kunming, Yunnan Province, ChinaABSTRACT Gastrointestinal colonization with carbapenem-resistant Enterobacteriaceae (CRE) is always a prerequisite for the development of translocated infections. Here, we sought to screen for fecal carriage of CRE and identify the risk factors for CRE colonization as well as subsequent translocated pneumonia in critically ill patients admitted to the intensive care unit (ICU) of a university hospital in China. We further focused on the intestinal flora composition and fecal metabolic profiles in CRE rectal colonization and translocated infection patients. Animal models of gastrointestinal colonization with a carbapenemase-producing Klebsiella pneumoniae (carbapenem-resistant K. pneumoniae [CRKP]) clinical isolate expressing green fluorescent protein (GFP) were established, and systemic infection was subsequently traced using an in vivo imaging system (IVIS). The intestinal barrier, inflammatory factors, and infiltrating immune cells were further investigated. In this study, we screened 54 patients hospitalized in the ICU with CRE rectal colonization, and 50% of the colonized patients developed CRE-associated pneumonia, in line with the significantly high mortality rate. Upon multivariate analysis, risk factors associated with subsequent pneumonia caused by CRE in patients with fecal colonization included enteral feeding and carbapenem exposure. Furthermore, CRKP colonization and translocated infection influenced the diversity and community composition of the intestinal microbiome. Downregulated propionate and butyrate probably play important and multiangle roles in regulating immune cell infiltration, inflammatory factor expression, and mucus and intestinal epithelial barrier integrity. Although the risk factors and intestinal biomarkers for subsequent infections among CRE-colonized patients were explored, further work is needed to elucidate the complicated mechanisms. IMPORTANCE Carbapenem-resistant Enterobacteriaceae have emerged as a major threat to modern medicine, and the spread of carbapenem-resistant Enterobacteriaceae is a clinical and public health problem. Gastrointestinal colonization by potential pathogens is always a prerequisite for the development of translocated infections, and there is a growing need to assess clinical risk factors and microbiological and intestinal characteristics to prevent the development of clinical infection by carbapenem-resistant Enterobacteriaceae.https://journals.asm.org/doi/10.1128/spectrum.01906-21carbapenem-resistant Enterobacteriaceaerectal colonizationrisk factorintestinal florametabolism
spellingShingle Wenli Yuan
Jiali Xu
Lin Guo
Yonghong Chen
Jinyi Gu
Huan Zhang
Chenghang Yang
Qiuping Yang
Shuwen Deng
Longlong Zhang
Qiongfang Deng
Zi Wang
Bin Ling
Deyao Deng
Clinical Risk Factors and Microbiological and Intestinal Characteristics of Carbapenemase-Producing Enterobacteriaceae Colonization and Subsequent Infection
Microbiology Spectrum
carbapenem-resistant Enterobacteriaceae
rectal colonization
risk factor
intestinal flora
metabolism
title Clinical Risk Factors and Microbiological and Intestinal Characteristics of Carbapenemase-Producing Enterobacteriaceae Colonization and Subsequent Infection
title_full Clinical Risk Factors and Microbiological and Intestinal Characteristics of Carbapenemase-Producing Enterobacteriaceae Colonization and Subsequent Infection
title_fullStr Clinical Risk Factors and Microbiological and Intestinal Characteristics of Carbapenemase-Producing Enterobacteriaceae Colonization and Subsequent Infection
title_full_unstemmed Clinical Risk Factors and Microbiological and Intestinal Characteristics of Carbapenemase-Producing Enterobacteriaceae Colonization and Subsequent Infection
title_short Clinical Risk Factors and Microbiological and Intestinal Characteristics of Carbapenemase-Producing Enterobacteriaceae Colonization and Subsequent Infection
title_sort clinical risk factors and microbiological and intestinal characteristics of carbapenemase producing enterobacteriaceae colonization and subsequent infection
topic carbapenem-resistant Enterobacteriaceae
rectal colonization
risk factor
intestinal flora
metabolism
url https://journals.asm.org/doi/10.1128/spectrum.01906-21
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