Intestinal colonization with ESBL-producing Klebsiella pneumoniae in healthy rural villager: A genomic surveillance study in China, 2015-2017

BackgroundThe worldwide emergence and diffusion of extended-spectrum β-lactamase-K. pneumoniae (ESBL-KP) is of particular concern. Although ESBL-KP can inhabit the human gut asymptomatically, colonization with ESBL-KP is associated with an increased risk of ESBL-KP infection and mortality. In this s...

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Main Authors: Shuang Wang, Hengjie Xie, Yuzhen Chen, Lu Liu, Ming Fang, Dapeng Sun, Liuchen Xu, Zhenqiang Bi, Gaoxiang Sun, Yan Li, Xiaolin Yu, Huaning Zhang, Zengqiang Kou, Beiwen Zheng
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-12-01
Series:Frontiers in Public Health
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpubh.2022.1017050/full
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author Shuang Wang
Hengjie Xie
Yuzhen Chen
Lu Liu
Ming Fang
Dapeng Sun
Liuchen Xu
Zhenqiang Bi
Gaoxiang Sun
Yan Li
Xiaolin Yu
Huaning Zhang
Zengqiang Kou
Beiwen Zheng
Beiwen Zheng
Beiwen Zheng
author_facet Shuang Wang
Hengjie Xie
Yuzhen Chen
Lu Liu
Ming Fang
Dapeng Sun
Liuchen Xu
Zhenqiang Bi
Gaoxiang Sun
Yan Li
Xiaolin Yu
Huaning Zhang
Zengqiang Kou
Beiwen Zheng
Beiwen Zheng
Beiwen Zheng
author_sort Shuang Wang
collection DOAJ
description BackgroundThe worldwide emergence and diffusion of extended-spectrum β-lactamase-K. pneumoniae (ESBL-KP) is of particular concern. Although ESBL-KP can inhabit the human gut asymptomatically, colonization with ESBL-KP is associated with an increased risk of ESBL-KP infection and mortality. In this study, we investigated the prevalence and characteristics of ESBL-KP in fecal samples from healthy persons in 12 villages in Shandong Province, China.MethodsScreening for ESBL-KP in fecal samples was performed by selective cultivation. The bacterial species were identified using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) and 16S rDNA sequence analysis. Minimum inhibitory concentrations (MICs) of 16 antibiotics were determined by the agar dilution method. Plasmid replicons, antimicrobial resistance genes and Sequence types (STs) of the isolates were determined by whole-genome sequencing (WGS). Genetic relatedness of ESBL-KP isolates was determined by the single nucleotide polymorphisms (SNP). The S1 nuclease-pulsed-field gel electrophoresis (S1-PFGE) was used to characterize the plasmids carried by ESBL-KP isolates. Conjugation assays was used to verify the transferability of blaCTX − M.ResultsESBL-KP prevalence rates increased from 12.0% in 2015 to 27.5% in 2017. The experimental results showed that 97% of isolates had multi-drug resistance. Multiple ESBL resistance genotypes were commonly detected in the isolates. STs among the ESBL-KP isolates were diverse. All 69 blaCTX−M−3-positive isolates were located on plasmids, and these genes could be transferred with plasmids between different strains. Phylogenetic analysis showed the possibility of transmission among some isolates.ConclusionThis study obtained the drug resistance patterns, the drug resistance phenotype and molecular characteristics of fecal-derived ESBL-KP in rural communities in Shandong Province, China. We report a rapid increase in occurrence of ESBL-KP among fecal samples collected from healthy rural residents of Shandong Province from 2015 to 2017. The carriage rate of multidrug-resistant bacteria in healthy residents is increasing. Thus, a need for further monitoring and possible interventions of ESBL-KP in this region is warranted.
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spelling doaj.art-d556b1b00172438bb722df318059d1022022-12-22T02:59:58ZengFrontiers Media S.A.Frontiers in Public Health2296-25652022-12-011010.3389/fpubh.2022.10170501017050Intestinal colonization with ESBL-producing Klebsiella pneumoniae in healthy rural villager: A genomic surveillance study in China, 2015-2017Shuang Wang0Hengjie Xie1Yuzhen Chen2Lu Liu3Ming Fang4Dapeng Sun5Liuchen Xu6Zhenqiang Bi7Gaoxiang Sun8Yan Li9Xiaolin Yu10Huaning Zhang11Zengqiang Kou12Beiwen Zheng13Beiwen Zheng14Beiwen Zheng15Infection Disease Control of Institute, Shandong Center for Disease Control and Prevention, Jinan, Shandong, ChinaDepartment of Supervise Sampling, Shandong Institute for Food and Drug Control, Jinan, Shandong, ChinaInfection Disease Control of Institute, Shandong Center for Disease Control and Prevention, Jinan, Shandong, ChinaInfection Disease Control of Institute, Shandong Center for Disease Control and Prevention, Jinan, Shandong, ChinaInfection Disease Control of Institute, Shandong Center for Disease Control and Prevention, Jinan, Shandong, ChinaInfection Disease Control of Institute, Shandong Center for Disease Control and Prevention, Jinan, Shandong, ChinaInfection Disease Control of Institute, Shandong Center for Disease Control and Prevention, Jinan, Shandong, ChinaInfection Disease Control of Institute, Shandong Center for Disease Control and Prevention, Jinan, Shandong, ChinaInfection Disease Control of Institute, Shandong Center for Disease Control and Prevention, Jinan, Shandong, ChinaInfection Disease Control of Institute, Shandong Center for Disease Control and Prevention, Jinan, Shandong, ChinaInfection Disease Control of Institute, Shandong Center for Disease Control and Prevention, Jinan, Shandong, ChinaInfection Disease Control of Institute, Shandong Center for Disease Control and Prevention, Jinan, Shandong, ChinaInfection Disease Control of Institute, Shandong Center for Disease Control and Prevention, Jinan, Shandong, ChinaState Key Laboratory for Diagnosis and Treatment of Infectious Disease, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou, Zhejiang, ChinaJinan Microecological Biomedicine Shandong Laboratory, Department of Structure and Morphology, Jinan, Shandong, ChinaResearch Units of Infectious Diseases and Microecology, Chinese Academy of Medical Sciences, Beijing, ChinaBackgroundThe worldwide emergence and diffusion of extended-spectrum β-lactamase-K. pneumoniae (ESBL-KP) is of particular concern. Although ESBL-KP can inhabit the human gut asymptomatically, colonization with ESBL-KP is associated with an increased risk of ESBL-KP infection and mortality. In this study, we investigated the prevalence and characteristics of ESBL-KP in fecal samples from healthy persons in 12 villages in Shandong Province, China.MethodsScreening for ESBL-KP in fecal samples was performed by selective cultivation. The bacterial species were identified using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) and 16S rDNA sequence analysis. Minimum inhibitory concentrations (MICs) of 16 antibiotics were determined by the agar dilution method. Plasmid replicons, antimicrobial resistance genes and Sequence types (STs) of the isolates were determined by whole-genome sequencing (WGS). Genetic relatedness of ESBL-KP isolates was determined by the single nucleotide polymorphisms (SNP). The S1 nuclease-pulsed-field gel electrophoresis (S1-PFGE) was used to characterize the plasmids carried by ESBL-KP isolates. Conjugation assays was used to verify the transferability of blaCTX − M.ResultsESBL-KP prevalence rates increased from 12.0% in 2015 to 27.5% in 2017. The experimental results showed that 97% of isolates had multi-drug resistance. Multiple ESBL resistance genotypes were commonly detected in the isolates. STs among the ESBL-KP isolates were diverse. All 69 blaCTX−M−3-positive isolates were located on plasmids, and these genes could be transferred with plasmids between different strains. Phylogenetic analysis showed the possibility of transmission among some isolates.ConclusionThis study obtained the drug resistance patterns, the drug resistance phenotype and molecular characteristics of fecal-derived ESBL-KP in rural communities in Shandong Province, China. We report a rapid increase in occurrence of ESBL-KP among fecal samples collected from healthy rural residents of Shandong Province from 2015 to 2017. The carriage rate of multidrug-resistant bacteria in healthy residents is increasing. Thus, a need for further monitoring and possible interventions of ESBL-KP in this region is warranted.https://www.frontiersin.org/articles/10.3389/fpubh.2022.1017050/fullintestinal colonizationST101CTX-M-3core-genome single nucleotide polymorphismsESBL-producing K. pneumoniae
spellingShingle Shuang Wang
Hengjie Xie
Yuzhen Chen
Lu Liu
Ming Fang
Dapeng Sun
Liuchen Xu
Zhenqiang Bi
Gaoxiang Sun
Yan Li
Xiaolin Yu
Huaning Zhang
Zengqiang Kou
Beiwen Zheng
Beiwen Zheng
Beiwen Zheng
Intestinal colonization with ESBL-producing Klebsiella pneumoniae in healthy rural villager: A genomic surveillance study in China, 2015-2017
Frontiers in Public Health
intestinal colonization
ST101
CTX-M-3
core-genome single nucleotide polymorphisms
ESBL-producing K. pneumoniae
title Intestinal colonization with ESBL-producing Klebsiella pneumoniae in healthy rural villager: A genomic surveillance study in China, 2015-2017
title_full Intestinal colonization with ESBL-producing Klebsiella pneumoniae in healthy rural villager: A genomic surveillance study in China, 2015-2017
title_fullStr Intestinal colonization with ESBL-producing Klebsiella pneumoniae in healthy rural villager: A genomic surveillance study in China, 2015-2017
title_full_unstemmed Intestinal colonization with ESBL-producing Klebsiella pneumoniae in healthy rural villager: A genomic surveillance study in China, 2015-2017
title_short Intestinal colonization with ESBL-producing Klebsiella pneumoniae in healthy rural villager: A genomic surveillance study in China, 2015-2017
title_sort intestinal colonization with esbl producing klebsiella pneumoniae in healthy rural villager a genomic surveillance study in china 2015 2017
topic intestinal colonization
ST101
CTX-M-3
core-genome single nucleotide polymorphisms
ESBL-producing K. pneumoniae
url https://www.frontiersin.org/articles/10.3389/fpubh.2022.1017050/full
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