Genetic relatedness of multidrug resistant  Escherichia coli  isolated from humans, chickens and poultry environments

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Abstract

Background

Inappropriate use of antimicrobial agents in animal production has led to the development of antimicrobial resistance (AMR) in foodborne pathogens. Transmission of AMR foodborne pathogens from reservoirs, particularly chickens to the human population does occur. Recently, we reported that occupational exposure was a risk factor for multidrug-resistant (MDR) Escherichia coli (E. coli) among poultry-workers. Here we determined the prevalence and genetic relatedness among MDR E. coli isolated from poultry-workers, chickens, and poultry environments in Abuja, Nigeria. This study was conducted to address the gaps identified by the Nigerian AMR situation analysis.

Methods

We conducted a cross-sectional study among poultry-workers, chickens, and poultry farm/live bird market (LBM) environments. The isolates were tested phenotypically for their antimicrobial susceptibility profiles, genotypically characterized using whole-genome sequencing (WGS) and in silico multilocus sequence types (MLST). We conducted a phylogenetic single nucleotide polymorphism (SNPs) analysis to determine relatedness and clonality among the isolates.

Results

A total of 115 (26.8%) out of 429 samples were positive for E. coli. Of these, 110 isolates were viable for phenotypic and genotypic characterization. The selection comprised 47 (42.7%) isolates from poultry-workers, 36 (32.7%) from chickens, and 27 (24.5%) from poultry-farm or LBM environments. Overall, 101 (91.8%) of the isolates were MDR conferring resistance to at least three drug classes . High frequency of resistance was observed for tetracycline (n = 102; 92.7%), trimethoprim/sulfamethoxazole (n = 93; 84.5%), streptomycin (n = 87; 79.1%) and ampicillin (n = 88; 80%). Two plasmid-mediated colistin genes— mcr-1.1 harboured on IncX4 plasmids were detected in environmental isolates. The most prevalent sequence types (ST) were ST-155 (n = 8), ST-48 (n = 8) and ST-10 (n = 6). Two isolates of human and environmental sources with a SNPs difference of 6161 originating from the same farm shared a novel ST. The isolates had similar AMR genes and plasmid replicons.

Conclusion

MDR E.coli isolates were prevalent amongst poultry-workers, poultry, and the poultry farm/LBM environment. The emergence of MDR E. coli with novel ST in two isolates may be plasmid-mediated. Competent authorities should enforce AMR regulations to ensure prudent use of antimicrobials to limit the risk of transmission along the food chain.

Supplementary Information

The online version contains supplementary material available at 10.1186/s13756-021-00930-x.

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Most cited references 52

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SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing.

Anton Bankevich, Sergey Nurk, Dmitry Antipov … (2012)

The lion's share of bacteria in various environments cannot be cloned in the laboratory and thus cannot be sequenced using existing technologies. A major goal of single-cell genomics is to complement gene-centric metagenomic data with whole-genome assemblies of uncultivated organisms. Assembly of single-cell data is challenging because of highly non-uniform read coverage as well as elevated levels of sequencing errors and chimeric reads. We describe SPAdes, a new assembler for both single-cell and standard (multicell) assembly, and demonstrate that it improves on the recently released E+V-SC assembler (specialized for single-cell data) and on popular assemblers Velvet and SoapDeNovo (for multicell data). SPAdes generates single-cell assemblies, providing information about genomes of uncultivatable bacteria that vastly exceeds what may be obtained via traditional metagenomics studies. SPAdes is available online ( http://bioinf.spbau.ru/spades ). It is distributed as open source software.

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In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing.

Alessandra Carattoli, Ea Zankari, Aurora García-Fernández … (2014)

In the work presented here, we designed and developed two easy-to-use Web tools for in silico detection and characterization of whole-genome sequence (WGS) and whole-plasmid sequence data from members of the family Enterobacteriaceae. These tools will facilitate bacterial typing based on draft genomes of multidrug-resistant Enterobacteriaceae species by the rapid detection of known plasmid types. Replicon sequences from 559 fully sequenced plasmids associated with the family Enterobacteriaceae in the NCBI nucleotide database were collected to build a consensus database for integration into a Web tool called PlasmidFinder that can be used for replicon sequence analysis of raw, contig group, or completely assembled and closed plasmid sequencing data. The PlasmidFinder database currently consists of 116 replicon sequences that match with at least at 80% nucleotide identity all replicon sequences identified in the 559 fully sequenced plasmids. For plasmid multilocus sequence typing (pMLST) analysis, a database that is updated weekly was generated from www.pubmlst.org and integrated into a Web tool called pMLST. Both databases were evaluated using draft genomes from a collection of Salmonella enterica serovar Typhimurium isolates. PlasmidFinder identified a total of 103 replicons and between zero and five different plasmid replicons within each of 49 S. Typhimurium draft genomes tested. The pMLST Web tool was able to subtype genomic sequencing data of plasmids, revealing both known plasmid sequence types (STs) and new alleles and ST variants. In conclusion, testing of the two Web tools using both fully assembled plasmid sequences and WGS-generated draft genomes showed them to be able to detect a broad variety of plasmids that are often associated with antimicrobial resistance in clinically relevant bacterial pathogens. Copyright © 2014, American Society for Microbiology. All Rights Reserved.

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Identification of acquired antimicrobial resistance genes

Ea Zankari, Henrik Hasman, Salvatore Cosentino … (2012)

Objectives Identification of antimicrobial resistance genes is important for understanding the underlying mechanisms and the epidemiology of antimicrobial resistance. As the costs of whole-genome sequencing (WGS) continue to decline, it becomes increasingly available in routine diagnostic laboratories and is anticipated to substitute traditional methods for resistance gene identification. Thus, the current challenge is to extract the relevant information from the large amount of generated data. Methods We developed a web-based method, ResFinder that uses BLAST for identification of acquired antimicrobial resistance genes in whole-genome data. As input, the method can use both pre-assembled, complete or partial genomes, and short sequence reads from four different sequencing platforms. The method was evaluated on 1862 GenBank files containing 1411 different resistance genes, as well as on 23 de- novo-sequenced isolates. Results When testing the 1862 GenBank files, the method identified the resistance genes with an ID = 100% (100% identity) to the genes in ResFinder. Agreement between in silico predictions and phenotypic testing was found when the method was further tested on 23 isolates of five different bacterial species, with available phenotypes. Furthermore, ResFinder was evaluated on WGS chromosomes and plasmids of 30 isolates. Seven of these isolates were annotated to have antimicrobial resistance, and in all cases, annotations were compatible with the ResFinder results. Conclusions A web server providing a convenient way of identifying acquired antimicrobial resistance genes in completely sequenced isolates was created. ResFinder can be accessed at www.genomicepidemiology.org. ResFinder will continuously be updated as new resistance genes are identified.

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Author and article information

Contributors

Mabel Kamweli Aworh:

ORCID: http://orcid.org/0000-0003-4213-6929

mabelaworh@yahoo.com

Journal

Journal ID (nlm-ta): Antimicrob Resist Infect Control

Journal ID (iso-abbrev): Antimicrob Resist Infect Control

Title: Antimicrobial Resistance and Infection Control

Publisher: BioMed Central (London )

ISSN (Electronic): 2047-2994

Publication date (Electronic): 23 March 2021

Publication date PMC-release: 23 March 2021

Publication date Collection: 2021

Volume: 10

Electronic Location Identifier: 58

Affiliations

[1 ]GRID grid.473394.e, ISNI 0000 0004 1785 2322, Department of Veterinary and Pest Control Services, , Federal Ministry of Agriculture and Rural Development, ; Abuja, Nigeria

[2 ]Nigeria Field Epidemiology and Laboratory Training Programme, Abuja, Nigeria

[3 ]GRID grid.411225.1, ISNI 0000 0004 1937 1493, Department of Veterinary Public Health and Preventive Medicine, , Ahmadu Bello University, ; Zaria, Nigeria

[4 ]GRID grid.40803.3f, ISNI 0000 0001 2173 6074, Department of Population Health and Pathobiology, College of Veterinary Medicine, , North Carolina State University, ; Raleigh, NC USA

[5 ]GRID grid.5170.3, ISNI 0000 0001 2181 8870, WHO, FAO, EU, Reference Laboratory for Antimicrobial Resistance, National Food Institute, , Technical University of Denmark, ; Kgs. Lyngby, Denmark

Author information

Mabel Kamweli Aworh http://orcid.org/0000-0003-4213-6929

Article

Publisher ID: 930

DOI: 10.1186/s13756-021-00930-x

PMC ID: 7988975

PubMed ID: 33757589

SO-VID: 3eeebbaf-c314-4d53-8746-b477af3bcf79

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

History

Date received : 19 June 2020

Date accepted : 19 March 2021

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100000038, U.S. Food and Drug Administration;

Award ID: 1U18FD00678801

Award Recipient : Siddhartha Thakur

Custom metadata

ScienceOpen disciplines: Infectious disease & Microbiology

Keywords: escherichia coli,antimicrobial resistance,prevalence,chicken,multidrug resistance,genetic relatedness,one health,nigeria

Data availability:

ScienceOpen disciplines: Infectious disease & Microbiology

Keywords: escherichia coli, antimicrobial resistance, prevalence, chicken, multidrug resistance, genetic relatedness, one health, nigeria

Genetic relatedness of multidrug resistant Escherichia coli isolated from humans, chickens and poultry environments

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Supplementary Information

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Point-Of-Care Testing for AMR

Most cited references 52

SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing.

In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing.

Identification of acquired antimicrobial resistance genes

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