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      CTX-M-15-Producing E. coli Isolates from Food Products in Germany Are Mainly Associated with an IncF-Type Plasmid and Belong to Two Predominant Clonal E. coli Lineages

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          Abstract

          Extended-spectrum beta-lactamases (ESBL) mediating resistance to 3rd generation cephalosporins are a major public health issue. As food may be a vehicle in the spread of ESLB-producing bacteria, a study on the occurrence of cephalosporin-resistantu Escherichia coli in food was initiated. A total of 404 ESBL-producing isolates were obtained from animal-derived food samples (e.g., poultry products, pork, beef and raw milk) between 2011 and 2013. As CTX-M-15 is the most abundant enzyme in ESBL-producing E. coli causing human infections, this study focusses on E. coli isolates from food samples harboring the bla CTX-M-15 gene. The bla CTX-M-15 gene was detected in 5.2% ( n = 21) of all isolates. Molecular analyses revealed a phylogenetic group A ST167 clone that was repeatedly isolated from raw milk and beef samples over a period of 6 months. The analyses indicate that spread of CTX-M-15-producing E. coli in German food samples were associated with a multireplicon IncF (FIA FIB FII) plasmid and additional antimicrobial resistance genes such as aac(6)-Ib-cr, bla OXA−1, catB3, different tet-variants as well as a class 1 integron with an aadA5/dfrA17 gene cassette. In addition, four phylogenetic group A ST410 isolates were detected. Three of them carried a chromosomal copy of the bla CTX-M-15 gene and a single isolate with the gene on a 90 kb IncF plasmid. The bla CTX-M-15 gene was always associated with the IS Ecp1 element. In conclusion, CTX-M-15-producing E. coli were detected in German food samples. Among isolates of different matrices, two prominent clonal lineages, namely A-ST167 and A-ST410, were identified. These lineages may be important for the foodborne dissemination of CTX-M-15-producing E. coli in Germany. Interestingly, these clonal lineages were reported to be widely distributed and especially prevalent in isolates from humans and livestock. Transmission of CTX-M-15-harboring isolates from food-producing animals to food appears probable, as isolates obtained from livestock and food samples within the same time period exhibit comparable characteristics as compared to isolates detected from human. However, the routes and direction of transmission need further investigation.

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          Most cited references32

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          Resistance plasmid families in Enterobacteriaceae.

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            Plasmids and the spread of resistance.

            Plasmids represent one of the most difficult challenge for counteracting the dissemination of antimicrobial resistance. They contribute to the spread of relevant resistance determinants, promoting horizontal gene transfer among unrelated bacteria. Undistinguishable plasmids were identified in unrelated bacterial strains isolated at huge geographically distant area, with no apparent epidemiological links. These plasmids belong to families that are largely prevalent in naturally occurring bacteria, usually carry multiple physically linked genetic determinants, conferring resistance to different classes of antibiotics simultaneously. Plasmids also harbour virulence factors and addiction systems, promoting their stability and maintenance in the bacterial host, in different environmental conditions. The characteristics of the most successful plasmids that were at the origin of the spread of carbapenemase, expanded-spectrum β-lactamase, and plasmid-mediated quinolone resistance genes are discussed in this review. Copyright © 2013 Elsevier GmbH. All rights reserved.
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              Dutch patients, retail chicken meat and poultry share the same ESBL genes, plasmids and strains.

              Intestinal carriage of extended-spectrum beta-lactamase (ESBL) -producing bacteria in food-producing animals and contamination of retail meat may contribute to increased incidences of infections with ESBL-producing bacteria in humans. Therefore, distribution of ESBL genes, plasmids and strain genotypes in Escherichia coli obtained from poultry and retail chicken meat in the Netherlands was determined and defined as 'poultry-associated' (PA). Subsequently, the proportion of E. coli isolates with PA ESBL genes, plasmids and strains was quantified in a representative sample of clinical isolates. The E. coli were derived from 98 retail chicken meat samples, a prevalence survey among poultry, and 516 human clinical samples from 31 laboratories collected during a 3-month period in 2009. Isolates were analysed using an ESBL-specific microarray, sequencing of ESBL genes, PCR-based replicon typing of plasmids, plasmid multi-locus sequence typing (pMLST) and strain genotyping (MLST). Six ESBL genes were defined as PA (bla(CTX-M-1) , bla(CTX-M-2) , bla(SHV-2) , bla(SHV-12) , bla(TEM-20) , bla(TEM-52) ): 35% of the human isolates contained PA ESBL genes and 19% contained PA ESBL genes located on IncI1 plasmids that were genetically indistinguishable from those obtained from poultry (meat). Of these ESBL genes, 86% were bla(CTX-M-1) and bla(TEM-52) genes, which were also the predominant genes in poultry (78%) and retail chicken meat (75%). Of the retail meat samples, 94% contained ESBL-producing isolates of which 39% belonged to E. coli genotypes also present in human samples. These findings are suggestive for transmission of ESBL genes, plasmids and E. coli isolates from poultry to humans, most likely through the food chain. 2011 The Authors. Clinical Microbiology and Infection; 2011 European Society of Clinical Microbiology and Infectious Diseases.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                21 November 2017
                2017
                : 8
                : 2318
                Affiliations
                [1] 1Department Biological Safety, German Federal Institute for Risk Assessment , Berlin, Germany
                [2] 2Institute of Medical Microbiology, German Center for Infection Research, Partner Site Giessen-Marburg-Langen, Justus Liebig University , Giessen, Germany
                [3] 3Barcelona Institute for Global Health (ISGlobal), Hospital Clínic-Universitat de Barcelona , Barcelona, Spain
                [4] 4European Food Safety Authority , Parma, Italy
                [5] 5Institute of Veterinary Public Health, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine , Vienna, Austria
                Author notes

                Edited by: Alberto Quesada, Universidad de Extremadura, Spain

                Reviewed by: Campos Jorge Campos, ESTM-IPLeiria, Portugal; Luisa Peixe, Universidade do Porto, Portugal

                *Correspondence: Jens A. Hammerl jens-andre.hammerl@ 123456bfr.bund.de

                This article was submitted to Food Microbiology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2017.02318
                5702323
                29209306
                ffadee78-3d19-45e3-805c-d8b40ab0b5a8
                Copyright © 2017 Irrgang, Falgenhauer, Fischer, Ghosh, Guiral, Guerra, Schmoger, Imirzalioglu, Chakraborty, Hammerl and Käsbohrer.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 03 June 2017
                : 09 November 2017
                Page count
                Figures: 2, Tables: 2, Equations: 0, References: 44, Pages: 10, Words: 5978
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                antimicrobial resistance,ctx-m-15,livestock,genome,plasmid,distribution,esbl
                Microbiology & Virology
                antimicrobial resistance, ctx-m-15, livestock, genome, plasmid, distribution, esbl

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