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      Prevalence of Beta-Lactam and Quinolone/Fluoroquinolone Resistance in Enterobacteriaceae From Dogs in France and Spain—Characterization of ESBL/pAmpC Isolates, Genes, and Conjugative Plasmids

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          Abstract

          Quantitative data on fecal shedding of antimicrobial-resistant bacteria are crucial to assess the risk of transmission from dogs to humans. Our first objective was to investigate the prevalence of quinolone/fluoroquinolone-resistant and beta-lactam-resistant Enterobacteriaceae in dogs in France and Spain. Due to the particular concern about possible transmission of extended-spectrum cephalosporin (ESC)-resistant isolates from dogs to their owners, we characterized the ESBL/pAmpC producers collected from dogs. Rectal swabs from 188 dogs, without signs of diarrhea and that had not received antimicrobials for 4 weeks before the study, were quantified for total and resistant Enterobacteriaceae on selective media alone or containing relevant antibiotic concentrations. Information that might explain antibiotic resistance was collected for each dog. Extended-spectrum cephalosporin-resistant isolates were subjected to bacterial species identification (API20E), genetic lineage characterization (MLST), ESBL/pAmpC genes identification (sequencing), and plasmid characterization (pMLST). Regarding beta-lactam resistance, amoxicillin- (AMX) and cefotaxime- (CTX) resistant Enterobacteriaceae were detected in 70 and 18% of the dogs, respectively, whereas for quinolone/fluoroquinolone-resistance, Nalidixic acid- (NAL) and ciprofloxacin- (CIP) resistant Enterobacteriaceae were detected in 36 and 18% of the dogs, respectively. Medical rather than preventive consultation was a risk marker for the presence of NAL and CIP resistance. CTX resistance was mainly due to a combination of specific ESBL/pAmpC genes and particular conjugative plasmids already identified in human patients: bla CTX−M−1/IncI1/ST3 ( n = 4), bla CMY−2/IncI1/ST12 ( n = 2), and bla CTX−M−15/IncI1/ST31 ( n = 1). bla SHV−12 ( n = 3) was detected in various plasmid lineages (InI1/ST3, IncI1/ST26, and IncFII). ESBL/pAmpC plasmids were located in different genetic lineages of E. coli, with the exception of two strains in France (ST6998) and two in Spain (ST602). Our study highlights dogs as a potential source of Q/FQ-resistant and ESBL/pAmpC-producing bacteria that might further disseminate to humans, and notably a serious risk of future acquisition of CTX-M-1 and CMY-2 plasmids by the owners of dogs.

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          Most cited references40

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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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            Rapid procedure for detection and isolation of large and small plasmids.

            Procedures are described for the detection and isolation of plasmids of various sizes (2.6 to 350 megadaltons) that are harbored in species of Agrobacterium, Rhizobium, Escherichia, Salmonella, Erwinia, Pseudomonas, and Xanthomonas. The method utilized the molecular characteristics of covalently closed circular deoxyribonucleic acid (DNA) that is released from cells under conditions that denature chromosomal DNA by using alkaline sodium dodecyl sulfate (pH 12.6) at elevated temperatures. Proteins and cell debris were removed by extraction with phenol-chloroform. Under these conditions chromosomal DNA concentrations were reduced or eliminated. The clarified extract was used directly for electrophoretic analysis. These procedures also permitted the selective isolation of plasmid DNA that can be used directly in nick translation, restriction endonuclease analysis, transformation, and DNA cloning experiments.
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              Antibiotics used most commonly to treat animals in Europe

              The Heads of Medicines Agencies and the Federation of Veterinarians of Europe undertook a survey to gain an insight into European prescribing of antibiotics for animals, in particular to highlight the diseases for which antibiotics are most commonly said to be prescribed and which different classes, including human critically important antibiotics (CIAs). The survey was completed by 3004 practitioners from 25 European countries. Many older antibiotics (eg, penicillins, tetracyclines) are cited most frequently as the prescribed classes to treat the main food producing species. The frequency of citation of non-CIAs predominates. CIAs are mostly frequently cited to be prescribed for: urinary diseases in cats (62 per cent), respiratory diseases in cattle (45 per cent), diarrhoea in cattle and pigs (respectively 29 per cent and 34 per cent), locomotion disorders in cattle (31 per cent), postpartum dysgalactia syndrome complex in pigs (31 per cent) and dental disease in dogs (36 per cent). Clear ‘preferences’ between countries can be observed between antibiotic classes. The use of national formularies and guidance helps to drive responsible use of antibiotics and can significantly reduce the extent of use of CIAs. A more widespread introduction of veterinary practice antibiotic prescribing policies and monitoring obedience to these should ensure more widespread compliance with responsible use guidelines.
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                Author and article information

                Contributors
                Journal
                Front Vet Sci
                Front Vet Sci
                Front. Vet. Sci.
                Frontiers in Veterinary Science
                Frontiers Media S.A.
                2297-1769
                30 August 2019
                2019
                : 6
                : 279
                Affiliations
                [1] 1InTheRes, Université de Toulouse, INRA, ENVT , Toulouse, France
                [2] 2Da Volterra , Paris, France
                [3] 3Departamento de Sanidad Animal, Facultad de Veterinaria y Centro de Vigilancia Sanitaria Veterinaria (VISAVET), Universidad Complutense de Madrid , Madrid, Spain
                [4] 4UDEAR, Université de Toulouse, INSERM, ENVT , Toulouse, France
                [5] 5Centro Veterinario Loranca , Fuenlabrada, Spain
                Author notes

                Edited by: Silke Salavati, University of Edinburgh, United Kingdom

                Reviewed by: Roger Stephan, University of Zurich, Switzerland; Abdelaziz Touati, University of Béjaïa, Algeria; Torahiko Okubo, Hokkaido University, Japan

                *Correspondence: Véronique Dupouy v.dupouy@ 123456envt.fr

                This article was submitted to Comparative and Clinical Medicine, a section of the journal Frontiers in Veterinary Science

                Article
                10.3389/fvets.2019.00279
                6730528
                31544108
                6c1ca081-c5ce-448a-91ae-a3895561acfa
                Copyright © 2019 Dupouy, Abdelli, Moyano, Arpaillange, Bibbal, Cadiergues, Lopez-Pulin, Sayah-Jeanne, de Gunzburg, Saint-Lu, Gonzalez-Zorn, Andremont and Bousquet-Mélou.

                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) and the copyright owner(s) 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
                : 31 May 2019
                : 07 August 2019
                Page count
                Figures: 1, Tables: 3, Equations: 0, References: 49, Pages: 10, Words: 7025
                Funding
                Funded by: Institut National de la Recherche Agronomique 10.13039/501100006488
                Categories
                Veterinary Science
                Original Research

                dog,feces,antibiotic resistance,esbl/pampc,fluoroquinolone,plasmid

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