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      Investigation of urban birds as source of β-lactamase-producing Gram-negative bacteria in Marseille city, France

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          Abstract

          Background

          We investigate here the presence of multidrug-resistant bacteria isolated from stool samples of yellow-legged gulls and chickens (n = 136) in urban parks and beaches of Marseille, France. Bacterial isolation was performed on selective media, including MacConkey agar with ceftriaxone and LBJMR medium. Antibiotic resistance genes, including extended-spectrum β-lactamases (ESBL) (i.e. bla CTX-M, bla TEM and bla SHV), carbapenemases ( bla KPC, bla VIM, bla NDM, bla OXA-23, bla OXA-24, bla OXA-48 and bla OXA-58) and colistin resistance genes ( mcr-1 to mcr-5) were screened by real-time PCR and standard PCR and sequenced when found.

          Results

          Of the 136 stools samples collected, seven ESBL-producing Gram-negative bacteria (BGN) and 12 colistin-resistant Enterobacteriaceae were isolated. Among them, five ESBL-producing Escherichia coli and eight colistin-resistant Hafnia alvei strains were identified. Four bla TEM-1 genes were detected in yellow-legged gulls and chickens. Three CTX-M-15 genes were detected in yellow-legged gulls and pigeons, and one CTX-M-1 in a yellow-legged gull. No mcr-1 to mcr-5 gene were detected in colistin-resistant isolates. Genotyping of E. coli strains revealed four different sequence types already described in humans and animals and one new sequence type.

          Conclusions

          Urban birds, which are believed to have no contact with antibiotics appear as potential source of ESBL genes. Our findings highlight the important role of urban birds in the proliferation of multidrug-resistant bacteria and also the possible zoonotic transmission of such bacteria from wild birds to humans.

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          Most cited references33

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          Global epidemiology of CTX-M β-lactamases: temporal and geographical shifts in genotype.

          Globally, rates of ESBL-producing Enterobacteriaceae are rising. We undertook a literature review, and present the temporal trends in blaCTX-M epidemiology, showing that blaCTX-M-15 and blaCTX-M-14 have displaced other genotypes in many parts of the world. Explanations for these changes can be attributed to: (i) horizontal gene transfer (HGT) of plasmids; (ii) successful Escherichia coli clones; (iii) ESBLs in food animals; (iv) the natural environment; and (v) human migration and access to basic sanitation. We also provide explanations for the changing epidemiology of blaCTX-M-2 and blaCTX-M-27. Modifiable anthropogenic factors, such as poor access to basic sanitary facilities, encourage the spread of blaCTX-M and other antimicrobial resistance (AMR) genes, such as blaNDM, blaKPC and mcr-1. We provide further justification for novel preventative and interventional strategies to reduce transmission of these AMR genes.
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            Dissemination of Escherichia coli with CTX-M Type ESBL between Humans and Yellow-Legged Gulls in the South of France

            Extended Spectrum β-Lactamase (ESBL) producing Enterobacteriaceae started to appear in the 1980s, and have since emerged as some of the most significant hospital-acquired infections with Escherichia coli and Klebsiella being main players. More than 100 different ESBL types have been described, the most widespread being the CTX-M β-lactamase enzymes (bla CTX-M genes). This study focuses on the zoonotic dissemination of ESBL bacteria, mainly CTX-M type, in the southern coastal region of France. We found that the level of general antibiotic resistance in single randomly selected E. coli isolates from wild Yellow-legged Gulls in France was high. Nearly half the isolates (47,1%) carried resistance to one or more antibiotics (in a panel of six antibiotics), and resistance to tetracycline, ampicillin and streptomycin was most widespread. In an ESBL selective screen, 9,4% of the gulls carried ESBL producing bacteria and notably, 6% of the gulls carried bacteria harboring CTX-M-1 group of ESBL enzymes, a recently introduced and yet the most common clinical CTX-M group in France. Multi locus sequence type and phylogenetic group designations were established for the ESBL isolates, revealing that birds and humans share E. coli populations. Several ESBL producing E. coli isolated from birds were identical to or clustered with isolates with human origin. Hence, wild birds pick up E. coli of human origin, and with human resistance traits, and may accordingly also act as an environmental reservoir and melting pot of bacterial resistance with a potential to re-infect human populations.
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              Prevalence and molecular epidemiology of CTX-M extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in Russian hospitals.

              A total of 904 consecutive nosocomial isolates of Escherichia coli and Klebsiella pneumoniae collected from 28 Russian hospitals were screened for production of extended-spectrum beta-lactamases (ESBLs). The ESBL phenotype was detected in 78 (15.8%) E. coli and 248 (60.8%) K. pneumoniae isolates. One hundred fifteen isolates carried the genes for CTX-M-type beta-lactamases, which, as shown by PCR-restriction fragment length polymorphism analysis, were distributed into the two genetic groups of CTX-M-1 (93%)- and CTX-M-2 (7%)-related enzymes. Isolates producing the enzymes of the first group were found in 20 hospitals from geographically distant regions of the country and were characterized by considerable diversity of genetic types, as was demonstrated by enterobacterial repetitive consensus PCR typing. Within this group the CTX-M-3 and the CTX-M-15 beta-lactamases were identified. In contrast, the enzymes of the CTX-M-2 group (namely, CTX-M-5) were detected only in eight clonally related E. coli isolates from a single hospital. Notably, the levels of resistance to ceftazidime were remarkably variable among the CTX-M producers. This study provides further evidence of the global dissemination of CTX-M type ESBLs and emphasizes the need for their epidemiological monitoring.
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                Author and article information

                Contributors
                edgarthengaiganam@yahoo.fr
                isabelle.pagnier@univ-amu.fr
                chaalal_w@hotmail.fr
                winmicro40@hotmail.com
                chabouselma@gmail.com
                jean-marc.rolain@univ-amu.fr
                seydina.diene@univ-amu.fr
                Journal
                Acta Vet Scand
                Acta Vet. Scand
                Acta Veterinaria Scandinavica
                BioMed Central (London )
                0044-605X
                1751-0147
                31 October 2019
                31 October 2019
                2019
                : 61
                : 51
                Affiliations
                [1 ]ISNI 0000 0001 2176 4817, GRID grid.5399.6, IRD, APHM, MEPHI, , IHU-Mediterranee Infection, Aix-Marseille Univ, ; 19-21 bd Jean Moulin, 13005 Marseille, France
                [2 ]ISNI 0000 0004 0519 5986, GRID grid.483853.1, IHU-Mediterranee Infection, ; Marseille, France
                Article
                486
                10.1186/s13028-019-0486-9
                6822345
                31672159
                a4f614a7-167c-4b8d-9ccd-13ca590b44bf
                © The Author(s) 2019

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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.

                History
                : 19 February 2019
                : 22 October 2019
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100007356, Fondation Méditerranée Infection;
                Award ID: 10-IAHU-03
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2019

                Veterinary medicine
                chickens,extended-spectrum beta-lactamases (esbl),marseille,pigeons,urban birds,yellow-legged gulls

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