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      Evolution of Antibiotic Resistance of Coagulase-Negative Staphylococci Isolated from Healthy Turkeys in Egypt: First Report of Linezolid Resistance

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          Abstract

          Coagulase-negative staphylococci (CoNS) are gaining much attention as causative agents of serious nosocomial infections in humans. This study aimed to determine the prevalence and phenotypic antimicrobial resistance of CoNS as well as the presence of resistance-associated genes in CoNS isolated from turkey farms in Egypt. Two hundred and fifty cloacal swabs were collected from apparently healthy turkeys in Egypt. Suspected isolates were identified by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS). The susceptibility testing of CoNS isolates against 20 antimicrobial agents was performed using the broth microdilution test. The presence of resistance-associated genes like mecA, vanA, blaZ, erm(A), erm(B), erm(C), aac- aphD, optrA, valS, and cfr was determined. Thirty-nine CoNS were identified. All isolates were phenotypically resistant to trimethoprim/sulfamethoxazole, penicillin, ampicillin, and tetracycline. The resistance rates to erythromycin, chloramphenicol, oxacillin, daptomycin, and tigecycline were 97.4%, 94.9%, 92.3%, 89.7%, and 87.2%, respectively. Thirty-one isolates were resistant to linezolid (79.5%). Low resistance rate was detected for both imipenem and vancomycin (12.8%). The erm(C) gene was identified in all erythromycin phenotypically resistant isolates, whereas two resistant isolates possessed three resistance-conferring genes erm(A), erm(B), and erm(C). The cfr and optrA genes were detected in 11 (35.5%) and 12 (38.7%) of the 31 linezolid-resistant isolates. The mecA, aac- aphD, and blaZ genes were identified in 22.2%, 41.9%, and 2.6% of phenotypically resistant isolates to oxacillin, gentamicin, and penicillin, respectively. This is the first study revealing the correlation between linezolid resistance and presence of cfr and optrA genes in CoNS isolates from Egypt, and it can help to improve knowledge about the linezolid resistance mechanism.

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          Coagulase-negative staphylococci.

          The definition of the heterogeneous group of coagulase-negative staphylococci (CoNS) is still based on diagnostic procedures that fulfill the clinical need to differentiate between Staphylococcus aureus and those staphylococci classified historically as being less or nonpathogenic. Due to patient- and procedure-related changes, CoNS now represent one of the major nosocomial pathogens, with S. epidermidis and S. haemolyticus being the most significant species. They account substantially for foreign body-related infections and infections in preterm newborns. While S. saprophyticus has been associated with acute urethritis, S. lugdunensis has a unique status, in some aspects resembling S. aureus in causing infectious endocarditis. In addition to CoNS found as food-associated saprophytes, many other CoNS species colonize the skin and mucous membranes of humans and animals and are less frequently involved in clinically manifested infections. This blurred gradation in terms of pathogenicity is reflected by species- and strain-specific virulence factors and the development of different host-defending strategies. Clearly, CoNS possess fewer virulence properties than S. aureus, with a respectively different disease spectrum. In this regard, host susceptibility is much more important. Therapeutically, CoNS are challenging due to the large proportion of methicillin-resistant strains and increasing numbers of isolates with less susceptibility to glycopeptides.
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            A novel gene, optrA, that confers transferable resistance to oxazolidinones and phenicols and its presence in Enterococcus faecalis and Enterococcus faecium of human and animal origin.

            The oxazolidinone-resistant Enterococcus faecalis E349 from a human patient tested negative for the cfr gene and 23S rRNA mutations. Here we report the identification of a novel oxazolidinone resistance gene, optrA, and a first investigation of the extent to which this gene was present in E. faecalis and Enterococcus faecium from humans and food-producing animals.
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              The Cfr rRNA methyltransferase confers resistance to Phenicols, Lincosamides, Oxazolidinones, Pleuromutilins, and Streptogramin A antibiotics.

              A novel multidrug resistance phenotype mediated by the Cfr rRNA methyltransferase is observed in Staphylococcus aureus and Escherichia coli. The cfr gene has previously been identified as a phenicol and lincosamide resistance gene on plasmids isolated from Staphylococcus spp. of animal origin and recently shown to encode a methyltransferase that modifies 23S rRNA at A2503. Antimicrobial susceptibility testing shows that S. aureus and E. coli strains expressing the cfr gene exhibit elevated MICs to a number of chemically unrelated drugs. The phenotype is named PhLOPSA for resistance to the following drug classes: Phenicols, Lincosamides, Oxazolidinones, Pleuromutilins, and Streptogramin A antibiotics. Each of these five drug classes contains important antimicrobial agents that are currently used in human and/or veterinary medicine. We find that binding of the PhLOPSA drugs, which bind to overlapping sites at the peptidyl transferase center that abut nucleotide A2503, is perturbed upon Cfr-mediated methylation. Decreased drug binding to Cfr-methylated ribosomes has been confirmed by footprinting analysis. No other rRNA methyltransferase is known to confer resistance to five chemically distinct classes of antimicrobials. In addition, the findings described in this study represent the first report of a gene conferring transferable resistance to pleuromutilins and oxazolidinones.
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                Author and article information

                Journal
                Microorganisms
                Microorganisms
                microorganisms
                Microorganisms
                MDPI
                2076-2607
                22 October 2019
                October 2019
                : 7
                : 10
                : 476
                Affiliations
                [1 ]Friedrich-Loeffler-Institut, Institute of Bacterial Infections and Zoonoses, Naumburger Str. 96a, 07743 Jena, Germany; Helmut.hotzel@ 123456fli.de (H.H.); Herbert.tomaso@ 123456fli.de (H.T.); heinrich.neubauer@ 123456fli.de (H.N.)
                [2 ]Mansoura Provincial Laboratory, Animal Health Research Institute, Mansoura 35516, Egypt
                [3 ]Faculty of Veterinary Medicine, Mansoura University, Mansoura 35516, Egypt; omnia.awad100@ 123456gmail.com
                [4 ]Institute for Animal Hygiene and Environmental Health, Free University Berlin, Robert-von Ostertag-Str. 7-13, 14163 Berlin, Germany; uwe.roesler@ 123456fu-berlin.de
                [5 ]Institute for Poultry Diseases, Free University Berlin, Königsweg 63, 14163 Berlin, Germany; Hafez.Mohamed@ 123456fu-berlin.de
                [6 ]Faculty of Veterinary Medicine, Kafrelsheikh University, Kafr El-Sheikh 33516, Egypt
                Author notes
                [* ]Correspondence: Amira.moawad@ 123456fli.de (A.A.M.); Hosny.eladawy@ 123456fli.de (H.E.-A.); Tel.: +49-3641-804-2289 (A.A.M.); +49-3641-804-2249 (H.E.-A.)
                Author information
                https://orcid.org/0000-0002-8585-4237
                Article
                microorganisms-07-00476
                10.3390/microorganisms7100476
                6843140
                31652567
                b25b17ab-66a0-4edb-9a5c-f62b10133888
                © 2019 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 24 September 2019
                : 19 October 2019
                Categories
                Article

                staphylococci,linezolid,cons,turkey,egypt
                staphylococci, linezolid, cons, turkey, egypt

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