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      High β-lactam resistance in Gram-negative bacteria associated with kennel cough and cat flu in Egypt

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          Abstract

          Antimicrobial resistance within pets has gained worldwide attention due to pets close contact with humans. This report examined at the molecular level, the antimicrobial resistance mechanisms associated with kennel cough and cat flu. 1378 pets in total were assessed for signs of respiratory infection, and nasal and conjunctival swabs were collected across 76 diseased animals. Phenotypically, 27% of the isolates were characterized by multidrug resistance and possessed high levels of resistance rates to β-lactams. Phenotypic ESBLs/AmpCs production were identified within 40.5% and 24.3% of the isolates, respectively. Genotypically, ESBL- and AmpC-encoding genes were detected in 33.8% and 10.8% of the isolates, respectively, with bla SHV comprising the most identified ESBL, and bla CMY and bla ACT present as the AmpC with the highest levels. qnr genes were identified in 64.9% of the isolates, with qnrS being the most prevalent (44.6%). Several antimicrobial resistance determinants were detected for the first time within pets from Africa, including bla CTX-M-37, bla CTX-M-156, bla SHV-11, bla ACT-23, bla ACT25/31, bla DHA-1, and bla CMY-169. Our results revealed that pets displaying symptoms of respiratory illness are potential sources for pathogenic microbes possessing unique resistance mechanisms which could be disseminated to humans, thus leading to the development of severe untreatable infections in these hosts.

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          Development of a set of multiplex PCR assays for the detection of genes encoding important beta-lactamases in Enterobacteriaceae.

          To develop a rapid and reliable tool to detect by multiplex PCR assays the most frequently widespread beta-lactamase genes encoding the OXA-1-like broad-spectrum beta-lactamases, extended-spectrum beta-lactamases (ESBLs), plasmid-mediated AmpC beta-lactamases and class A, B and D carbapenemases. Following the design of a specific group of primers and optimization using control strains, a set of six multiplex PCRs and one simplex PCR was created. An evaluation of the set was performed using a collection of 31 Enterobacteriaceae strains isolated from clinical specimens showing a resistance phenotype towards broad-spectrum cephalosporins and/or cephamycins and/or carbapenems. Direct sequencing from PCR products was subsequently carried out to identify beta-lactamase genes. Under optimized conditions, all positive controls confirmed the specificity of group-specific PCR primers. Except for the detection of carbapenemase genes, multiplex and simplex PCR assays were carried out using the same PCR conditions, allowing assays to be performed in a single run. Out of 31 isolates selected, 22 strains produced an ESBL, mostly CTX-M-15 but also CTX-M-1 and CTX-M-9, SHV-12, SHV-5, SHV-2, TEM-21, TEM-52 and a VEB-type ESBL, 6 strains produced a plasmid-mediated AmpC beta-lactamase (five DHA-1 and one CMY-2) and 3 strains produced both an ESBL (two SHV-12, one CTX-M-15) and a plasmid-mediated AmpC beta-lactamase (DHA-1). We report here the development of a useful method composed of a set of six multiplex PCRs and one simplex PCR for the rapid screening of the most frequently encountered beta-lactamases. This method allowed direct sequencing from the PCR products.
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            Mechanisms of drug resistance: quinolone resistance.

            Quinolone antimicrobials are synthetic and widely used in clinical medicine. Resistance emerged with clinical use and became common in some bacterial pathogens. Mechanisms of resistance include two categories of mutation and acquisition of resistance-conferring genes. Resistance mutations in one or both of the two drug target enzymes, DNA gyrase and DNA topoisomerase IV, are commonly in a localized domain of the GyrA and ParE subunits of the respective enzymes and reduce drug binding to the enzyme-DNA complex. Other resistance mutations occur in regulatory genes that control the expression of native efflux pumps localized in the bacterial membrane(s). These pumps have broad substrate profiles that include quinolones as well as other antimicrobials, disinfectants, and dyes. Mutations of both types can accumulate with selection pressure and produce highly resistant strains. Resistance genes acquired on plasmids can confer low-level resistance that promotes the selection of mutational high-level resistance. Plasmid-encoded resistance is due to Qnr proteins that protect the target enzymes from quinolone action, one mutant aminoglycoside-modifying enzyme that also modifies certain quinolones, and mobile efflux pumps. Plasmids with these mechanisms often encode additional antimicrobial resistances and can transfer multidrug resistance that includes quinolones. Thus, the bacterial quinolone resistance armamentarium is large.
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              Pet animals as reservoirs of antimicrobial-resistant bacteria.

              Pet animal numbers have substantially increased in modern society and attention is increasingly devoted to pet welfare. Because of these changes, antimicrobial agents are frequently used in small animal veterinary practice, often including antimicrobial preparations used in human medicine, with heavy use of broad-spectrum agents such as aminopenicillins plus clavulanic acid, cephalosporins and fluoroquinolones. Several longitudinal studies conducted at veterinary hospitals have indicated that resistance to various antimicrobial agents has emerged amongst pet animal isolates of Staphylococcus intermedius, Escherichia coli and other bacteria, including species with a potential for zoonotic transmission and resistance phenotypes of clinical interest, such as methicillin-resistant Staphylococcus aureus, vancomycin-resistant enterococci and multidrug-resistant Salmonella Typhimurium DT104. Based on a review of the current literature, the role of pets in the dissemination of antimicrobial resistance has been given little attention when compared with that of food animals. A marked contrast is evident between the current policies on antimicrobial usage in food and companion animals. Apart from a few countries where limited data on antimicrobial usage and occurrence of resistance in bacteria from pet animals are provided, national surveillance programmes only focus on food animals. However, data on pet animals are clearly needed for guiding antimicrobial use policy in small animal veterinary practice as well as for assessing the risk of transmission of antimicrobial resistance to humans.
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                Author and article information

                Contributors
                hazem.khalifa1@vet.kfs.edu.eg
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                8 February 2021
                8 February 2021
                2021
                : 11
                : 3347
                Affiliations
                [1 ]GRID grid.411731.1, ISNI 0000 0004 0531 3030, Department of Infectious Diseases, Graduate School of Medicine, , International University of Health and Welfare, ; Narita, 286-0048 Japan
                [2 ]GRID grid.411978.2, ISNI 0000 0004 0578 3577, Department of Pharmacology, Faculty of Veterinary Medicine, , Kafrelsheikh University, ; Kafr El-Sheikh, Egypt
                [3 ]GRID grid.136304.3, ISNI 0000 0004 0370 1101, Division of Clinical Research, Medical Mycology Research Center, , Chiba University, ; Chiba, Japan
                [4 ]GRID grid.411978.2, ISNI 0000 0004 0578 3577, Department of Animal Medicine (Infectious Diseases), Faculty of Veterinary Medicine, , Kafrelsheikh University, ; Kafr El-Sheikh, Egypt
                [5 ]GRID grid.412764.2, ISNI 0000 0004 0372 3116, Department of Microbiology, , St. Marianna University School of Medicine, ; Sugao, Miyamae-ku, Kawasaki, Japan
                Author information
                http://orcid.org/0000-0001-9861-9693
                Article
                82061
                10.1038/s41598-021-82061-2
                7870956
                24c374b0-0919-483c-9953-2d003f46b574
                © The Author(s) 2021

                Open Access This 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/.

                History
                : 24 June 2020
                : 12 January 2021
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                © The Author(s) 2021

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                microbiology,molecular biology
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                microbiology, molecular biology

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