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      Molecular analysis of bla SHV, bla TEM, and bla CTX-M in extended-spectrum β-lactamase producing Enterobacteriaceae recovered from fecal specimens of animals

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          Abstract

          Colonization of extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae as animal gut microbiota is a substantial global threat. This study aimed to determine the molecular characterization of bla SHV, bla TEM, and bla CTX-M variants in animals, as well as to evaluate the antimicrobial resistance conferred by these genes. We prospectively analyzed 1273 fecal specimens of farm and domestic animals for the isolation of enterobacteria that had the ESBL phenotype by using biochemical methods. The extracted genes were amplified by polymerase chain reaction and sequenced for the characterization of bla SHV, bla TEM, and bla CTX-M variants. The drug-resistance spectrum and hierarchical clusters were analyzed against 19 antibacterial agents. Out of 245 (19.2%) ESBL enterobacteria, 180 (75.5%) Escherichia coli and 34 (13.9%) Klebsiella pneumoniae were prevalent species. A total of 73.9% bla CTX-M, 26.1% bla TEM, and 14.2% bla SHV were found among the enterobacteria; however, their association with farm or domestic animals was not statistically significant. The distribution of bla gene variants showed the highest number of bla CTX-M-1 (133; 54.3%), followed by bla CTX-M-15 (28; 11.4%), bla TEM-52 (40; 16.3%), and bla SHV-12 (22; 9%). In addition, 84.5% of the enterobacteria had the integrons intI1. We observed ±100% enterobacteria resistant to cephalosporin, 7 (2.9%) to colistin (minimum inhibitory concentration breakpoint ≥4 μg/mL), 9 (3.7%) to piperacillin-tazobactam, 11 (4.5%) to imipenem, 14 (5.7%) to meropenem, and 18 (7.3%) to cefoperazone-sulbactam, without statistically significant association. Animal gut microbiota contain a considerable number of bla CTX-M, bla TEM, bla SHV, and integrons, which are a potential source of acquired extensive drug resistance in human strains and leaves fewer therapeutic substitutes.

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          CTX-M-type β-lactamases: a successful story of antibiotic resistance.

          Production of extended-spectrum β-lactamases (ESBLs) is the principal mechanism of resistance to oxyimino-cephalosporins evolved by members of the family Enterobacteriaceae. Among the several ESBLs emerged among clinical pathogens, the CTX-M-type enzymes have proved the most successful in terms of promiscuity and diffusion in different epidemiological settings, where they have largely replaced and outnumbered other types of ESBLs. Originated by the capture and mobilization of chromosomal β-lactamase genes of strains of Kluyvera species, the blaCTX-M genes have become associated with a variety of mobile genetic elements that have mediated rapid and efficient inter-replicon and cell-to-cell dissemination involving highly successful enterobacterial lineages (e.g. Escherichia coli ST131 and ST405, or Klebsiella pneumoniae CC11 and ST147) to yield high-risk multiresistant clones that have spread on a global scale. The CTX-Mβ-lactamase lineage exhibits a striking plasticity, with a large number of allelic variants belonging in several sublineages, which can be associated with functional heterogeneity of clinical relevance. This review article provides an update on CTX-M-type ESBLs, with focus on structural and functional diversity, epidemiology and clinical significance. Copyright © 2013 Elsevier GmbH. All rights reserved.
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            Antibiotic resistance and extended spectrum beta-lactamases: Types, epidemiology and treatment.

            Antibiotic resistance is a problem of deep scientific concern both in hospital and community settings. Rapid detection in clinical laboratories is essential for the judicious recognition of antimicrobial resistant organisms. Production of extended-spectrum β-lactamases (ESBLs) is a significant resistance-mechanism that impedes the antimicrobial treatment of infections caused by Enterobacteriaceae and is a serious threat to the currently available antibiotic armory. ESBLs are classified into several groups according to their amino acid sequence homology. Proper infection control practices and barriers are essential to prevent spread and outbreaks of ESBL producing bacteria. As bacteria have developed different strategies to counter the effects of antibiotics, the identification of the resistance mechanism may help in the discovery and design of new antimicrobial agents. The carbapenems are widely regarded as the drugs of choice for the treatment of severe infections caused by ESBL-producing Enterobacteriaceae, although comparative clinical trials are scarce. Hence, more expeditious diagnostic testing of ESBL-producing bacteria and the feasible modification of guidelines for community-onset bacteremia associated with different infections are prescribed.
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              Extended-spectrum β-lactamase-producing and AmpC-producing Escherichia coli from livestock and companion animals, and their putative impact on public health: a global perspective.

              The possible zoonotic spread of antimicrobial-resistant bacteria is controversial. This review discusses global molecular epidemiological data combining both analyses of the chromosomal background, using multilocus sequence typing (MLST), and analyses of plasmid (episomal) extended-spectrum β-lactamase (ESBL)/AmpC genes in Escherichia coli present in humans and animals. For consideration of major epidemiological differences, animals were separated into livestock and companion animals. MLST revealed the existence of ESBL-producing isolates thoughout the E. coli population, with no obvious association with any ancestral EcoR group. A similar distribution of major ESBL/AmpC types was apparent only in human isolates, regardless of their geographical origin from Europe, Asia, or the Americas, whereas in animals this varied extensively between animal groups and across different geographical areas. In contrast to the diversity of episomal ESBL/AmpC types, isolates from human and animals mainly shared identical sequence types (STs), suggesting transmission or parallel micro-evolution. In conclusion, the opinion that animal ESBL-producing E. coli is a major source of human infections is oversimplified, and neglects a highly complex scenario. © 2012 The Authors. Clinical Microbiology and Infection © 2012 European Society of Clinical Microbiology and Infectious Diseases.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: InvestigationRole: Writing – original draft
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: MethodologyRole: SoftwareRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – original draft
                Role: Formal analysisRole: MethodologyRole: Writing – original draft
                Role: InvestigationRole: MethodologyRole: SoftwareRole: Writing – original draft
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ValidationRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: ValidationRole: Writing – original draft
                Role: Editor
                Journal
                PLoS One
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                7 January 2021
                2021
                : 16
                : 1
                : e0245126
                Affiliations
                [1 ] Department of Clinical Laboratory Sciences, College of Applied Medical Sciences, Jouf University, Al Jouf, Saudi Arabia
                [2 ] Department of Pathology, Tehsil Headquarter Hospital Kamoke, District Gujranwala, Pakistan
                [3 ] Faculty of Medical Laboratory Sciences, Omdurman Islamic University, Omdurman, Sudan
                [4 ] Department of Microbiology, Faculty of Life Sciences, Government College University, Faisalabad, Pakistan
                [5 ] Faculty of Medicine, Department of Medical Microbiology and Immunology, Menoufia University, Menoufia, Egypt
                [6 ] Department of Microbiology, King Abdulaziz Specialist Hospital, Sakaka, Saudi Arabia
                Nitte University, INDIA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0002-6185-2042
                https://orcid.org/0000-0002-2636-238X
                https://orcid.org/0000-0003-1239-4898
                Article
                PONE-D-20-21539
                10.1371/journal.pone.0245126
                7790543
                33412564
                7150b78c-d46e-4a9f-9715-e11f50d36d44
                © 2021 Ejaz et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 11 July 2020
                : 22 December 2020
                Page count
                Figures: 5, Tables: 4, Pages: 15
                Funding
                Funded by: Deanship of Scientific Research, Jouf University, Saudi Arabia
                Award ID: 47/40
                Award Recipient :
                HE received the award. The study was supported by the Deanship of Scientific Research, Jouf University, Al Jouf, Saudi Arabia, through project No. 47/40. Most of the authors are Jouf University employees, so the study design, data collection, and analysis, decision to publish, or preparation of the manuscript is contributed through the employees. https://www.ju.edu.sa/en/home/.
                Categories
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                Microbiology
                Microbial Control
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                Antibiotic Resistance
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