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      Antibiogram Signatures of Some Enterobacteria Recovered from Irrigation Water and Agricultural Soil in two District Municipalities of South Africa

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          Abstract

          This study was undertaken to evaluate the antibiogram fingerprints of some Enterobacteria recovered from irrigation water and agricultural soil in two District Municipalities of the Eastern Cape Province, South Africa using standard culture-based and molecular methods. The prevalent resistance patterns in the isolates follow the order: Salmonella enterica serovar Typhimurium [tetracycline (92.3%), ampicillin (69.2%)]; Enterobacter cloacae [amoxicillin/clavulanic acid (77.6%), ampicillin (84.5%), cefuroxime (81.0%), nitrofurantoin (81%), and tetracycline (80.3%)]; Klebsiella pneumoniae [amoxicillin/clavulanic acid (80.6%), ampicillin (88.9%), and cefuroxime (61.1%)]; and Klebsiella oxytoca [chloramphenicol (52.4%), amoxicillin/clavulanic acid (61.9%), ampicillin (61.9%), and nitrofurantoin (61.9%)]. Antibiotic resistance genes detected include tetC (86%), sulII (86%), and bla AmpC (29%) in Salmonella enterica serovar Typhimurium., tetA (23%), tetB (23%), tetC (12%), sulI (54%), sulII (54%), catII (71%), bla AmpC (86%), bla TEM (43%), and bla PER (17%) in Enterobacter cloacae., tetA (20%), tetC (20%), tetD (10%), sulI (9%), sulII (18%), FOX (11%) and CIT (11%)-type plasmid-mediated AmpC, bla TEM (11%), and bla SHV (5%) in Klebsiella pneumoniae and bla AmpC (18%) in Klebsiella oxytoca. Our findings document the occurrence of some antibiotic-resistant Enterobacteria in irrigation water and agricultural soil in Amathole and Chris Hani District Municipalities, Eastern Cape Province of South Africa, thus serving as a potential threat to food safety.

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          Extended-spectrum beta-lactamase-producing Enterobacteriaceae: an emerging public-health concern.

          The medical community relies on clinical expertise and published guidelines to assist physicians with choices in empirical therapy for system-based infectious syndromes, such as community-acquired pneumonia and urinary-tract infections (UTIs). From the late 1990s, multidrug-resistant Enterobacteriaceae (mostly Escherichia coli) that produce extended-spectrum beta lactamases (ESBLs), such as the CTX-M enzymes, have emerged within the community setting as an important cause of UTIs. Recent reports have also described ESBL-producing E coli as a cause of bloodstream infections associated with these community-onset UTIs. 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. Thus, more rapid diagnostic testing of ESBL-producing bacteria and the possible modification of guidelines for community-onset bacteraemia associated with UTIs are required.
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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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              CTX-M Enzymes: Origin and Diffusion

              CTX-M β-lactamases are considered a paradigm in the evolution of a resistance mechanism. Incorporation of different chromosomal bla CTX-M related genes from different species of Kluyvera has derived in different CTX-M clusters. In silico analyses have shown that this event has occurred at least nine times; in CTX-M-1 cluster (3), CTX-M-2 and CTX-M-9 clusters (2 each), and CTX-M-8 and CTX-M-25 clusters (1 each). This has been mainly produced by the participation of genetic mobilization units such as insertion sequences (ISEcp1 or ISCR1) and the later incorporation in hierarchical structures associated with multifaceted genetic structures including complex class 1 integrons and transposons. The capture of these bla CTX-M genes from the environment by highly mobilizable structures could have been a random event. Moreover, after incorporation within these structures, β-lactam selective force such as that exerted by cefotaxime and ceftazidime has fueled mutational events underscoring diversification of different clusters. Nevertheless, more variants of CTX-M enzymes, including those not inhibited by β-lactamase inhibitors such as clavulanic acid (IR-CTX-M variants), only obtained under in in vitro experiments, are still waiting to emerge in the clinical setting. Penetration and the later global spread of CTX-M producing organisms have been produced with the participation of the so-called “epidemic resistance plasmids” often carried in multi-drug resistant and virulent high-risk clones. All these facts but also the incorporation and co-selection of emerging resistance determinants within CTX-M producing bacteria, such as those encoding carbapenemases, depict the currently complex pandemic scenario of multi-drug resistant isolates.
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                Author and article information

                Journal
                Microorganisms
                Microorganisms
                microorganisms
                Microorganisms
                MDPI
                2076-2607
                07 August 2020
                August 2020
                : 8
                : 8
                Affiliations
                [1 ]SAMRC Microbial Water Quality Monitoring Centre, University of Fort Hare, Alice 5700, South Africa; nnontongana@ 123456ufh.ac.za (N.N.); aokoh@ 123456ufh.ac.za (A.I.O.)
                [2 ]Applied and Environmental Microbiology Research Group, Department of Biochemistry and Microbiology, University of Fort Hare, Alice 5700, South Africa
                [3 ]Department of Plant and Soil Sciences, Faculty of Natural and Agricultural Sciences, University of Pretoria, Pretoria 0002, South Africa; erika.duplessis@ 123456up.ac.za (E.M.d.P.); lise.korsten@ 123456up.ac.za (L.K.)
                Author notes
                Article
                microorganisms-08-01206
                10.3390/microorganisms8081206
                7463487
                32784678
                d29ec46b-e787-4eb4-b523-fff57334607a
                © 2020 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/).

                Categories
                Article

                antibiotic resistance,irrigation water,agricultural soil,public health,food safety,food microbiology,environmental health

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