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      Occurrence and molecular characteristics of antimicrobial resistance, virulence factors, and extended-spectrum β-lactamase (ESBL) producing Salmonella enterica and Escherichia coli isolated from the retail produce commodities in Bangkok, Thailand

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          Abstract

          The incidence of antimicrobial resistance (AMR) in the environment is often overlooked and leads to serious health threats under the One Health paradigm. Infection with extended-spectrum β-lactamase (ESBL) producing bacteria in humans and animals has been widely examined, with the mode of transmission routes such as food, water, and contact with a contaminated environment. The purpose of this study was to determine the occurrence and molecular characteristics of resistant Salmonella enterica ( S. enterica) ( n = 59) and Escherichia coli ( E. coli) ( n = 392) isolated from produce commodities collected from fresh markets and supermarkets in Bangkok, Thailand. In this study, the S. enterica isolates exhibited the highest prevalence of resistance to tetracycline (11.9%) and streptomycin (8.5%), while the E. coli isolates were predominantly resistant to tetracycline (22.5%), ampicillin (21.4%), and sulfamethoxazole (11.5%). Among isolates of S. enterica (6.8%) and E. coli (15.3%) were determined as multidrug resistant (MDR). The prevalence of ESBL-producing isolates was 5.1% and 1.0% in S. enterica and E. coli, respectively. A minority of S. enterica isolates, where a single isolate exclusively carried bla CTX-M-55 (n = 1), and another isolate harbored both bla CTX-M-55 and bla TEM-1 (n = 1); similarly, a minority of E. coli isolates contained bla CTX-M-55 ( n = 2) and bla CTX-M-15 ( n = 1). QnrS (11.9%) and bla TEM (20.2%) were the most common resistant genes found in S. enterica and E. coli, respectively. Nine isolates resistant to ciprofloxacin contained point mutations in gyrA and parC. In addition, the odds of resistance to tetracycline among isolates of S. enterica were positively associated with the co-occurrence of ampicillin resistance and the presence of tetB ( P = 0.001), while the E. coli isolates were positively associated with ampicillin resistance, streptomycin resistance, and the presence of tetA ( P < 0.0001) in this study. In summary, these findings demonstrate that fresh vegetables and fruits, such as cucumbers and tomatoes, can serve as an important source of foodborne AMR S. enterica and E. coli in the greater Bangkok area, especially given the popularity of these fresh commodities in Thai cuisine.

          Highlights

          • First report on semi-quantitative data on antimicrobial resistance in S. enterica and E. coli isolated from vegetables and fruits in Thailand.

          • S. enterica And E. coli isolates were predominantly resistant to tetracycline (12% and 23%, respectively) with the multidrug resistance phenotype (7% and 15%, respectively).

          • ESBL-producing S. enterica ( n = 2) and E. coli ( n = 3) harbored CTX- M-55, which is commonly found in Thailand's livestock animals, aquaculture, humans, and the environment.

          • The QRDR mutation in gyrA and parC is trending toward being related to the level of ciprofloxacin resistance in this study.

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          Most cited references60

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          MEGA11: Molecular Evolutionary Genetics Analysis Version 11

          The Molecular Evolutionary Genetics Analysis (MEGA) software has matured to contain a large collection of methods and tools of computational molecular evolution. Here, we describe new additions that make MEGA a more comprehensive tool for building timetrees of species, pathogens, and gene families using rapid relaxed-clock methods. Methods for estimating divergence times and confidence intervals are implemented to use probability densities for calibration constraints for node-dating and sequence sampling dates for tip-dating analyses. They are supported by new options for tagging sequences with spatiotemporal sampling information, an expanded interactive Node Calibrations Editor , and an extended Tree Explorer to display timetrees. Also added is a Bayesian method for estimating neutral evolutionary probabilities of alleles in a species using multispecies sequence alignments and a machine learning method to test for the autocorrelation of evolutionary rates in phylogenies. The computer memory requirements for the maximum likelihood analysis are reduced significantly through reprogramming, and the graphical user interface has been made more responsive and interactive for very big data sets. These enhancements will improve the user experience, quality of results, and the pace of biological discovery. Natively compiled graphical user interface and command-line versions of MEGA11 are available for Microsoft Windows, Linux, and macOS from www.megasoftware.net .
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            The global burden of nontyphoidal Salmonella gastroenteritis.

            To estimate the global burden of nontyphoidal Salmonella gastroenteritis, we synthesized existing data from laboratory-based surveillance and special studies, with a hierarchical preference to (1) prospective population-based studies, (2) "multiplier studies," (3) disease notifications, (4) returning traveler data, and (5) extrapolation. We applied incidence estimates to population projections for the 21 Global Burden of Disease regions to calculate regional numbers of cases, which were summed to provide a global number of cases. Uncertainty calculations were performed using Monte Carlo simulation. We estimated that 93.8 million cases (5th to 95th percentile, 61.8-131.6 million) of gastroenteritis due to Salmonella species occur globally each year, with 155,000 deaths (5th to 95th percentile, 39,000-303,000 deaths). Of these, we estimated 80.3 million cases were foodborne. Salmonella infection represents a considerable burden in both developing and developed countries. Efforts to reduce transmission of salmonellae by food and other routes must be implemented on a global scale.
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              Extended-Spectrum β-Lactamases: a Clinical Update

              Extended-spectrum β-lactamases (ESBLs) are a rapidly evolving group of β-lactamases which share the ability to hydrolyze third-generation cephalosporins and aztreonam yet are inhibited by clavulanic acid. Typically, they derive from genes for TEM-1, TEM-2, or SHV-1 by mutations that alter the amino acid configuration around the active site of these β-lactamases. This extends the spectrum of β-lactam antibiotics susceptible to hydrolysis by these enzymes. An increasing number of ESBLs not of TEM or SHV lineage have recently been described. The presence of ESBLs carries tremendous clinical significance. The ESBLs are frequently plasmid encoded. Plasmids responsible for ESBL production frequently carry genes encoding resistance to other drug classes (for example, aminoglycosides). Therefore, antibiotic options in the treatment of ESBL-producing organisms are extremely limited. Carbapenems are the treatment of choice for serious infections due to ESBL-producing organisms, yet carbapenem-resistant isolates have recently been reported. ESBL-producing organisms may appear susceptible to some extended-spectrum cephalosporins. However, treatment with such antibiotics has been associated with high failure rates. There is substantial debate as to the optimal method to prevent this occurrence. It has been proposed that cephalosporin breakpoints for the Enterobacteriaceae should be altered so that the need for ESBL detection would be obviated. At present, however, organizations such as the Clinical and Laboratory Standards Institute (formerly the National Committee for Clinical Laboratory Standards) provide guidelines for the detection of ESBLs in klebsiellae and Escherichia coli . In common to all ESBL detection methods is the general principle that the activity of extended-spectrum cephalosporins against ESBL-producing organisms will be enhanced by the presence of clavulanic acid. ESBLs represent an impressive example of the ability of gram-negative bacteria to develop new antibiotic resistance mechanisms in the face of the introduction of new antimicrobial agents.
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                Author and article information

                Contributors
                Journal
                Heliyon
                Heliyon
                Heliyon
                Elsevier
                2405-8440
                23 February 2024
                15 March 2024
                23 February 2024
                : 10
                : 5
                : e26811
                Affiliations
                [a ]Department of Veterinary Public Health, Chulalongkorn University, Bangkok, Thailand
                [b ]Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, Davis, CA, USA
                [c ]Research Unit in Microbial Food Safety and Antimicrobial resistance, Department of Veterinary Public Health, Chulalongkorn University, Bangkok, Thailand
                Author notes
                []Corresponding author. Department of Veterinary Public Health, Chulalongkorn University, Bangkok, Thailand. Saharuetai.j@ 123456chula.ac.th
                Article
                S2405-8440(24)02842-1 e26811
                10.1016/j.heliyon.2024.e26811
                10912461
                38444485
                df6e5c8d-9ddc-43e9-885e-8424c1b181cd
                © 2024 The Authors

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 13 July 2023
                : 1 February 2024
                : 20 February 2024
                Categories
                Research Article

                antimicrobial resistance,esbl,escherichia coli,produce,salmonella enterica

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