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Abstract
The increasing occurrence of multidrug-resistant (MDR) extended-spectrum β-lactamase- (ESBL) and/or AmpC β-lactamase- (AmpC) producing Enterobacterales in irrigation water and associated irrigated fresh produce represents risks related to the environment, food safety, and public health. In South Africa, information about the presence of ESBL/AmpC-producing Enterobacterales from non-clinical sources is limited, particularly in the water–plant-food interface. This study aimed to characterize 19 selected MDR ESBL/AmpC-producing Escherichia coli (n=3), Klebsiella pneumoniae (n=5), Serratia fonticola (n=10), and Salmonella enterica (n=1) isolates from spinach and associated irrigation water samples from two commercial spinach production systems within South Africa, using whole genome sequencing (WGS). Antibiotic resistance genes potentially encoding resistance to eight different classes were present, with blaCTX-M-15 being the dominant ESBL encoding gene and blaACT-types being the dominant AmpC encoding gene detected. A greater number of resistance genes across more antibiotic classes were seen in all the K. pneumoniae strains, compared to the other genera tested. From one farm, blaCTX-M-15-positive K. pneumoniae strains of the same sequence type 985 (ST 985) were present in spinach at harvest and retail samples after processing, suggesting successful persistence of these MDR strains. In addition, ESBL-producing K. pneumoniae ST15, an emerging high-risk clone causing nosocomical outbreaks worldwide, was isolated from irrigation water. Known resistance plasmid replicon types of Enterobacterales including IncFIB, IncFIA, IncFII, IncB/O, and IncHI1B were observed in all strains following analysis with PlasmidFinder. However, blaCTX-M-15 was the only β-lactamase resistance gene associated with plasmids (IncFII and IncFIB) in K. pneumoniae (n=4) strains. In one E. coli and five K. pneumoniae strains, integron In191 was observed. Relevant similarities to human pathogens were predicted with PathogenFinder for all 19 strains, with a confidence of 0.635–0.721 in S. fonticola, 0.852–0.931 in E. coli, 0.796–0.899 in K. pneumoniae, and 0.939 in the S. enterica strain. The presence of MDR ESBL/AmpC-producing E. coli, K. pneumoniae, S. fonticola, and S. enterica with similarities to human pathogens in the agricultural production systems reflects environmental and food contamination mediated by anthropogenic activities, contributing to the spread of antibiotic resistance genes.
Highlights
The discovery of antibiotics in the 1940s led to a new age in medical care
Plasmid-mediated AmpC β-lactamases (AmpCs) genes were present in two E. coli strains from irrigation water and blaACT-13, blaACT-38, blaACT-6, and/or blaACT-58 were present in 10 S. fonticola strains from irrigation water (n = 2) and spinach (n = 8) samples (Figure 1)
The ESBL genes included blaSFO-1 in all 10 S. fonticola strains, blaCTX-M-15 in five K. pneumoniae strains from irrigation water and spinach, and one E. coli strain from spinach
Summary
The discovery of antibiotics in the 1940s led to a new age in medical care. the global increase in antimicrobial resistance (AMR) is reducing the effectiveness of clinically important antibiotics (Lobanovska and Pilla, 2017; Dandachi et al, 2019). Plasmid encoded AmpC genes have been known since 1989 (Jacoby, 2009) and are regularly reported in clinical and environmental strains (Khari et al, 2016; Colosi et al, 2020; Tekele et al, 2020) Both chromosomally encoded and plasmid-mediated AmpC β-lactamases confer resistance to a broad spectrum of β-lactams such as penicillins, oxyimino-cephalosporins (including cefotaxime and ceftazidime), cephamycins, and aztreonam at variable levels (Jacoby, 2009; Palzkill, 2018; Furlan and Stehling, 2021; Lopes et al, 2021b)
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