One health investigation of multidrug resistance efflux pump OqxAB-positive escherichia coli from food-chain and human samples

Abstract

An increase in antibiotic resistance during the past decade has revived the use of old antibiotics and, nowadays, nitrofurantoin is frequently used to treat urinary tract infections. However, the plasmid-mediated multidrug-resistant efflux pump OqxAB, which can induce resistance against nitrofurantoin and other antibiotics, is frequently reported in China. Here, we studied the prevalence of oqxAB-positive Escherichia coli in food chain samples and its molecular epidemiology in food chain and clinical isolates, to increase our understanding of oqxAB dissemination in Hong Kong and aid the use of antimicrobials in the future.

The prevalence of oqxAB-positive E. coli was determined for various food chain samples, of which 207 non-duplicate isolates were recovered from animal faecal samples (17%, pigs 89/152; chickens 11/300; cattle 2/150), raw meat samples (13%, fresh meat 52/79; chilled meat 46/649), and food-processing surface swab samples (7%, wet-market 5/8; household 2/95). A high prevalence of oqxAB-positive E. coli was observed in fresh meat samples and wet market surface samples, suggesting that wet markets could served as the bacteria niche and the food chain plays an important role in disseminating the bacteria.

The molecular epidemiology of 78 food-chain and 20 human oqxAB-positive E. coli were investigated by WGS. The majority of isolates were classified as non-pathogenic strains from multiple lineages and no significant correlation was observed between the clinical and food chain isolates. It is worth mentioning that high risk ST410 clones with known capability to causes outbreak were identified from several clinical isolates. From isolates of various sources, structurally similar IncF plasmids were identified, suggesting that oqxAB is disseminated via horizontal gene transfer. Similar sets of virulence factors and antibiotic resistance genes were encoded by plasmids of the same IncF alleles, and most virulence factors enhancing bacteria host survival and most of the resistance genes conferring resistance against first-line antibiotics used in clinical settings.

Further investigation of virulence factors encoded by oqxAB-encoding IncF plasmids was conducted using Galleria mellonella larvae infection model, with isogenic pairs of E. coli J53 with or without oqxAB-encoding IncF plasmids. Significant health decline was only observed in larvae infected with plasmid-carrying transconjugant, suggested the oqxAB-encoding IncF plasmids did increase the pathogenicity of the bacteria.

Furthermore, in response to the isolation of oqxAB-positive E. coli from food-processing surfaces, various cleaning methods were tested for their antibacterial efficiency to identify an effective method for disinfecting wooden cutting boards. Among tested methods, hot water submerging and flushing achieved 5-log reduction in all tests with steam cleaning showed a lower reduction against E. faecalis, while ozonated water only achieved 2-log bacterial reduction. Hot water methods were then recommended to be used household settings while steam cleaning was recommended for wet market used,

This study demonstrated how oqxAB-positive E. coli disseminated in Hong Kong through food chain and illustrated the importance in managing antibiotic resistance through One Health approach. Furthermore, this study has demonstrated the close relationship between daily environmental hygiene and antibiotic resistance in community.