Induction of Antimicrobial Resistance in Escherichia coli and Non-Typhoidal Salmonella Strains after Adaptation to Disinfectant Commonly Used on Farms in Vietnam.

Nguyen Nhung,Stephen Baker,Guy Thwaites,Cao Thuy,Ngo Hoa,Nguyen Trung,James Campbell,Juan Carrique-Mas

doi:10.3390/antibiotics4040480

Abstract

In Vietnam, commercial disinfectants containing quaternary ammonium compounds (QACs) are commonly used in pig and poultry farms to maintain hygiene during production. We hypothesized that sustained exposure to sub-bactericidal concentrations of QAC-based disinfectants may result in increased levels of antimicrobial resistance (AMR) among Enterobacteriacea due to the increase of efflux pump expression. To test this hypothesis we exposed six antimicrobial-susceptible Escherichia coli (E. coli) and six antimicrobial-susceptible non-typhoidal Salmonella (NTS) isolates to increasing concentrations of a commonly used commercial disinfectant containing a mix of benzalkonium chloride and glutaraldehyde. Over the 12-day experiment, strains exhibited a significant change in their minimum inhibitory concentration (MIC) of the disinfectant product (mean increase of 31% (SD ± 40)) (p = 0.02, paired Wilcoxon test). Increases in MIC for the disinfectant product were strongly correlated with increases in MIC (or decreases in inhibition zone) for all antimicrobials (Pearson’s correlation coefficient 0.71–0.83, all p < 0.01). The greatest increases in MIC (or decreases in inhibition zone) were observed for ampicillin, tetracycline, ciprofloxacin, and chloramphenicol, and the smallest for gentamicin, trimethoprim/sulphamethoxazole. The treatment of 155 representative E. coli isolates from farmed and wild animals in the Mekong Delta (Vietnam) with phenyl-arginine beta-naphthylamide (PAβN), a generic efflux pump inhibitor, resulted in reductions in the prevalence of AMR ranging from 0.7% to 3.3% in these organisms, indicating a small contribution of efflux pumps on the observed prevalence of AMR on farms. These results suggest that the mass usage of commercial disinfectants, many of which contain QACs, is potentially a contributing factor on the generation and maintenance of AMR in animal production in Vietnam.

Highlights

Antimicrobial resistance (AMR) is a major global health threat recognized by the research community as well as by international agencies concerned with human and veterinary medicine [1,2].The intensity of antimicrobial use is firmly established as one of the key drivers for the development of antimicrobial resistance (AMR) both in human and veterinary medicine [3,4].Disinfectants are substances applied to kill microorganisms on inanimate objects
The investigated product is widely used on food animal farms in southern Vietnam, the chosen strains originated from healthy human individuals since we expected such isolates have a low chance of previous exposure to disinfectants commonly used on pig and poultry farms
4 μg/mL to 256 μg/mL, i.e., a +6300% increase [18]. Such experiments were carried out using pure benzalkonium chloride; in contrast, in our study we investigated a commercial product that contains a mixture of benzalkonium chloride and glutaraldehyde, and adaptation to either of the two components could theoretically result in an increased minimum inhibitory concentration (MIC) for the commercial product

Summary

Introduction

Antimicrobial resistance (AMR) is a major global health threat recognized by the research community as well as by international agencies concerned with human and veterinary medicine [1,2].The intensity of antimicrobial use is firmly established as one of the key drivers for the development of AMR both in human and veterinary medicine [3,4].Disinfectants are substances applied to kill microorganisms on inanimate objects. Antimicrobial resistance (AMR) is a major global health threat recognized by the research community as well as by international agencies concerned with human and veterinary medicine [1,2]. The intensity of antimicrobial use is firmly established as one of the key drivers for the development of AMR both in human and veterinary medicine [3,4]. The use of disinfectants at the end of the food animal production cycle (i.e., terminal cleaning and disinfection) is a crucial procedure for limiting the transmission of infections between animals sequentially housed in the same buildings, contributing to overall flock/herd health and productivity [6]. There has been mounting evidence that exposure to certain disinfectant agents may induce reduced susceptibility and cross-resistance with antimicrobial agents [7,8,9]

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Discussion

Conclusion