Evaluation of Antimicrobial Resistance in Enterobacteriaceae and Coliforms Isolated on Farm, Packaged and Loose Vegetables in Kentucky

Abstract

Fresh produce normally carry epiphytic microorganisms; however, it can be contaminated with pathogenic bacteria. Categorized as 'ready-to-eat', most vegetables are consumed raw, thus, may present a food safety risk. Over the last three decades, global consumption of fresh vegetables has increased considerably, and the market has expanded by more than 20%. Concomitantly, the number of outbreaks involving fresh vegetables has increased significantly. Enterobacteriaceae members are involved in most of the bacterial outbreaks linked to fresh produce. There is a worldwide concern about the increased use of antimicrobials in agriculture. Antimicrobial resistant bacteria enter the food chain from the farm, often due to the use of animal manure. In the current study, the presence of entero-coliform bacteria and their antimicrobial susceptibilities in fresh vegetables sampled from small farms to retail was evaluated. Samples of vegetables were (i) collected directly from small farms from central Kentucky (n=59) and (ii) from four supermarkets in Frankfort, KY including loose and pre-packaged produce (n=72), analyzed for isolation of entero-coliform species. Members of the Enterobacteriaceae were detected on 25% of farm and 40% of retail produce, respectively. Approximately, 61% of the packaged produce and 19.4% of the loose produce had entero-bacterial presence, respectively. Their resistance to fourteen common antimicrobials was tested using Kirby-Bauer method. Approximately, 63% of isolates from farm and 70% of isolates from retail produce displayed resistance to at least three antimicrobial agents, while 18% of the isolates from farm and 41% from retail samples displayed resistance to at least ten antimicrobial agents. We conclude that 'ready-to-eat' fresh vegetables can be a source of exposure to pathogens with multiple drug resistance (MDR), defined as resistance to at-least three antimicrobial agents, leading to greater risks in immunocompromised individuals, and may serve as reservoirs for resistance gene transfers in human colon.

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

“…This is probably due to antibiotic resistance selective pressure in the environment, caused by the misuse of antimicrobial agents for therapeutic and metaphylactic reasons. The results of this present study corroborate with the findings of [ 18 ], where 18.2% of the Enterobacteria isolated from farm produce displayed MDR to 10 antimicrobial agents.…”

“…The resistance patterns of members of Enterobacteriales in this study, especially against antimicrobial agents like ampicillin, amoxicillin/clavulanic acid, tetracycline, cefuroxime, nitrofurantoin, and chloramphenicol, is similar to the findings of [ 18 ], where a high proportion of the Enterobacteria isolated from farm produce in Kentucky conferred resistance against ampicillin and tetracyclines. These antimicrobial agents belong to the beta-lactams, tetracyclines, cephalosporins, nitrofurans, and phenicols, which are thought to be the most effective classes of antimicrobial agents used for the remediation of infections induced by Enterobacteria [ 45 ], thus posing serious risks to clinical medicine.…”

“…E. coli was recovered from various river water used for irrigation of vegetables in South Africa [ 15 , 16 ], while Salmonella enterica and Shiga toxin-producing E. coli (STEC) was recovered from freshwater sources used for irrigation [ 13 ] as well as from watersheds close to vegetable production area in the California central coast agricultural region [ 17 ]. This suggests that irrigation water and soil are important reservoirs of Enterobacteria which consequently drives their dissemination to fresh produce [ 18 ].…”

“…Several Enterobacteria found on fresh produce harbors multidrug resistance determinants, thereby exposing consumers to more safety issues [ 28 , 29 ]. Usually, antimicrobial-resistant pathogens emerging due to the indiscriminate use of antimicrobial agents in both veterinary and agricultural niches escape from the farm environments to the food chain through animal manure, soil, and irrigation water with the potential of transfer of the resistance determinants to other related and non-related species via horizontal gene transfer [ 18 , 30 , 31 , 32 ]. The spread of multidrug-resistant Enterobacteria is causing serious challenges to the management of infectious diseases due to the rapid emergence of strains capable of resisting the effects of most currently available antimicrobial agents [ 33 , 34 , 35 ].…”

High prevalence of multidrug resistant Escherichia coli isolated from fresh vegetables sold by selected formal and informal traders in the most densely populated Province of South Africa

“…Enterobacteriaceae form part of the indigenous microbiota of vegetables (Blaak, van Hoek, Veenman, Docters van Leeuwen, & Lynch, 2014). Members of this family, that is, Escherichia coli and Salmonella spp., have often been associated with foodborne bacterial outbreaks following raw fresh produce consumption (Tope, Hitter, & Patel, 2016). This includes diarrheagenic E. coli strains, including enteropathogenic (EPEC), enterotoxigenic (ETEC), enterohaemorrhagic (EHEC), enteroaggregative (EAEC), and enteroinvasive (EIEC) E. coli in foodborne disease outbreaks (Aijuka, Santiago, Girón, Nataro, & Buys, 2018; Canizalez‐Roman et al., 2019).…”