Abstract
BackgroundThe role of the crop environment as a conduit for antimicrobial resistance (AMR) through soil, water, and plants has received less attention than other sectors. Food crops may provide a link between the agro-environmental reservoir of AMR and acquisition by humans, adding to existing food safety hazards associated with microbial contamination of food crops.ObjectivesThe objectives of this review were: (1) to use a systematic methodology to characterize AMR in food crop value chains globally, and (2) to identify knowledge gaps in understanding exposure risks to humans.MethodsFour bibliographic databases were searched using synonyms of AMR in food crop value chains. Following two-stage screening, phenotypic results were extracted and categorized into primary and secondary combinations of acquired resistance in microbes of concern based on established prioritization. Occurrence of these pathogen-AMR phenotype combinations were summarized by sample group, value chain stage, and world region. Sub-analyses on antimicrobial resistance genes (ARG) focused on extended-spectrum beta-lactamase and tetracycline resistance genes.ResultsScreening of 4,455 citations yielded 196 studies originating from 49 countries, predominantly in Asia (89 studies) and Africa (38). Observations of pathogen-phenotype combinations of interest were reported in a subset of 133 studies (68%). Primary combinations, which include resistance to antimicrobials of critical importance to human medicine varied from 3% (carbapenem resistance) to 13% (fluoroquinolones), whereas secondary combinations, which include resistance to antimicrobials also used in agriculture ranged from 14% (aminoglycoside resistance) to 20% (aminopenicillins). Salad crops, vegetables, and culinary herbs were the most sampled crops with almost twice as many studies testing post-harvest samples. Sub-analysis of ARG found similar patterns corresponding to phenotypic results.DiscussionThese results suggest that acquired AMR in opportunistic and obligate human pathogens is disseminated throughout food crop value chains in multiple world regions. However, few longitudinal studies exist and substantial heterogeneity in sampling methods currently limit quantification of exposure risks to consumers. This review highlights the need to include agriculturally-derived AMR in monitoring food safety risks from plant-based foods, and the challenges facing its surveillance.
Highlights
Recognition of waning antimicrobial efficacy and the rise of untreatable bacterial infections in hospitals has driven the issue of antimicrobial resistance (AMR) to the forefront of the global health agenda
An a priori protocol was written, setting out the objectives and methods of the review using the “Population, Concept, and Context” framework (Peters et al, 2015) to identify four initial research questions: (1) In pre- and post-harvest production stages, what is the current evidence that Antimicrobial resistant bacteria (ARB) and antimicrobial resistance genes (ARG) contamination in human opportunistic or obligate pathogenic microbes and selected phytopathogens occurs in food crops?; (2) What is the evidence that contamination of food crops with antimicrobial residues leads to emergence of ARB important to human health?; (3) What is currently understood about transmission dynamics of ARBand ARG-contaminated food crops to consumers?; (4) What is known about the human health risks of AMR in the food crop value chain with particular regard to low- and middle-income countries (LMICs)?
Reasons for exclusion of 70 studies were as follows: six studies represented an opinion or narrative review; nine studies sampled plant-foods that were cooked or fermented; seven studies focused on non-eligible animal or environmental samples; 25 studies investigated non-AMR aspects of microbial contamination such as virulence traits or focused on microbe species not included in this review, and 23 studies reported AMR results of food crop samples aggregated with non-crop samples, such as meat or wildlife feces
Summary
Recognition of waning antimicrobial efficacy and the rise of untreatable bacterial infections in hospitals has driven the issue of antimicrobial resistance (AMR) to the forefront of the global health agenda. Initial efforts to address antimicrobial misuse and overuse have prioritized human health care systems and livestock production, other sources of AMR, such as discharges from wastewater treatment facilities, generate a reservoir of antimicrobial resistant microbes in the environment that may be pertinent to human health (O’Neill, 2016; Singer et al, 2016). Particular attention has been paid to food animal production due to large volume use of antimicrobials and the risk of transmission of zoonotic pathogens to humans through animal-source foods. Recent modeling suggests reductions in antimicrobial use in animal agriculture may have a limited impact on decreasing AMR infections in human populations (Van Bunnik and Woolhouse, 2017; Van Boeckel et al, 2019; Booton et al, 2021). Food crops may provide a link between the agro-environmental reservoir of AMR and acquisition by humans, adding to existing food safety hazards associated with microbial contamination of food crops
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