Unraveling the Role of Metals and Organic Acids in Bacterial Antimicrobial Resistance in the Food Chain

Abstract

Antimicrobial resistance (AMR) has a significant impact on human, animal, and environmental health, being spread in diverse settings. Antibiotic misuse and overuse in the food chain are widely recognized as primary drivers of antibiotic-resistant bacteria. However, other antimicrobials, such as metals and organic acids, commonly present in agri-food environments (e.g., in feed, biocides, or as long-term pollutants), may also contribute to this global public health problem, although this remains a debatable topic owing to limited data. This review aims to provide insights into the current role of metals (i.e., copper, arsenic, and mercury) and organic acids in the emergence and spread of AMR in the food chain. Based on a thorough literature review, this study adopts a unique integrative approach, analyzing in detail the known antimicrobial mechanisms of metals and organic acids, as well as the molecular adaptive tolerance strategies developed by diverse bacteria to overcome their action. Additionally, the interplay between the tolerance to metals or organic acids and AMR is explored, with particular focus on co-selection events. Through a comprehensive analysis, this review highlights potential silent drivers of AMR within the food chain and the need for further research at molecular and epidemiological levels across different food contexts worldwide.

DecodingKlebsiella pneumoniaein Poultry Chain: Unveiling Genetic Landscape, Antibiotic Resistance, and Biocide Tolerance in Non-Clinical Reservoirs

“…Metals and biocides are used in food-animal production for various purposes, including as feed additives, growth promoters, antiseptics, and disinfectants, to decrease the dependence on antibiotics [(EMA Committee for Medicinal Products for Veterinary Use (CVMP) and EFSA Panel on Biological Hazards (BIOHAZ) et al, 2017; Rebelo et al, 2023)]. Copper is one of the metals commonly added to chicken feed.…”

Decoding Klebsiella pneumoniae in poultry chain: unveiling genetic landscape, antibiotic resistance, and biocide tolerance in non-clinical reservoirs

“…This reliance becomes even more concerning when considering that poultry presents potential risks to human health as it can be a reservoir of zoonotic pathogens causing infectious diseases and can contribute to the spread of antimicrobial resistance (AMR) within the food chain [ Golden et al, 2021 ; European Food Safety Authority (EFSA) and European Centre for Disease Prevention and Control (ECDC), 2023 ]. While antibiotics have traditionally been seen as the main drivers of AMR, recent restrictions on their use in food-producing animals, as well as alternative antimicrobial approaches, suggest the contribution of other compounds as selectors of antibiotic-resistant bacteria ( Rebelo et al, 2023 ).…”

“…Metals and biocides are used in food-animal production for various purposes, including as feed additives, growth promoters, antiseptics, and disinfectants, to decrease the dependence on antibiotics [ EMA Committee for Medicinal Products for Veterinary Use (CVMP) and EFSA Panel on Biological Hazards (BIOHAZ) et al, 2017 ; Rebelo et al, 2023 ]. Copper-Cu is one of the metals commonly added to chicken feed.…”

“…Genes associated with tolerance to metals and QACs often share the same genetic contexts with antibiotic-resistance genes ( Slifierz et al, 2015 ; Li et al, 2022 ; Pereira et al, 2023 ). Thus, the use of copper-supplemented feed and QAC-based biocides could contribute to co-selection effects ( Webber et al, 2015 ; Kampf, 2018 ; Rebelo et al, 2023 ).…”

“…Current intensive chicken production involves large-scale operations that span breeding and hatching to rearing, processing, and distribution. However, the impact of diverse antimicrobial strategies used throughout farm to fork on the spread of AMR remains underexplored [ EMA Committee for Medicinal Products for Veterinary Use (CVMP) and EFSA Panel on Biological Hazards (BIOHAZ) et al, 2017 ; Rebelo et al, 2023 ]. To effectively address AMR, a One Health approach – which emphasizes coordinated efforts across the domains of animals, humans, and the environment – is essential.…”