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Scientific Opinion SCIENTIFIC OPINION ADOPTED: 29 April 2021 doi: 10.2903/j.efsa.2021.6651 Role played by the environment in the emergence and spread of antimicrobial resistance (AMR) through the food chain EFSA Panel on Biological Hazards (BIOHAZ), Konstantinos Koutsoumanis, Ana Allende, Avelino Alvarez-Ord onez,~ Declan Bolton, Sara Bover-Cid, Marianne Chemaly, Robert Davies, Alessandra De Cesare, Lieve Herman, Friederike Hilbert, Roland Lindqvist, Maarten Nauta, Giuseppe Ru, Marion Simmons, Panagiotis Skandamis, Elisabetta Suffredini, Hector Arguello,€ Thomas Berendonk, Lina Maria Cavaco, William Gaze, Heike Schmitt, Ed Topp, Beatriz Guerra, Ernesto Liebana, Pietro Stella and Luisa Peixe Abstract The role of food-producing environments in the emergence and spread of antimicrobial resistance (AMR) in EU plant-based food production, terrestrial animals (poultry, cattle and pigs) and aquaculture was assessed. Among the various sources and transmission routes identified, fertilisers of faecal origin, irrigation and surface water for plant-based food and water for aquaculture were considered of major importance. For terrestrial animal production, potential sources consist of feed, humans, water, air/dust, soil, wildlife, rodents, arthropods and equipment. Among those, evidence was found for introduction with feed and humans, for the other sources, the importance could not be assessed. Several ARB of highest priority for public health, such as carbapenem or extended-spectrum cephalosporin and/or fluoroquinolone-resistant Enterobacterales (including Salmonella enterica), fluoroquinolone-resistant Campylobacter spp., methicillin-resistant Staphylococcus aureus and glycopeptide-resistant Enterococcus faecium and E. faecalis were identified. Among highest priority ARGs blaCTX-M, blaVIM, blaNDM, blaOXA-48- like, blaOXA-23, mcr, armA, vanA, cfr and optrA were reported. These highest priority bacteria and genes were identified in different sources, at primary and post-harvest level, particularly faeces/manure, soil and water. For all sectors, reducing the occurrence of faecal microbial contamination of fertilisers, water, feed and the production environment and minimising persistence/recycling of ARB within animal production facilities is a priority. Proper implementation of good hygiene practices, biosecurity and food safety management systems is very important. Potential AMR-specific interventions are in the early stages of development. Many data gaps relating to sources and relevance of transmission routes, diversity of ARB and ARGs, effectiveness of mitigation measures were identified. Representative epidemiological and attribution studies on AMR and its effective control in food production environments at EU level, linked to One Health and environmental initiatives, are urgently required. © 2021 European Food Safety Authority. EFSA Journal published by John Wiley and Sons Ltd on behalf of European Food Safety Authority. Keywords: antimicrobial resistance, food-producing environment, antimicrobial resistance genes, antimicrobial-resistant bacteria, animals, plants, aquaculture, environment, food Requestor: EFSA Question number: EFSA-Q-2019-00343 Correspondence: [email protected] www.efsa.europa.eu/efsajournal EFSA Journal 2021;19(6):6651 AMR in food-producing environment Panel members: Konstantinos Koutsoumanis, Ana Allende, Avelino Alvarez-Ord onez,~ Declan Bolton, Sara Bover-Cid, Marianne Chemaly, Robert Davies, Alessandra De Cesare, Lieve Herman, Friederike Hilbert, Roland Lindqvist, Maarten Nauta, Luisa Peixe, Giuseppe Ru, Marion Simmons, Panagiotis Skandamis and Elisabetta Suffredini. Declarations of interest: The declarations of interest of all scientific experts active in EFSA’s work are available at https://ess.efsa.europa.eu/doi/doiweb/doisearch. Acknowledgements: The Panel wishes to thank the following observers who followed the development of the scientific output for the support received: European Medicines Agency, specially Ricardo Carapeto (member of EMA CVMP), Michael Empl, Zoltan Kunsagi and Ana Vidal; European Environment Agency, Caroline Whalley; European Centre for Disease Prevention and Control, Dominique Monnet; and the European Commission. The Panel also wishes to thank EFSA staff Karoline Nørstrud for her contributions to the drafting of this scientific output, Eleonora Sarno, Pierre-Alexandre Beloeil and Gina Cioacata. Suggested citation: EFSA BIOHAZ Panel (EFSA Panel on Biological Hazards), Koutsoumanis K, Allende A, Alvarez-Ord onez~ A, Bolton D, Bover-Cid S, Chemaly M, Davies R, De Cesare A, Herman L, Hilbert F, Lindqvist R, Nauta M, Ru G, Simmons M, Skandamis P, Suffredini E, Arguello€ H, Berendonk T, Cavaco LM, Gaze W, Schmitt H, Topp E, Guerra B, Liebana E, Stella P and Peixe L, 2021. Scientific Opinion on the role played by the environment in the emergence and spread of antimicrobial resistance (AMR) through the food chain. EFSA Journal 2021;19(6):6651, 188 pp. https://doi.org/ 10.2903/j.efsa.2021.6651 ISSN: 1831-4732 © 2021 European Food Safety Authority. EFSA Journal published by John Wiley and Sons Ltd on behalf of European Food Safety Authority. This is an open access article under the terms of the Creative Commons Attribution-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited and no modifications or adaptations are made. The EFSA Journal is a publication of the European Food Safety Authority, a European agency funded by the European Union. www.efsa.europa.eu/efsajournal 2 EFSA Journal 2021;19(6):6651 AMR in food-producing environment Summary The European Food Safety authority (EFSA) asked the Panel on Biological Hazards (BIOHAZ) to provide a scientific opinion on the role played by the environment in the emergence and spread of antimicrobial resistance (AMR) through the food chain. In particular, the Panel was asked: 1) to identify the main environmental sources and transmission routes leading to the contamination of foods of animal and non-animal origin with antimicrobial-resistant bacteria (ARB) and/or resistance determinants/genes (ARGs) (ToR1); 2) to identify the ARB and/or ARGs of highest priority for public health contaminating food through the environmental routes identified, as well as the main risk factors influencing their occurrence and persistence in food-producing environments and food (ToR2); 3) to review and, if possible, assess the impact of strategies and options to mitigate the risk of emergence, spread and food-borne transmission of those ARB (ToR3); 4) to identify data gaps influencing the assessment of food chain-related AMR risks posed by the environment and provide recommendations to inform future EU research priorities on this topic (ToR4). For the purpose of this mandate, food-producing environments were defined as environments where food of animal or non-animal origin is produced or processed, at both preharvest (primary production) and post-harvest level (processing: e.g. slaughterhouses, processing plants). Three food sectors were considered: plant-based food production (fruits, vegetables and other crops), terrestrial animal production (poultry, cattle and pigs) and aquaculture (finfish, shellfish). To address the mandate, a qualitative assessment was undertaken based on information from international reports, European Legislation, scientific literature (focusing primarily on European data for sources and occurrence of specific ARB/ARGs) and expert knowledge. Uncertainty was addressed in a qualitative manner following EFSA guidance. Food production sector maps, representing the sources of AMR and pathways for AMR dissemination in the different primary production and processing steps, were developed. ARB and ARGs of highest priority for public health in food-producing environments were defined based on international guidance documents and a consideration of the public health burden. Food-producing sectors are linked with human sources and animal and environmental sources of AMR (ARB and ARGs) in a cyclical manner. These ARB and ARGs (as well as substances with antimicrobial activity) are introduced to animal- and plant-based food production environments, mostly through faecal waste (human and animal). Most of the sources identified also play a role as transmission routes. Fertilisers of faecal origin (e.g. manure), irrigation and surface water were identified as transmission routes of faecal ARB/ARGs of animal and human origin for plant-based food. Potential sources for this sector include soil, dust, farm animals, wildlife, arthropods, workers, equipment and process water. For terrestrial animals, feed, farm workers, air/dust, rodents, equipment and visitors, were identified as sources. Pastures, soil, surface water, drinking water, air, dust, wildlife or other domestic animal species are other potential sources of higher relevance for animals kept outdoor as compared to closed facilities. For aquaculture, water, sediments and feed were identified as sources. Wildlife, workers, ice and equipment were considered potential sources. Based on expert knowledge, fertilisers of faecal origin (e.g. manure), irrigation and surface water are major sources and transmission routes of contamination for plant-based food. For terrestrial animals, the published evidence did not allow the importance of most of the sources identified to be determined, although, limited circumstantial evidence points to feed and, to a lesser extent, humans, as important sources/transmission routes. For aquaculture, water is the main transmission route. Resistance to last resort
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