Role played by the environment in the emergence and spread of antimicrobial resistance (AMR) through the food chain
EFSA Panel on Biological Hazards (BIOHAZ)
(2021) EFSA Journal, volume 19, issue 6, pp. 1 - 188
(Article)
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
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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 bla CTX -M, bla VIM, bla NDM, bla OXA -48-like, bla OXA -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.
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Keywords: animals, antimicrobial resistance, antimicrobial resistance genes, antimicrobial-resistant bacteria, aquaculture, environment, food, food-producing environment, plants, Parasitology, Food Science, Microbiology, Animal Science and Zoology, veterinary (miscalleneous), Plant Science
ISSN: 1831-4732
Publisher: Wiley-Blackwell Publishing Ltd
Note: Funding Information: 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 N?rstrud for her contributions to the drafting of this scientific output, Eleonora Sarno, Pierre-Alexandre Beloeil and Gina Cioacata. Funding Information: The role of natural and farm environments in the emergence, selection, dissemination and ultimately transmission of AMR has received much less attention than selection and transmission within and between humans and animals and most reports and policy documents focus on the clinical perspective. However, over the last decade there has been an increased emphasis on the environment with the 2015 World Health Organization (WHO) AMR Action Plan (WHO, 2015 ) highlighting concerns around the impact of antimicrobials in the environment. Specific questions include how AMR circulates through the environment and how resistant organisms can be transmitted to humans through food and the environment. Environmental aspects received great attention also in the European Union (EU) One Health Action Plan Against Antimicrobial Resistance 7 published in 2017, with ‘environment’ being mentioned over 30 times, acknowledging the environment as an important contributor to the development and spread of AMR in humans and animals. In 2017 the United Nations (UN) published a report on Emerging Issues of Environmental Concern, highlighting the environmental dimension of AMR as one of the most pressing environmental issues of our time (UNEP, 2017 ). This report gives details of the phenomena that drive selection and dissemination of AMR in the environment, but without providing details in relation to food‐borne exposure and transmission. A commitment to help tackle AMR was agreed at the 3rd United Nations Environment Assembly in Nairobi in 2017 (UNEA 3) as part of a resolution on environment and health (UNEP, 2018 ). In the same year the International AMR Forum was established supported by the Wellcome Trust in the UK, UK Science and Innovation, the US Centers for Disease Control and Prevention (CDC) and the Canadian government (Wellcome Trust, 2018a ). A working group of approximately 40 specialists produced a scientific white paper entitled ‘Initiatives for Addressing Antimicrobial Resistance in the Environment ‐ Current Situation and Challenges’ (Wellcome Trust, 2018b ) and a symposium was held in Vancouver in April 2018. The white paper, published in 2018, focused on areas relevant to this report including human and animal contamination of the environment, and antimicrobials used as crop pesticides. The authors concluded that human and animal waste introduces ARB and antimicrobials into the environment, where selection for AMR may occur with some evidence of onwards transmission to humans. In 2019 the Interagency Coordination Group on AMR (IACG) published their final report which was presented to the UN Director General (WHO, 2019a ). The report acknowledges the role of the environment and the risks to food and feed production: ‘although evidence remains limited, concerns are also growing about the impact of AMR on the environment and natural ecosystems due to overuse and discharge of antimicrobials and resistant micro‐organisms in manure and waste from health care facilities and pharmaceutical manufacturing, commercial livestock and plant production, and fish and seafood farming, a problem that may be fuelled by changes in the world's climate’. In March 2019, as one of the actions in the Action Plan, the European Commission adopted the European Union Strategic Approach to Pharmaceuticals in the Environment (PiE), 8 which focuses on actions to address the environmental implications of all phases of the lifecycle of (both human and veterinary) pharmaceuticals, from design and production through use to disposal. It includes some quite specific actions on AMR and identifies ‘the links between the presence of antimicrobials in the environment and the development and spread of antimicrobial resistance’ as a knowledge gap. A progress overview of the implementation was published in 2020. 9 The EU Strategic Approach to Pharmaceuticals acknowledges that whilst there is currently no clear link established between pharmaceuticals present in the environment and direct impacts on human health, the presence of antimicrobials (antibiotics and antifungals) may play a role in accelerating the development, maintenance and spread of resistant bacteria and fungi. The Strategic Approach also notes that there is limited monitoring of ‘hotspot’ locations, such as those affected by hospital effluents, and that even less is known about antimicrobial concentrations and AMR in soils. The latter may be a specific concern for food‐producing environments where antimicrobials enter soils in livestock manures or through direct application to crops in the case of fungicides. The Organisation for Economic Co‐operation and Development (OECD) report on pharmaceuticals and freshwater environments recommended that environmental risk assessment includes the risk potential of developing AMR (OECD, 2019 ). Also, the European Medicines Agency (EMA) has issued several considerations related to the approach to be followed to minimise environmental contamination with ARB and ARGs and to the assessment of the risk of antimicrobials for the environment (EMA/CVMP, 2021 ). Publisher Copyright: © 2021 European Food Safety Authority. EFSA Journal published by John Wiley and Sons Ltd on behalf of European Food Safety Authority.
(Non peer reviewed)
