Global resistance to antimicrobials and their sustainable use in agriculture

Abstract

Decision-making on antimicrobial use relies on an interdependent mix of economic, behavioural, ethical, and cultural factors. In animal agriculture, antimicrobials are used to achieve: economic objectives, via optimisation of farm benefits related to sale of animal derived foodstuffs; animal welfare objectives, by ensuring good health at individual and herd levels; and public health objectives, via limiting risk of zoonotic diseases. There is evidence showing the effect of antimicrobial use in animal agriculture on antimicrobial resistance in humans.1Tang KL Caffrey NP Nóbrega DB et al.Restricting the use of antibiotics in food-producing animals and its associations with antibiotic resistance in food-producing animals and human beings: a systematic review and meta-analysis.Lancet Planet Health. 2017; 1: 316-327Summary Full Text Full Text PDF PubMed Scopus (399) Google Scholar The growing magnitude of this public health issue is encouraging the development and implementation of policies such as voluntary agreements, taxes, or permits, to decrease antimicrobial use in food-producing animals.2Van Boeckel TP Glennon EE Chen D et al.Reducing antimicrobial use in food animals.Science. 2017; 357: 1350-1352Crossref PubMed Scopus (290) Google Scholar The growing scientific literature spanning from microbiology, agricultural and environmental sciences, medicine and public health, pharmaceutical development, and ethics and law, to behaviour and economics, provides evidence for the public commitment dedicated to tackle antimicrobial resistance. Additionally, other research stresses the importance of understanding anthropological and socioeconomic factors contributing to antimicrobial resistance,3Collignon P Beggs JJ Walsh TR Gandra S Laxminarayan R Anthropological and socioeconomic factors contributing to global antimicrobial resistance: a univariate and multivariable analysis.Lancet Planet Health. 2018; 2: e398-e405Summary Full Text Full Text PDF PubMed Scopus (304) Google Scholar and pinpoints that there are gaps in the global governance of this issue.4Wernli D Jørgensen PS Harbarth S et al.Antimicrobial resistance: The complex challenge of measurement to inform policy and the public.PLoS Med. 2017; 14: 1-9Crossref Scopus (58) Google Scholar An appropriate and functional scientific framework can help to integrate different strategies to curb antimicrobial resistance. As with many unsustainable production and consumption practices, the responses to address the challenge caused by the rise of antimicrobial resistance have been formulated after the event, and scarcely consider the complexity of social-ecological systems (SES), overlooking unexpected consequences of potential policies.5Merrett GLB Bloom G Wilkinson A MacGregor H Towards the just and sustainable use of antibiotics.J Pharm Policy Pract. 2016; 9: 31Crossref PubMed Scopus (25) Google Scholar We advocate that evaluating antimicrobial use in animal agriculture as a sustainability issue under an SES perspective, in which human and nature are deeply entangled,6McGinnis MD Ostrom E Social-ecological system framework: initial changes and continuing challenges.Ecol Soc. 2014; 19: 30Crossref Scopus (741) Google Scholar can help to decompartmentalise national and international traditionally sector-based decision making, which affects stakeholders with opposing interests. We propose to determine optimal antimicrobial use in animal agriculture using a SES framework and multi-criteria decision analysis, beyond the classic cost–benefit or risk analysis perspectives. This scheme requires determining which indicators at the frontier of biological and social domains would be able to capture the social, environmental, and economic implications of a specific SES scaled to time and space. The Public Health-Economic-Environmental-Social-Political model shows a set of public health, economic, environmental, social, and policy response indicators (appendix). Public health indicators commonly used in health economics, such as value of a statistical life or quality-adjusted life year, allow all for the presentation of different outcomes of the sustainability assessment in the common metric of monetary units. A challenge is to determine the extent of these metrics as a function of antimicrobial use in agriculture. Economic indicators consist of a set of indicators capturing the viability of the farming system.7Food and Agriculture OrganizationSustainability assessment of food and agriculture systems. Guidelines version 3.0.http://www.fao.org/nr/sustainability/sustainability-assessments-safa/en/Date: 2013Date accessed: February 14, 2019Google Scholar One ideal environmental indicator consists of measuring the evolution of bacterial susceptibility over space, time, and among animal and human communities and in the environment. Given the technical feasibility and availability of such data, a set of indicators of susceptibility to be included in our model should be identified per animal production category. However, the complexity of collecting harmonised data for bacterial susceptibility trends among countries requires the addition of complementary indicators, such as antimicrobial consumption, as the most simple and easy way to monitor and compare across the food systems of countries. Social indicators are related to the wellbeing of farm communities, consumers, and animals. They integrate the dimensions of food safety, food security, and animal welfare. Policy response indicators measure qualitatively and quantitatively the implementation of national policies. They encompass the feasibility of the response, depending on the time horizon of the policy planning and on available resources. These indicators also consider the progression of the policies from the framing to implementation, and the deadlines specified (if any) to observe an improvement in the SES, because of the expected delays between enactment and the effects on the other indicators.8Hoffman SJ Outterson K What will it take to address the global threat of antibiotic resistance?.J Law Med Ethics. 2015; 43: 363-368Crossref PubMed Scopus (28) Google Scholar To achieve a sustainability assessment on antimicrobial use, combining methods developed for environmental systems analysis with tools used in public health and economics is of particular relevance. A simultaneous assessment of the associations and indicators presented here should be completed by the use of a system dynamics modelling approach. A multi-criteria objective function with trade-offs between animal and human welfare would produce a single index social welfare function to be assessed by simulation, or optimised with specified controls, such as antimicrobial use by an animal group over time. Functional relations would be estimated with data collected or generated by various techniques, including expert judgements and experiments, as well as primary and secondary data collection. This online publication has been corrected. The corrected version first appeared at thelancet.com/planetary-health on April 1, 2019 This online publication has been corrected. The corrected version first appeared at thelancet.com/planetary-health on April 1, 2019 We declare no competing interests. Download .pdf (.4 MB) Help with pdf files Supplementary appendix Correction to Lancet Planet Health 2019; 3: e109–10Lhermie G, Wernli D, Søgaard Jørgensen P, Kenkel D, Tauer LW, Gröhn YT. Global resistance to antimicrobials and their sustainable use in agriculture. Lancet Planet Health 2019; 3: e109–10. In this Comment, the appendix was not mentioned in the margin or uploaded online. Also, the author surname Wernli was misspelled as Wernlii. These corrections have been made as of April 1, 2019. Full-Text PDF Open Access