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Review of Airborne Antimicrobial Resistance

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Review of Airborne Antimicrobial Resistance Title of report (limited to 10 words) Report – XXXXXX/R (project code number) Review of airborne antimicrobial resistance We are the Environment Agency. We protect and improve the environment. Acting to reduce the impacts of a changing climate on people and wildlife is at the heart of everything we do. We reduce the risks to people, properties and businesses from flooding and coastal erosion. We protect and improve the quality of water, making sure there is enough for people, businesses, agriculture and the environment. Our work helps to ensure people can enjoy the water environment through angling and navigation. We look after land quality, promote sustainable land management and help protect and enhance wildlife habitats. And we work closely with businesses to help them comply with environmental regulations. We can’t do this alone. We work with government, local councils, businesses, civil society groups and communities to make our environment a better place for people and wildlife. Published by: Author(s): Environment Agency, Horizon House, Deanery Road, Matt Jones Bristol, BS1 5AH Dissemination status: http://www.gov.uk/government/organisations/environme Publicly available nt-agency Environment Agency’s Project Manager: ISBN: 978-1-84911-424-0 Alwyn Hart, Research, Analysis and Evaluation © Environment Agency – February 2020 All rights reserved. This document may be reproduced with prior permission of the Environment Agency. Further copies of this report are available from our publications catalogue: http://www.gov.uk/government/publications For our National Customer Contact Centre: T: 03708 506506 Email: [email protected] ii Review of airborne antimicrobial resistance Evidence at the Environment Agency Scientific research and analysis underpins everything the Environment Agency does. It helps us to understand and manage the environment effectively. Our own experts work with leading scientific organisations, universities and other parts of the Defra group to bring the best knowledge to bear on the environmental problems that we face now and in the future. Our scientific work is published as summaries and reports, freely available to all. This report is the result of research commissioned by the Environment Agency’s Research, Analysis and Evaluation group. You can find out more about our current science programmes at https://www.gov.uk/government/organisations/environment-agency/about/research If you have any comments or questions about this report or the Environment Agency’s other scientific work, please contact [email protected]. Professor Doug Wilson Director, Research, Analysis and Evaluation Review of airborne antimicrobial resistance iii Executive summary The spread of antimicrobial-resistant microorganisms and their genes in the environment is of increasing concern, with legislators seeking evidence to advise the regulation of environmental pathways for the spread of resistance. However, most of this evidence has been gathered from aquatic (for example, freshwaters, seawater) and terrestrial (for example, soil) systems, with little concerted effort to establish a knowledge base for airborne antimicrobial resistance. This report seeks to summarise the available literature on airborne antimicrobial resistance, with a view to establishing what is known, what hypotheses are emerging from this, and what knowledge gaps there are in current scientific work on airborne antimicrobial resistance. Based on a literature review, this project sought to identify: current coverage of the issue types of organism studied types of antimicrobial studied field and laboratory methods used environments studied This information was used to characterise the types and levels of multi-antimicrobial resistance in the different environments that have so far been studied. As of August 2018, the literature was dominated by studies focusing exclusively on airborne antibiotic resistance in bacteria. Most of these studies are of Staphylococci (31 out of 88 studies) and Enterobacteriacae (24 out of 88 studies). Very few studies looked at fungi (9 out of 88 studies). No studies or data on airborne antimicrobial resistance for the UK were found. Most studies were culture-dependent (that is, they used a laboratory culture medium in agar plates and culturing with antibiotics to measure antimicrobial resistance; 53 out of 88 studies), not culture-independent (that is, using polymerase chain reaction (PCR), quantitative PCR or metagenomics to measure antimicrobial resistance). Despite biases towards studying certain classes of antibiotics and differences in the antibiotics for which resistance was tested between studies, it was clear that different environments were associated with different types of levels of antibiotic resistance. For example, tetracycline resistance appeared to be more prevalent in agriculturally associated air. The literature review suggested that: different environments are associated with different types and levels of airborne antimicrobial resistance the 2 main conditions driving airborne antimicrobial resistance are: - the presence of large accumulations of antimicrobial-resistant organism- laden faecal matter iv Review of airborne antimicrobial resistance - physical processes for the aerosolisation of this faecal matter (for example, animal movement, aeration in WWTPs) It is hypothesised that livestock-associated environments in the UK will be major hotspots of airborne antimicrobial resistance. However, specific conclusions about which types of environment (for example, CAFOs, WWTPs) are the most problematic source of airborne antimicrobial resistance for the Environment Agency and associated government bodies are difficult because no UK research on airborne antimicrobial resistance was identified by the literature search. The major knowledge gap in current research is the relative importance of airborne exposure to antimicrobial resistance. Is the air a primary route by which antimicrobial resistance spreads to humans and other vulnerable hosts (for example, crops)? How does it do so (via microorganism hosts or free-living genes?) What are the consequences of this? More epidemiological evidence is needed in this regard, as are studies on airborne antimicrobial resistance in the UK in the many neglected environments (for example, arable farming, slurry spreading areas), and fungi and other non-bacterial microorganisms. More research is recommended to close knowledge gaps and test emergent hypotheses. Also needed is a more concerted effort to report and share the results of antimicrobial susceptibility testing in a standardised way, and more careful and standardised collection and reporting of air sampling. Review of airborne antimicrobial resistance v Acknowledgements Thank you to Amanna Giles and Alwyn Hart for conceiving and supporting this project, as well as to Charlotte Hutton and Gerard Lenagan for their motivation and advice. Thank you to Jonathan Porter for his extensive feedback on the original draft. Thank you to Rob Kinnersley and Kerry Walsh for scientific guidance and other help with the project and discussing its wider context, and providing feedback. Thank you to Alfredo Sanchez-Tojar for his extensive advice on systematic review and meta-analysis. Thank you also to Sean Tyrell, Ian Colbeck, Toni Gladding, Frederic Coulon, Rob Ferguson, Corinne Whitby, Zaheer Nasir, Alex Dumbrell, Andrew Singer, Jennifer Shelton, George Leahy, Tracy Barker and Chris Lloyd for feedback on parts of the report and/or insightful meetings. vi Review of airborne antimicrobial resistance Contents 1 Introduction and methods 1 1.1 Background 1 1.2 Project aims 1 1.3 Methods 2 1.4 Structure of the report 6 2 Results 7 2.1 General trends across all studies 7 2.2 Quantitative comparison 8 2.3 Concentrated animal feeding operations 12 2.4 Wastewater treatment plants 17 2.5 Urban areas 19 2.6 Other environments 22 2.7 Comparison across types of air 26 3 Conclusions 29 3.1 What is known 29 3.2 Emerging major hypotheses for further testing 31 3.3 Knowledge gaps 32 3.4 Recommendations for future research 37 3.5 Closing remarks 39 References 40 List of abbreviations 49 Appendix A: Data and code availability 50 Appendix B: Additional analysis to validate meta-analysis 51 List of tables and figures Figure 2.1 Forest plot comparing MAR indices between types and environmental sources of air (and studies) 28 Figure B.1 Comparison of MAR indices between different types (environments) of air 53 Figure B.2 Distance–decay relationship of number of bacteria isolated across different studies 54 Review of airborne antimicrobial resistance vii 1 Introduction and methods 1.1 Background Antimicrobials – including antibacterial, antifungal and antiviral agents – are an essential component of modern life. For the first time in human history, we are more likely to die of chronic, age-related disease than infection (Surette and Wright 2017). However, there is a growing risk that such gains will be reversed by the ever-growing problem of antimicrobial resistance. Recent predictions indicate that, without policy and regulatory changes, more people will die from infections of multi-drug resistant bacteria than cancer by 2050 (O’Neill 2016). The role of the Environment Agency and its partners in invoking such a policy change may not seem immediately obvious, as antibiotic resistance has conventionally been thought of as a public health issue. However, given that the outdoor environment represents one of the largest
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