PerspectivesPerspectives

The : a critical missing link in national action plans on antimicrobial resistance Graziella Iossaa & Piran CL Whiteb

Antimicrobial resistance, that is, the environment in contributing to antimi- antimicrobial use in livestock and the ability of a microorganism to stop an crobial resistance, we call for greater in- selection of resistance in is antimicrobial from working against it, is tegration of the natural environment in difficult to establish, there is evidence one of the most important global existing and new national action plans, of an association.8 Resistant bacteria challenges. Antimicrobial resistance is so that we can maximize our chances of of animal origin can be transmitted to projected to become the leading cause of finding holistic and sustainable solutions humans directly via food or indirectly death worldwide, claiming an estimated to this global health threat. via the natural environment. More- 10 million a year by 2050, primarily over, wastewater treatment plants, ma- in low- and middle-income countries.1 Resistance in the nure from farm animals and spill-over In 2015, the World Health Assembly ad- from the pharmaceutical production opted a global action plan on antimicro- environment industry contribute to an environmen- bial resistance underpinned by the One tal reservoir of resistance.7 The natural Antimicrobial resistance develops Health approach.2 One Health seeks to environment should therefore be a key in, and is maintained and transmit- improve health and well-being through consideration in understanding and ted across humans, animals and the the integrated management of disease developing strategies to control anti- natural environment. Resistance is risks at the interface between humans, microbial resistance, as acknowledged an ancient and naturally occurring animals and the natural environment. through the One Health approach.9 phenomenon, but anthropogenic an- Efforts are based on closer collabora- tibiotic use since the 1930s has been tion among individual disciplines and National action plans linked to the increasing occurrence a cross-sectoral approach to research, of antimicrobial-resistant micro- One of the key guiding principles surveillance and response.3 The natural , particularly bacteria.5,6 of the national plans is to use a One or here in- The natural environment presents a Health approach and multisectoral cludes all living (biotic) and non-living transmission route and a reservoir for coordination. This principle gives the (abiotic) factors affecting the survival of resistant microorganisms and plays a various collaborating organizations all organisms, including humans, at the significant role in the development of, equal status and emphasizes a sense individual, , community or and response to, antimicrobial resis- of ownership of the plan.4 As of May ecosystem level. In this context, an eco- tance.7 Antimicrobial use in the live- 2018, 56 Member States (29.0%) out system refers to a community of plants, stock industry is driving the selection of 194 have published national action animals and microorganisms that live, of resistant bacteria in farm animals, plans, of which 21 have been published feed, reproduce and interact within the and while the causal link between since 2015. same area or environment. Antimicro- bial resistance connects health to the health of ecosystems and the natural Box 1. The national action plans on antimicrobial resistance considered in our analysis, environment. With the global action by WHO Region plan on antimicrobial resistance, Mem- African Region ber States agreed to develop individual United Republic of Tanzania (2017) national action plans on antimicrobial resistance by May 2017.2,4 Here we pres- Region of Americas ent an analysis of the extent to which the Barbados (2017) and Canada (2017) national action plans developed after Eastern Mediterranean Region 2015 have been successful in integrating Oman (2017) the natural environment within a One European Region Health approach. We found that the Denmark (2017) and Sweden (2016) action plans feature human and animal South-East Asia Region health prominently, but that most do Bangladesh (2017), India (2017), Indonesia (2017), Maldives (2017), Nepal (2016), Sri Lanka not specifically incorporate the natural (2017), Thailand (2016) and Timor-Leste (2017) environment, and hence fall short of Western Pacific Region achieving a genuine One Health ap- China (2016), Japan (2016), Mongolia (2017) and New Zealand (2017) proach. Given the key role of the natural a School of Sciences, Joseph Banks Laboratories, University of Lincoln, Lincoln LN6 7TS, England. b Department of Environment and Geography, University of York, York, England. Correspondence to Graziella Iossa (email: [email protected]). (Submitted: 21 February 2018 – Revised version received: 13 June 2018 – Accepted: 2 July 2018 – Published online: 10 October 2018 )

858 Bull World Health Organ 2018;96:858–860 | doi: http://dx.doi.org/10.2471/BLT.18.210898 Perspectives Graziella Iossa & Piran CL White National action plans on antimicrobial resistance

We analysed the 18 national action plans published in English between Fig. 1. Content analysis of national action plans on antimicrobial resistance published 2015 and October 2017 (Box 1) to de- after 2015 termine the extent to which the plans integrated the natural environment 30.0

within a One Health approach. We used e content analysis10 by constructing a set 25.0 of categories: (i) One Health (inclusion of the term itself, related terms or no ref- 20.0 erence); (ii) human-animal-agriculture y of occurrenc 15.0 (agriculture appeared to be used as synonymous for natural environment; 10.0 inclusion of these keywords was linked to One Health, but with no specific men- erage frequenc 5.0 tion of One Health, related terms or no Av reference); (iii) environment (inclusion 0.0 of the term itself, related terms or no ref- African Region Region of Eastern European South-East Western Pacific Americas Mediterranean Region Asia Region Region erence); and (iv) human-animal health Region (inclusion of the term itself, related One health Human-animal health Human-animal agriculture terms or no reference). The categories Environment Multisectoral also identified the broader context in which those terms were used: in the Note: Content analysis (average frequency of occurrence) of the search terms around One Health, introduction or problem definition of human-animal health, human-animal-agriculture, environment and multisectoral engagement for 18 antimicrobial resistance; in the plans’ national action plans on antimicrobial resistance published after 2015. strategic objectives; in the implementa- tion; and/or in the evaluation process. 14.1 in the text of the action plans. Although most plans have been As we were particularly interested in This was followed by human-animal- drafted by multisectoral coordination multisectoral approaches to tackling an- agriculture, which occurred an aver- teams who acknowledge that One Health timicrobial resistance, we also searched age of 5.1 times, and the environment, guides their approach, the predominance for evidence of the presence or absence which occurred an average of 2.6 times. of topics around human-animal health of such approaches in the national ac- No plans included the terms , and the scarcity of topics around the nat- tion plans. ecologist or ecosystem. Ecosystem ural environment suggests that there are Ten out of 18 action plans followed was mentioned in five plans but the more representatives of human-animal the World Health Organization (WHO) context, for instance “clinical settings health in the coordination teams. The guidelines and identified five objectives represent an ecosystem of high antimi- reason for this could be twofold. First, in line with the global action plan on crobial usage” or “the entire ecosystem we have an increasing understanding of antimicrobial resistance: (i) improve of antimicrobial resistance,” suggests resistance mechanisms in human-animal awareness and understanding of anti- a non-ecological meaning. The term systems, alongside better developed microbial resistance through effective One Health occurred an average of 1.3 surveillance methods, and longer-term communication, education and train- times in the plans and multisectoral collaborations among key agencies, such ing; (ii) strengthen the knowledge and coordination occurred an average of as WHO, the Food and Agriculture Or- evidence base through surveillance and 3.0 times (Fig. 1). Across all plans, with ganization of the United Nations (FAO) research; (iii) reduce the incidence of regards to the context, a One Health and the World Organisation for Animal through effective sanitation, approach was occasionally referenced Health (OIE).7,9 Second, the recent his- hygiene and infection prevention mea- in the introductory section and in the tory of the One Health approach has sures; (iv) optimize the use of antimi- definition of antimicrobial resistance as stemmed from the need to confront crobial medicines in human and animal a challenge. Twelve of the 18 plans also emerging infectious diseases outbreaks. health; and (v) develop the economic mentioned a One Health approach in The development of the One Health case for sustainable investment that takes their strategic objectives. However, this approach has therefore so far has been account of the needs of all countries, and was mainly restricted to the need for an primarily embraced by veterinarians and, increase investment in new medicines, integrated surveillance system, with the to a certain extent, physicians.3 Currently, diagnostic tools, vaccines and other in- acknowledgement of a current focus on two of greatest challenges to ensure terventions.2,4 The eight remaining action human and animal health and an inten- that One Health becomes embedded plans identified further country-specific tion to integrate the natural environ- in governance are ensuring that greater objectives. Encouragingly, a further ment in the future. Reference to a One emphasis is placed on the key role of the objective was to establish governance Health approach was related mainly natural environment and ecosystems in and a multisectoral approach to combat to multisectoral collaboration and to contributing to antimicrobial resistance antimicrobial resistance. a whole-of-society engagement. In risk and management,11 and working The most frequent term across contrast, there was frequent reference to break down disciplinary and policy all action plans (Fig. 1) was that of to human-animal-agriculture terms in silos and embrace the changes needed to human-animal health, which had an the strategic objectives, but these were implement a genuinely interdisciplinary average frequency of occurrence of not specifically linked to One Health. and cross-sectoral approach.12

Bull World Health Organ 2018;96:858–860| doi: http://dx.doi.org/10.2471/BLT.18.210898 859 Perspectives National action plans on antimicrobial resistance Graziella Iossa & Piran CL White

Concluding observations multisectoral committees and, in some resistance; and the role of co-selective cases, governance. Yet, while human factors such as biocides and metals. Antimicrobial resistance is a complex and animal health feature prominently, Without the more specific integration multisectoral challenge. Some progress the natural environment has yet to be of the natural environment into national is being made towards embedding a fully integrated into these plans. Since action plans and future strategies, we One Health approach in national action the natural environment is a key source risk jeopardizing many of our efforts plans on antimicrobial resistance. For and driver of antimicrobial resistance, to tackle the increasing threat posed by example, the national plan of Sri Lanka as highlighted by the WHO/OIE/FAO antimicrobial resistance.7 ■ provides an example of a cross-sectoral Tripartite and by the global action plan approach including expertise from rural on antimicrobial resistance,2 this is an Acknowledgments economy, fisheries, aquatic sciences, important omission. More research on We thank Hilary Graham. veterinarians and , and the ecology of antimicrobial resistance the national plan of India includes an in the natural environment is needed, for Funding: This project was funded under a objective on reducing the environmen- example on the population dynamics of Natural Environment Research Council tal spread of antimicrobial resistance. antimicrobial resistant and resis- Valuing Placement award to However, our analysis suggests that the tant microorganisms; the transmission Graziella Iossa. first set of national action plans have not dynamics of resistance including the been wholly successful in incorporat- role of wildlife;13 the role of biodiversity Competing interests: None declared. ing a One Health approach. The plans in enhancing or regulating resistance; have prompted the establishment of the selection pressures operating on

References 1. O’Neill J, editor. Tackling drug-resistant globally: final report and 8. Antimicrobials in agriculture and the environment: reducing unnecessary recommendations. London: The review on antimicrobial resistance; 2016. use and waste. London: The review on antimicrobial resistance; 2015. Available from: https://amr-review.org/sites/default/files/160518_Final%20 Available from: https://amr-review.org/sites/default/files/Antimicrobials%20 paper_with%20cover.pdf [cited 2018 Jun 12]. in%20agriculture%20and%20the%20environment%20-%20Reducing%20 2. Global action plan on antimicrobial resistance. Geneva: World Health unnecessary%20use%20and%20waste.pdf [cited 2018 Jun 12]. Organization; 2015. Available from: http://www.who.int/antimicrobial- 9. High-level technical meeting to address health risks at the human-animal resistance/publications/global-action-plan/en/ [cited 2018 Jun 12]. ecosystems interfaces. Mexico City, Mexico 15–17 November 2011. 3. Gibbs EPJ. The of One Health: a decade of progress and Geneva, Rome and Paris: World Health Organization, Food and Agriculture challenges for the future. Vet Rec. 2014 Jan 25;174(4):85–91. doi: http:// Organization of the United Nations and World Organisation for Animal dx.doi.org/10.1136/vr.g143 PMID: 24464377 Health; 2012‎. Available from: http://www.who.int/iris/handle/10665/78100 4. World Health Organization, Food and Agriculture Organization of the United [cited 2018 Jun 12]. Nations, World Organisation for Animal Health. Antimicrobial resistance: a 10. Bowen GA. Document analysis as a qualitative research method. Qual Res J. manual for developing national action plans, version 1. Geneva, Rome and 2009 Aug 3;9(2):27–40. doi: http://dx.doi.org/10.3316/QRJ0902027 Paris: World Health Organization, Food and Agriculture Organization of the 11. Barrett MA, Bouley TA. Need for enhanced environmental representation in United Nations and World Organisation for Animal Health; 2016. Available the implementation of One Health. EcoHealth. 2015 Jun;12(2):212–9. doi: from: http://www.who.int/iris/handle/10665/204470 [cited 2018 Jun 12]. http://dx.doi.org/10.1007/s10393-014-0964-5 PMID: 25233830 5. Martínez JL. Natural antibiotic resistance and contamination by antibiotic 12. Allen-Scott LK, Buntain B, Hatfield JM, Meisser A, Thomas CJ. Academic resistance determinants: the two ages in the evolution of resistance institutions and One health: building capacity for transdisciplinary research to antimicrobials. Front Microbiol. 2012 01 13;3:1–3. doi: http://dx.doi. approaches to address complex health issues at the animal-human- org/10.3389/fmicb.2012.00001 PMID: 22275914 ecosystem interface. Acad Med. 2015 Jul;90(7):866–71. doi: http://dx.doi. 6. Allen HK. Antibiotic resistance discovery in food-producing animals. org/10.1097/ACM.0000000000000639 PMID: 25650827 Curr Opin Microbiol. 2014 Jun;19:25–9. doi: http://dx.doi.org/10.1016/j. 13. Arnold KE, Williams NJ, Bennett M. ‘Disperse abroad in the land’: the role mib.2014.06.001 PMID: 24994584 of wildlife in the dissemination of antimicrobial resistance. Biol Lett. 2016 7. Singer AC, Shaw H, Rhodes V, Hart A. Review of antimicrobial resistance 08;12(8):20160137–8. doi: http://dx.doi.org/10.1098/rsbl.2016.0137 PMID: in the environment and its relevance to environmental regulators. 27531155 Front Microbiol. 2016 11 1;7:1728. doi: http://dx.doi.org/10.3389/ fmicb.2016.01728 PMID: 27847505

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