Review: ‘Disperse abroad in the land’: The role of ...
Review: ‘Disperse abroad in the land’: The role of wildlife in the dissemination of antimicrobial resistanceKathryn E. Arnold1, Nicola J. Williams2 and Malcolm Bennett3 1 Environment Department, Faculty of Sciences, University of York, Heslington, York YO10 5NG, UK2 Department of Epidemiology and Population Health, Institute of Infection and Global Health, Leahurst Campus, University of Liverpool, Neston, CH64 7TE, UK3 School of Veterinary Medicine and Science, The University of Nottingham, Sutton Bonington Campus, Sutton Bonington, Leicestershire, LE12 5RD, UKCorresponding Author: Kathryn Arnold, Environment Department, Faculty of Sciences, University of York, Heslington, York YO10 5NG, UKEmail: Kathryn.Arnold@york.ac.ukPhone: 01904 322997Running head: AMR dispersal by wildlifeKey words: antibiotic resistance, migration, disease transmission, animal dispersal, resistome, sewage treatmentAbstractAntimicrobial resistance (AMR) has been detected in the microbiota of many wildlife species, including long distance migrants. Inadequately treated wastes from humans and livestock dosed with antimicrobial drugs are often assumed to be the main sources of AMR to wildlife. While wildlife populations closely associated with human populations are more likely to harbour clinically important AMR related to that found in local humans and livestock, AMR is still common in remote wildlife populations with little direct human influence. Most reports of AMR in wildlife are survey based and/or small scale, so researchers can only speculate on possible sources and sinks of AMR or the impact of wildlife AMR on clinical resistance. This lack of quantitative data on the flow of antimicrobial resistance genes and AMR bacteria across the natural environment could reflect the numerous AMR sources and amplifiers in the populated world. Ecosystems with relatively simple and well characterised potential inputs of AMR can provide tractable, but realistic, systems for studying AMR in the natural environment. New tools, such as animal tracking technologies and high-throughput sequencing of resistance genes and mobilomes, should be integrated with existing methodologies to understand how wildlife maintains and disperses AMR.Introduction A growing human population and increasing fragmentation of natural habitats inevitably forces wildlife into greater contact, both direct and indirect, with humans and their livestock, thereby increasing the opportunities for transmission of infection between and within populations ADDIN EN.CITE <EndNote><Cite><Author>Jones</Author><Year>2008</Year><RecNum>4696</RecNum><DisplayText>[1]</DisplayText><record><rec-number>4696</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">4696</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Jones, Kate E.</author><author>Patel, Nikkita G.</author><author>Levy, Marc A.</author><author>Storeygard, Adam</author><author>Balk, Deborah</author><author>Gittleman, John L.</author><author>Daszak, Peter</author></authors></contributors><titles><title>Global trends in emerging infectious diseases</title><secondary-title>Nature</secondary-title></titles><periodical><full-title>Nature</full-title></periodical><pages>990-993</pages><volume>451</volume><number>7181</number><dates><year>2008</year><pub-dates><date>02/21/print</date></pub-dates></dates><publisher>Nature Publishing Group</publisher><isbn>0028-0836</isbn><work-type>10.1038/nature06536</work-type><urls><related-urls><url>;[1]. While some progress has been made in understanding the epidemiology of multi-host infections involving wildlife ADDIN EN.CITE <EndNote><Cite><Author>Wiethoelter</Author><Year>2015</Year><RecNum>4798</RecNum><DisplayText>[2]</DisplayText><record><rec-number>4798</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">4798</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Wiethoelter, Anke K.</author><author>Beltrán-Alcrudo, Daniel</author><author>Kock, Richard</author><author>Mor, Siobhan M.</author></authors></contributors><titles><title>Global trends in infectious diseases at the wildlife–livestock interface</title><secondary-title>Proceedings of the National Academy of Sciences</secondary-title></titles><periodical><full-title>Proceedings of the National Academy of Sciences</full-title></periodical><pages>9662-9667</pages><volume>112</volume><number>31</number><dates><year>2015</year><pub-dates><date>August 4, 2015</date></pub-dates></dates><urls><related-urls><url>;[2], less attention has been paid to the role of wild animals in the ecology and evolution of antimicrobial resistance (AMR) PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5IdWlqYmVyczwvQXV0aG9yPjxZZWFyPjIwMTU8L1llYXI+
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ADDIN EN.CITE.DATA [3, 4]. Although AMR is considered one of the greatest challenges to global health security ADDIN EN.CITE <EndNote><Cite><Author>WHO</Author><Year>2014</Year><RecNum>4246</RecNum><DisplayText>[5]</DisplayText><record><rec-number>4246</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">4246</key></foreign-keys><ref-type name="Report">27</ref-type><contributors><authors><author>WHO</author></authors><tertiary-authors><author>HWorl Health Organisation</author></tertiary-authors></contributors><titles><title>Antimicrobial resistance: global report on surveillance 2014</title></titles><dates><year>2014</year></dates><publisher>World Health Organisation</publisher><accession-num>978 92 4 156474 8</accession-num><urls></urls></record></Cite></EndNote>[5], to date, most AMR research has been based in clinical settings ADDIN EN.CITE <EndNote><Cite><Author>Davies</Author><Year>2010</Year><RecNum>4185</RecNum><DisplayText>[6]</DisplayText><record><rec-number>4185</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">4185</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Davies, Julian</author><author>Davies, Dorothy</author></authors></contributors><titles><title>Origins and Evolution of Antibiotic Resistance</title><secondary-title>Microbiology and Molecular Biology Reviews</secondary-title><alt-title>Microbiol Mol Biol Rev</alt-title></titles><periodical><full-title>Microbiology and Molecular Biology Reviews</full-title></periodical><pages>417-+</pages><volume>74</volume><number>3</number><dates><year>2010</year><pub-dates><date>Sep</date></pub-dates></dates><isbn>1092-2172</isbn><accession-num>WOS:000281417600004</accession-num><urls><related-urls><url><Go to ISI>://WOS:000281417600004</url></related-urls></urls><electronic-resource-num>10.1128/mmbr.00016-10</electronic-resource-num></record></Cite></EndNote>[6]. Relatively little is known about the flow and fate of AMR in the natural environment PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5XZWxsaW5ndG9uPC9BdXRob3I+PFllYXI+MjAxMzwvWWVh
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ADDIN EN.CITE.DATA [3, 4] (Figure 1). In this review, we discuss the possible role of wildlife in the dissemination of AMR, specifically how wildlife might acquire and transport AMR and the potential for them to transmit AMR to humans and livestock.Antimicrobial ResistanceAntimicrobial drugs have saved millions of human lives and improved animal health and welfare globally ADDIN EN.CITE <EndNote><Cite><Author>Davies</Author><Year>2010</Year><RecNum>4185</RecNum><DisplayText>[6]</DisplayText><record><rec-number>4185</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">4185</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Davies, Julian</author><author>Davies, Dorothy</author></authors></contributors><titles><title>Origins and Evolution of Antibiotic Resistance</title><secondary-title>Microbiology and Molecular Biology Reviews</secondary-title><alt-title>Microbiol Mol Biol Rev</alt-title></titles><periodical><full-title>Microbiology and Molecular Biology Reviews</full-title></periodical><pages>417-+</pages><volume>74</volume><number>3</number><dates><year>2010</year><pub-dates><date>Sep</date></pub-dates></dates><isbn>1092-2172</isbn><accession-num>WOS:000281417600004</accession-num><urls><related-urls><url><Go to ISI>://WOS:000281417600004</url></related-urls></urls><electronic-resource-num>10.1128/mmbr.00016-10</electronic-resource-num></record></Cite></EndNote>[6]. Consequently, the evolution and dispersal of AMR is considered to be a major problem facing medical science and food security ADDIN EN.CITE <EndNote><Cite><Author>WHO</Author><Year>2014</Year><RecNum>4246</RecNum><DisplayText>[5]</DisplayText><record><rec-number>4246</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">4246</key></foreign-keys><ref-type name="Report">27</ref-type><contributors><authors><author>WHO</author></authors><tertiary-authors><author>HWorl Health Organisation</author></tertiary-authors></contributors><titles><title>Antimicrobial resistance: global report on surveillance 2014</title></titles><dates><year>2014</year></dates><publisher>World Health Organisation</publisher><accession-num>978 92 4 156474 8</accession-num><urls></urls></record></Cite></EndNote>[5]. AMR is an ancient phenomenon, having evolved in dynamic microbial communities within which antimicrobials are produced by environmental bacteria and fungi naturally living in soil, water etc ADDIN EN.CITE <EndNote><Cite><Author>Davies</Author><Year>2010</Year><RecNum>4185</RecNum><DisplayText>[6]</DisplayText><record><rec-number>4185</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">4185</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Davies, Julian</author><author>Davies, Dorothy</author></authors></contributors><titles><title>Origins and Evolution of Antibiotic Resistance</title><secondary-title>Microbiology and Molecular Biology Reviews</secondary-title><alt-title>Microbiol Mol Biol Rev</alt-title></titles><periodical><full-title>Microbiology and Molecular Biology Reviews</full-title></periodical><pages>417-+</pages><volume>74</volume><number>3</number><dates><year>2010</year><pub-dates><date>Sep</date></pub-dates></dates><isbn>1092-2172</isbn><accession-num>WOS:000281417600004</accession-num><urls><related-urls><url><Go to ISI>://WOS:000281417600004</url></related-urls></urls><electronic-resource-num>10.1128/mmbr.00016-10</electronic-resource-num></record></Cite></EndNote>[6]. Such AMR, plus AMR as a side effect of selection of other properties, including efflux pumps for removing environmental stressors such as heavy metals, is often referred to as ‘intrinsic’ AMR. In contrast, ‘acquired’ AMR is the result of exposure to antimicrobial drugs which promotes resistance by selecting bacteria within a population with genetic traits conferring resistance. Thus, the selection of AMR in both pathogens and the normal gut microbiota of livestock and humans is believed to be largely a consequence of increased selective pressure provided by clinical antimicrobial use: recent hospitalisation, for example, is a risk factor for shedding antibiotic resistant E. coli in both horses ADDIN EN.CITE <EndNote><Cite><Author>Maddox</Author><Year>2012</Year><RecNum>4104</RecNum><DisplayText>[8]</DisplayText><record><rec-number>4104</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">4104</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Maddox, T. W.</author><author>Pinchbeck, G. L.</author><author>Clegg, P. D.</author><author>Wedley, A. L.</author><author>Dawson, S.</author><author>Williams, N. J.</author></authors></contributors><titles><title>Cross-sectional study of antimicrobial-resistant bacteria in horses. Part 2: Risk factors for faecal carriage of antimicrobial-resistant Escherichia coli in horses</title><secondary-title>Equine Veterinary Journal</secondary-title><alt-title>Equine Vet J</alt-title></titles><periodical><full-title>Equine Vet J</full-title><abbr-1>Equine veterinary journal</abbr-1></periodical><alt-periodical><full-title>Equine Vet J</full-title><abbr-1>Equine veterinary journal</abbr-1></alt-periodical><pages>297-303</pages><volume>44</volume><number>3</number><keywords><keyword>horses</keyword><keyword>antimicrobial resistance</keyword><keyword>risk factors</keyword><keyword>Escherichia coli</keyword><keyword>extended spectrum β-lactamases</keyword></keywords><dates><year>2012</year></dates><publisher>Blackwell Publishing Ltd</publisher><isbn>2042-3306</isbn><urls><related-urls><url>;[8] and humans PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5DYXJkb3NvPC9BdXRob3I+PFllYXI+MjAxMjwvWWVhcj48
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ADDIN EN.CITE.DATA [9]. In many parts of the world, antimicrobials are still used, not just in clinical settings, but as ‘growth promoters’ in food-producing animals, an activity banned in the EU owing to concerns about the selection of AMR ADDIN EN.CITE <EndNote><Cite><Author>Marshall</Author><Year>2011</Year><RecNum>4806</RecNum><DisplayText>[10]</DisplayText><record><rec-number>4806</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">4806</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Marshall, Bonnie M.</author><author>Levy, Stuart B.</author></authors></contributors><titles><title>Food Animals and Antimicrobials: Impacts on Human Health</title><secondary-title>Clinical Microbiology Reviews</secondary-title><alt-title>Clin Microbiol Rev</alt-title></titles><periodical><full-title>Clinical Microbiology Reviews</full-title></periodical><alt-periodical><full-title>Clin Microbiol Rev</full-title></alt-periodical><pages>718-733</pages><volume>24</volume><number>4</number><dates><year>2011</year><pub-dates><date>October 1, 2011</date></pub-dates></dates><urls><related-urls><url>;[10]. So, while wildlife could provide a reservoir of intrinsic genetic determinants for resistance, it has usually been assumed that AMR detected in wildlife samples is acquired AMR resulting directly or indirectly from antibiotic-treated humans or livestock ADDIN EN.CITE <EndNote><Cite><Author>Vittecoq</Author><Year>2016</Year><RecNum>5158</RecNum><DisplayText>[11]</DisplayText><record><rec-number>5158</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">5158</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Vittecoq, Marion</author><author>Godreuil, Sylvain</author><author>Prugnolle, Franck</author><author>Durand, Patrick</author><author>Brazier, Lionel</author><author>Renaud, Nicolas</author><author>Arnal, Audrey</author><author>Aberkane, Salim</author><author>Jean-Pierre, Hélène</author><author>Gauthier-Clerc, Michel</author><author>Thomas, Frédéric</author><author>Renaud, Fran?ois</author></authors></contributors><titles><title>REVIEW: Antimicrobial resistance in wildlife</title><secondary-title>Journal of Applied Ecology</secondary-title></titles><periodical><full-title>Journal of Applied Ecology</full-title></periodical><pages>519-529</pages><volume>53</volume><number>2</number><keywords><keyword>antibiotic resistance</keyword><keyword>antibiotic-resistant bacteria</keyword><keyword>emerging infectious disease</keyword><keyword>Escherichia?coli</keyword><keyword>health ecology</keyword><keyword>Klebsiella?pneumoniae</keyword><keyword>MRSA</keyword><keyword>pathogens</keyword><keyword>Salmonella?spp.</keyword><keyword>transmission routes</keyword></keywords><dates><year>2016</year></dates><isbn>1365-2664</isbn><urls><related-urls><url>;[11]. The ecology of AMR is complicated by the horizontal spread of the genes encoding AMR through communities of different species and even genera of bacteria via mobile genetic elements such as plasmids (extra-chromosomal DNA molecules). These mobile genetic elements often encode multiple genes, providing resistance to antimicrobials and, indeed, other environmental chemical stressors including metals and disinfectants. Consequently exposure to one antimicrobial (or other stressor) can select for all co-encoded genes and thus the rapid emergence of multi-drug resistance ADDIN EN.CITE <EndNote><Cite><Author>Davies</Author><Year>2010</Year><RecNum>4185</RecNum><DisplayText>[6]</DisplayText><record><rec-number>4185</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">4185</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Davies, Julian</author><author>Davies, Dorothy</author></authors></contributors><titles><title>Origins and Evolution of Antibiotic Resistance</title><secondary-title>Microbiology and Molecular Biology Reviews</secondary-title><alt-title>Microbiol Mol Biol Rev</alt-title></titles><periodical><full-title>Microbiology and Molecular Biology Reviews</full-title></periodical><pages>417-+</pages><volume>74</volume><number>3</number><dates><year>2010</year><pub-dates><date>Sep</date></pub-dates></dates><isbn>1092-2172</isbn><accession-num>WOS:000281417600004</accession-num><urls><related-urls><url><Go to ISI>://WOS:000281417600004</url></related-urls></urls><electronic-resource-num>10.1128/mmbr.00016-10</electronic-resource-num></record></Cite></EndNote>[6]. Thus, wildlife and other environmental bacteria that have never been found to infect humans can, through horizontal gene transfer, exchange resistance mechanisms with human pathogens PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5WaXR0ZWNvcTwvQXV0aG9yPjxZZWFyPjIwMTY8L1llYXI+
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ADDIN EN.CITE.DATA [13].Potential sources of AMR in the environment to wildlifeFollowing selection of resistance within individuals (human or domesticated animals) treated with antimicrobials ADDIN EN.CITE <EndNote><Cite><Author>Marshall</Author><Year>2011</Year><RecNum>4806</RecNum><DisplayText>[10]</DisplayText><record><rec-number>4806</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">4806</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Marshall, Bonnie M.</author><author>Levy, Stuart B.</author></authors></contributors><titles><title>Food Animals and Antimicrobials: Impacts on Human Health</title><secondary-title>Clinical Microbiology Reviews</secondary-title><alt-title>Clin Microbiol Rev</alt-title></titles><periodical><full-title>Clinical Microbiology Reviews</full-title></periodical><alt-periodical><full-title>Clin Microbiol Rev</full-title></alt-periodical><pages>718-733</pages><volume>24</volume><number>4</number><dates><year>2011</year><pub-dates><date>October 1, 2011</date></pub-dates></dates><urls><related-urls><url>;[10], both resistant bacteria and antimicrobials are subsequently excreted by the patient (Figure 1). These can be dispersed in the environment, for example in sewage effluent pumped into rivers ADDIN EN.CITE <EndNote><Cite><Author>Graham</Author><Year>2014</Year><RecNum>5120</RecNum><DisplayText>[14]</DisplayText><record><rec-number>5120</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">5120</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Graham, David W.</author><author>Collignon, Peter</author><author>Davies, Julian</author><author>Larsson, D. G. Joakim</author><author>Snape, Jason</author></authors></contributors><titles><title>Underappreciated Role of Regionally Poor Water Quality on Globally Increasing Antibiotic Resistance</title><secondary-title>Environmental Science & Technology</secondary-title><alt-title>Amer Chem Soc</alt-title></titles><periodical><full-title>Environmental Science & Technology</full-title></periodical><pages>11746-11747</pages><volume>48</volume><number>20</number><dates><year>2014</year><pub-dates><date>2014/10/21</date></pub-dates></dates><publisher>American Chemical Society</publisher><isbn>0013-936X</isbn><urls><related-urls><url>;[14] and spreading sewage sludge as a fertiliser, or in the faeces of treated livestock and pets PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5MZWF0aGVyYmFycm93PC9BdXRob3I+PFllYXI+MjAwNzwv
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ADDIN EN.CITE.DATA [15, 16](Figure 2). Effluent and run-off from fields will often end up flowing into the sea, resulting in estuaries, coastal waters and beaches polluted by faecal matter ADDIN EN.CITE <EndNote><Cite><Author>Graham</Author><Year>2014</Year><RecNum>5120</RecNum><DisplayText>[14]</DisplayText><record><rec-number>5120</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">5120</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Graham, David W.</author><author>Collignon, Peter</author><author>Davies, Julian</author><author>Larsson, D. G. Joakim</author><author>Snape, Jason</author></authors></contributors><titles><title>Underappreciated Role of Regionally Poor Water Quality on Globally Increasing Antibiotic Resistance</title><secondary-title>Environmental Science & Technology</secondary-title><alt-title>Amer Chem Soc</alt-title></titles><periodical><full-title>Environmental Science & Technology</full-title></periodical><pages>11746-11747</pages><volume>48</volume><number>20</number><dates><year>2014</year><pub-dates><date>2014/10/21</date></pub-dates></dates><publisher>American Chemical Society</publisher><isbn>0013-936X</isbn><urls><related-urls><url>;[14](Figure 1). This could be a critical point of contact where humans and marine animals, as well as waders and seabirds, are exposed to AMR ADDIN EN.CITE <EndNote><Cite><Author>Leonard</Author><Year>2015</Year><RecNum>4799</RecNum><DisplayText>[17]</DisplayText><record><rec-number>4799</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">4799</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Leonard, Anne F. C.</author><author>Zhang, Lihong</author><author>Balfour, Andrew J.</author><author>Garside, Ruth</author><author>Gaze, William H.</author></authors></contributors><titles><title>Human recreational exposure to antibiotic resistant bacteria in coastal bathing waters</title><secondary-title>Environment International</secondary-title></titles><periodical><full-title>Environment International</full-title></periodical><pages>92-100</pages><volume>82</volume><keywords><keyword>Antibiotic resistant bacteria</keyword><keyword>Third-generation cephalosporin</keyword><keyword>Escherichia coli</keyword><keyword>Coastal waters</keyword><keyword>Water sports</keyword></keywords><dates><year>2015</year><pub-dates><date>9//</date></pub-dates></dates><isbn>0160-4120</isbn><urls><related-urls><url>;[17]. The aquaculture industry, is another source of AMR and antimicrobials to the environment: fish and seafood farmed in some countries where antimicrobial usage is high and poorly regulated are particularly likely to carry medically significant resistant pathogens PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5DYWJlbGxvPC9BdXRob3I+PFllYXI+MjAxMzwvWWVhcj48
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ADDIN EN.CITE.DATA [4, 18].Evolution of AMR does not necessarily stop in the gastro-intestinal tract of animals (including humans) undergoing treatment; many antimicrobials can be excreted in an active form and persist in the environment ADDIN EN.CITE <EndNote><Cite><Author>Kasprzyk-Hordern</Author><Year>2009</Year><RecNum>4202</RecNum><DisplayText>[19]</DisplayText><record><rec-number>4202</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">4202</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Kasprzyk-Hordern, Barbara</author><author>Dinsdale, Richard M.</author><author>Guwy, Alan J.</author></authors></contributors><titles><title>The removal of pharmaceuticals, personal care products, endocrine disruptors and illicit drugs during wastewater treatment and its impact on the quality of receiving waters</title><secondary-title>Water Research</secondary-title><alt-title>Water Research</alt-title></titles><periodical><full-title>Water Research</full-title></periodical><alt-periodical><full-title>Water Research</full-title></alt-periodical><pages>363-380</pages><volume>43</volume><number>2</number><keywords><keyword>Pharmaceuticals</keyword><keyword>Personal care products</keyword><keyword>Illicit drugs</keyword><keyword>Endocrine disruptors</keyword><keyword>Wastewater</keyword><keyword>Surface water</keyword><keyword>Activated sludge</keyword><keyword>Trickling filter beds</keyword></keywords><dates><year>2009</year><pub-dates><date>2//</date></pub-dates></dates><isbn>0043-1354</isbn><urls><related-urls><url>;[19]. Thus ongoing exposure to antimicrobial drugs, for example in sewage, might maintain the selective advantage of AMR and promote the proliferation of resistance determinants and resistant bacteria in the environment. There is an added risk from sites highly contaminated with excreta, such as intensive farms and sewage treatment plants. Places with a high abundance and diversity of bacteria provide a high density of bacterial hosts and excellent conditions for the horizontal transmission of antimicrobial resistance genes from commensal or environmental to pathogenic bacteria ADDIN EN.CITE <EndNote><Cite><Author>Heuer</Author><Year>2011</Year><RecNum>4182</RecNum><DisplayText>[20]</DisplayText><record><rec-number>4182</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">4182</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Heuer, Holger</author><author>Schmitt, Heike</author><author>Smalla, Kornelia</author></authors></contributors><titles><title>Antibiotic resistance gene spread due to manure application on agricultural fields</title><secondary-title>Current Opinion in Microbiology</secondary-title><alt-title>Curr Opin Microbiol</alt-title></titles><periodical><full-title>Current Opinion in Microbiology</full-title></periodical><pages>236-243</pages><volume>14</volume><number>3</number><dates><year>2011</year><pub-dates><date>Jun</date></pub-dates></dates><isbn>1369-5274</isbn><accession-num>WOS:000292948300003</accession-num><urls><related-urls><url><Go to ISI>://WOS:000292948300003</url></related-urls></urls><electronic-resource-num>10.1016/j.mib.2011.04.009</electronic-resource-num></record></Cite></EndNote>[20]. It is clear that, particularly in areas with dense human or livestock populations, there is a myriad of AMR sources and amplifiers. If AMR genes and bacteria are carried in the gut of wildlife, then coupled with inadequate waste management and long-range animal movements, there is potential for wildlife to transport new and emerging antimicrobial resistance genes around the world ADDIN EN.CITE <EndNote><Cite><Author>Graham</Author><Year>2014</Year><RecNum>5120</RecNum><DisplayText>[14]</DisplayText><record><rec-number>5120</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">5120</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Graham, David W.</author><author>Collignon, Peter</author><author>Davies, Julian</author><author>Larsson, D. G. Joakim</author><author>Snape, Jason</author></authors></contributors><titles><title>Underappreciated Role of Regionally Poor Water Quality on Globally Increasing Antibiotic Resistance</title><secondary-title>Environmental Science & Technology</secondary-title><alt-title>Amer Chem Soc</alt-title></titles><periodical><full-title>Environmental Science & Technology</full-title></periodical><pages>11746-11747</pages><volume>48</volume><number>20</number><dates><year>2014</year><pub-dates><date>2014/10/21</date></pub-dates></dates><publisher>American Chemical Society</publisher><isbn>0013-936X</isbn><urls><related-urls><url>;[14] (Figure 1). Patterns of AMR infection in wildlifeWith increasing pressure from expanding human populations, wild animals are increasingly forced to forage on resources contaminated by human ‘pathogen pollution’ PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5HcmFoYW08L0F1dGhvcj48WWVhcj4yMDE0PC9ZZWFyPjxS
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ADDIN EN.CITE.DATA [2, 14]. So it is not surprising that AMR has often been described in peri-domestic wildlife ADDIN EN.CITE <EndNote><Cite><Author>Vittecoq</Author><Year>2016</Year><RecNum>5158</RecNum><DisplayText>[11]</DisplayText><record><rec-number>5158</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">5158</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Vittecoq, Marion</author><author>Godreuil, Sylvain</author><author>Prugnolle, Franck</author><author>Durand, Patrick</author><author>Brazier, Lionel</author><author>Renaud, Nicolas</author><author>Arnal, Audrey</author><author>Aberkane, Salim</author><author>Jean-Pierre, Hélène</author><author>Gauthier-Clerc, Michel</author><author>Thomas, Frédéric</author><author>Renaud, Fran?ois</author></authors></contributors><titles><title>REVIEW: Antimicrobial resistance in wildlife</title><secondary-title>Journal of Applied Ecology</secondary-title></titles><periodical><full-title>Journal of Applied Ecology</full-title></periodical><pages>519-529</pages><volume>53</volume><number>2</number><keywords><keyword>antibiotic resistance</keyword><keyword>antibiotic-resistant bacteria</keyword><keyword>emerging infectious disease</keyword><keyword>Escherichia?coli</keyword><keyword>health ecology</keyword><keyword>Klebsiella?pneumoniae</keyword><keyword>MRSA</keyword><keyword>pathogens</keyword><keyword>Salmonella?spp.</keyword><keyword>transmission routes</keyword></keywords><dates><year>2016</year></dates><isbn>1365-2664</isbn><urls><related-urls><url>;[11]. AMR has been detected, particularly among commensal gut bacteria, in wild mammals, birds, reptiles and fish, with the prevalence and resistance patterns varying across species, locations and possibly time (e.g. PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5PcmF2Y292YTwvQXV0aG9yPjxZZWFyPjIwMTM8L1llYXI+
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ADDIN EN.CITE.DATA [28]. Similarly, in the Galapagos, molecular markers of AMR were more common in both seawater samples and marine iguanas close to tourist sites compared with those from more pristine conservation areas ADDIN EN.CITE <EndNote><Cite><Author>Wheeler</Author><Year>2012</Year><RecNum>3864</RecNum><DisplayText>[23]</DisplayText><record><rec-number>3864</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">3864</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Wheeler, Emily</author><author>Hong, Pei-Ying</author><author>Bedon, Lenin Cruz</author><author>Mackie, Roderick I.</author></authors></contributors><titles><title>Carriage of antibiotic-resistant enteric bacteria varies among sites in Galapagos reptiles</title><secondary-title>Journal of Wildlife Diseases</secondary-title><alt-title>J Wildlife Dis</alt-title></titles><periodical><full-title>Journal of Wildlife Diseases</full-title></periodical><pages>56-67</pages><volume>48</volume><number>1</number><dates><year>2012</year><pub-dates><date>January 1, 2012</date></pub-dates></dates><urls><related-urls><url> </url></related-urls></urls></record></Cite></EndNote>[23]. There are, however, exceptions to the generally positive relationship between spatial distance to anthropogenic wastes and the detection of clinically important resistance genes. For example, resistance to ciprofloxacin, a relatively recently developed and completely synthetic antimicrobial, was detected even in the most remote groups of monkeys in Mexico ADDIN EN.CITE <EndNote><Cite><Author>Cristóbal-Azkarate</Author><Year>2014</Year><RecNum>4694</RecNum><DisplayText>[27]</DisplayText><record><rec-number>4694</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">4694</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Cristóbal-Azkarate, Jurgi</author><author>Dunn, Jacob C.</author><author>Day, Jennifer M. W.</author><author>Amábile-Cuevas, Carlos F.</author></authors></contributors><titles><title>Resistance to Antibiotics of Clinical Relevance in the Fecal Microbiota of Mexican Wildlife</title><secondary-title>PLoS ONE</secondary-title></titles><periodical><full-title>Plos One</full-title></periodical><pages>e107719</pages><volume>9</volume><number>9</number><dates><year>2014</year></dates><publisher>Public Library of Science</publisher><urls><related-urls><url>;[27]. This is suggestive of de novo evolution of resistance, horizontal gene transfer from environmental microbes and/or greater contact with humans than previously thought. Further molecular and ecological investigations are clearly required. In general, however, study sites with relatively low or well defined AMR inputs enable us to quantify spatial patterns, pathways and processes that drive AMR dissemination at different scales. In heavily populated areas, high background AMR levels often cloud observations. In the UK, for example, we and others have found that AMR is frequently found in both wild mammals and birds, although the sources and drivers of AMR are often unclear PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5XaWxsaWFtczwvQXV0aG9yPjxZZWFyPjIwMTE8L1llYXI+
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ADDIN EN.CITE.DATA [22, 29-31]; see Fig. 2 and Table 1]. We found that the patterns of AMR in E. coli from rodents resident on intensive livestock farms (Table 1), and the genes encoding that resistance, were often similar. The E. coli only rarely identified shared genotypes, however, suggesting an important role for the mobilome (all mobile genetic elements in a genome, e.g. plasmids) and horizontal transmission of AMR rather than simple cross-species transmission of resistant bacteria. In contrast, at less intensively farmed sites, such as dairy farms with cattle kept outside, no clear relationships between either patterns or the genetics of AMR were found in livestock and wildlife ADDIN EN.CITE <EndNote><Cite><Author>Al-Tunesi</Author><Year>2009</Year><RecNum>5142</RecNum><DisplayText>[31]</DisplayText><record><rec-number>5142</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">5142</key></foreign-keys><ref-type name="Thesis">32</ref-type><contributors><authors><author>Al-Tunesi, Lutfi Abdelhamid</author></authors></contributors><titles><title>Prevalence of antibiotic-resistant Escherichia coli in faecal samples from domestic animals and wildlife : a cross-sectional study</title><secondary-title>Veterinary Pathology</secondary-title></titles><volume>Thesis Ph.D.</volume><dates><year>2009</year></dates><publisher>University of Liverpool</publisher><urls></urls></record></Cite></EndNote>[31]. As in the African and South American studies, we also found AMR in wildlife in relatively remote and uninhabited (by humans) areas (Table 1). Furthermore, sympatric populations of wild mammals, including different species of rodents sharing the same woodland habitat, had different patterns of AMR and/or different temporal dynamics ADDIN EN.CITE <EndNote><Cite><Author>Williams</Author><Year>2011</Year><RecNum>4152</RecNum><DisplayText>[29]</DisplayText><record><rec-number>4152</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">4152</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Williams, N. J.</author><author>Sherlock, C.</author><author>Jones, T. R.</author><author>Clough, H. E.</author><author>Telfer, S. E.</author><author>Begon, M.</author><author>French, N.</author><author>Hart, C. A.</author><author>Bennett, M.</author></authors></contributors><titles><title>The prevalence of antimicrobial-resistant Escherichia coli in sympatric wild rodents varies by season and host</title><secondary-title>Journal of Applied Microbiology</secondary-title><alt-title>J App Microbiol</alt-title></titles><periodical><full-title>Journal of Applied Microbiology</full-title></periodical><pages>962-970</pages><volume>110</volume><number>4</number><dates><year>2011</year><pub-dates><date>Apr</date></pub-dates></dates><isbn>1364-5072</isbn><accession-num>WOS:000288169600012</accession-num><urls><related-urls><url><Go to ISI>://WOS:000288169600012</url></related-urls></urls><electronic-resource-num>10.1111/j.1365-2672.2011.04952.x</electronic-resource-num></record></Cite></EndNote>[29]. This strongly suggests that AMR in the bacterial microbiota of wildlife is not simply a matter of recent anthropogenic contamination or selection. So while most studies in wildlife have assumed that AMR in wildlife is the consequence of spill-over of resistant bacteria from domestic animals or people PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5XYXJkeW48L0F1dGhvcj48WWVhcj4yMDEyPC9ZZWFyPjxS
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ADDIN EN.CITE.DATA [13]) are, and have always been, a normal finding in commensal gut microbiota. Moreover, distinguishing between AMR recently acquired from anthropogenic sources, such as a farm or sewage treatment plants, and ‘intrinsic’ (or at least ‘naturalised’) background AMR will be challenging. Comparing the similarity of sequences of resistance genes collected from sites differing in their connectedness to sources of acquired AMR (e.g. using sequence similarity network approaches) ADDIN EN.CITE <EndNote><Cite><Author>Fondi</Author><Year>2016</Year><RecNum>5159</RecNum><DisplayText>[12]</DisplayText><record><rec-number>5159</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">5159</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Fondi, M</author><author>Karkman, A</author><author>Tamminen, M</author><author>Bosi, E</author><author>Virta, M</author><author>Fani, R</author><author>Alm, E</author><author>McInerney, JO</author></authors></contributors><titles><title>Every gene is everywhere but the environment selects: Global geo-localization of gene sharing in environmental samples through network analysis</title><secondary-title>Genome Biology and Evolution</secondary-title></titles><periodical><full-title>Genome Biology and Evolution</full-title></periodical><dates><year>2016</year><pub-dates><date>April 29, 2016</date></pub-dates></dates><urls><related-urls><url>;[12] could provide the evidence required. A particular concern about AMR dispersal is wildlife species that have the capacity for long range movements. Migratory birds could transfer new or emerging patterns of AMR, but even resident species have the potential to move AMR from hotspots to vulnerable populations. The potential of wild animals to disseminate AMR depends on their AMR ‘infection’ status, their direct and indirect contact with other populations and their movements within the landscape. In communal corvid roosts in Europe and the USA, 2.5 – 6.0% of faecal samples contained resistance genes for vancomycin, a antimicrobial ‘of last resort’ in human medicine PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5PcmF2Y292YTwvQXV0aG9yPjxZZWFyPjIwMTM8L1llYXI+
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ADDIN EN.CITE.DATA [21, 34]. Gulls carrying medically significant AMR, are capable of long range movements and are increasingly found feeding on anthropogenic waste and nesting in urban areas ADDIN EN.CITE <EndNote><Cite><Author>Bonnedahl</Author><Year>2014</Year><RecNum>4678</RecNum><DisplayText>[22]</DisplayText><record><rec-number>4678</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">4678</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Bonnedahl, Jonas</author><author>J?rhult, Josef D.</author></authors></contributors><titles><title>Antibiotic resistance in wild birds</title><secondary-title>Upsala Journal of Medical Sciences</secondary-title></titles><periodical><full-title>Upsala Journal of Medical Sciences</full-title></periodical><pages>113-116</pages><volume>119</volume><number>2</number><dates><year>2014</year></dates><accession-num>24697355</accession-num><urls><related-urls><url>;[22], PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5TasO2bHVuZDwvQXV0aG9yPjxZZWFyPjIwMDg8L1llYXI+
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ADDIN EN.CITE.DATA [25, 35]. Similarly, in aquatic ecosystems uneaten food and faeces from human sewage, agriculture and aquaculture containing antimicrobials and AMR bacteria can be ingested by wild fish and other organisms, which can travel enormous distances and in some cases enter the human food chain ADDIN EN.CITE <EndNote><Cite><Author>Cabello</Author><Year>2013</Year><RecNum>4800</RecNum><DisplayText>[18]</DisplayText><record><rec-number>4800</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">4800</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Cabello, Felipe C.</author><author>Godfrey, Henry P.</author><author>Tomova, Alexandra</author><author>Ivanova, Larisa</author><author>D?lz, Humberto</author><author>Millanao, Ana</author><author>Buschmann, Alejandro H.</author></authors></contributors><titles><title>Antimicrobial use in aquaculture re-examined: its relevance to antimicrobial resistance and to animal and human health</title><secondary-title>Environmental Microbiology</secondary-title></titles><periodical><full-title>Environmental Microbiology</full-title></periodical><pages>1917-1942</pages><volume>15</volume><number>7</number><dates><year>2013</year></dates><isbn>1462-2920</isbn><urls><related-urls><url>;[18]. However, most of these studies on globally moving species are one-off surveys of AMR prevalence with no attempt to identify infection sources (or sinks) ADDIN EN.CITE <EndNote><Cite><Author>Huijbers</Author><Year>2015</Year><RecNum>5067</RecNum><DisplayText>[3]</DisplayText><record><rec-number>5067</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">5067</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Huijbers, Patricia M. C.</author><author>Blaak, Hetty</author><author>de Jong, Mart C. M.</author><author>Graat, Elisabeth A. M.</author><author>Vandenbroucke-Grauls, Christina M. J. E.</author><author>Husman, Ana Maria de Roda</author></authors></contributors><titles><title>Role of the Environment in the Transmission of Antimicrobial Resistance to Humans: A Review</title><secondary-title>Environmental Science & Technology</secondary-title></titles><periodical><full-title>Environmental Science & Technology</full-title></periodical><pages>11993-12004</pages><volume>49</volume><number>20</number><dates><year>2015</year><pub-dates><date>Oct 20</date></pub-dates></dates><isbn>0013-936X</isbn><accession-num>WOS:000363348700002</accession-num><urls><related-urls><url><Go to ISI>://WOS:000363348700002</url></related-urls></urls><electronic-resource-num>10.1021/acs.est.5b02566</electronic-resource-num></record></Cite></EndNote>[3], which limits our ability to estimate the risk posed by migratory species in disseminating AMR. Finally, it remains unknown whether AMR can be or, more importantly, is transmitted from wildlife to humans or domestic animals, which is the main concern of clinicians and policy makers.Studying AMR dispersal by wildlifeGiven the many knowledge gaps, a range of tools and approaches will be needed to identify and characterise transmission routes of AMR in wildlife. At a broad scale, identifying traits that predispose wildlife species or functional groups to transmit AMR could be determined by integrating ecological, biological and life history datasets for vertebrate hosts with metagenome sequences embedding resistance determinants ADDIN EN.CITE <EndNote><Cite><Author>Fondi</Author><Year>2016</Year><RecNum>5159</RecNum><DisplayText>[12]</DisplayText><record><rec-number>5159</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">5159</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Fondi, M</author><author>Karkman, A</author><author>Tamminen, M</author><author>Bosi, E</author><author>Virta, M</author><author>Fani, R</author><author>Alm, E</author><author>McInerney, JO</author></authors></contributors><titles><title>Every gene is everywhere but the environment selects: Global geo-localization of gene sharing in environmental samples through network analysis</title><secondary-title>Genome Biology and Evolution</secondary-title></titles><periodical><full-title>Genome Biology and Evolution</full-title></periodical><dates><year>2016</year><pub-dates><date>April 29, 2016</date></pub-dates></dates><urls><related-urls><url>;[12]. While this is an efficient and informative approach, one caveat is that by mining such data, we can only find known resistance determinants. Some evidence from wildlife studies shows that the genes responsible for phenotypic resistance are often not detectable using PCRs targeted at common clinical AMR genes, suggesting a greater diversity of resistance genes (many of which will already have been associated with other, non-AMR, functions) in the environment than found in clinical isolates (Authors’ Unpub. Data).At a finer scale, study systems are needed in which clear and measurable transmission routes for AMR exist and the movement of wildlife can be tracked. The discovery of multidrug resistance in species of high conservation value on oceanic islands ADDIN EN.CITE <EndNote><Cite><Author>Wheeler</Author><Year>2012</Year><RecNum>3864</RecNum><DisplayText>[23]</DisplayText><record><rec-number>3864</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">3864</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Wheeler, Emily</author><author>Hong, Pei-Ying</author><author>Bedon, Lenin Cruz</author><author>Mackie, Roderick I.</author></authors></contributors><titles><title>Carriage of antibiotic-resistant enteric bacteria varies among sites in Galapagos reptiles</title><secondary-title>Journal of Wildlife Diseases</secondary-title><alt-title>J Wildlife Dis</alt-title></titles><periodical><full-title>Journal of Wildlife Diseases</full-title></periodical><pages>56-67</pages><volume>48</volume><number>1</number><dates><year>2012</year><pub-dates><date>January 1, 2012</date></pub-dates></dates><urls><related-urls><url> </url></related-urls></urls></record></Cite></EndNote>[23] and in samples from isolated, relatively untouched points on continents ADDIN EN.CITE <EndNote><Cite><Author>Sj?lund</Author><Year>2008</Year><RecNum>4698</RecNum><DisplayText>[25]</DisplayText><record><rec-number>4698</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">4698</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Sj?lund, Maria</author><author>Bonnedahl, Jonas</author><author>Hernandez, Jorge</author><author>Bengtsson, Stina</author><author>Cederbrant, Gunilla</author><author>Pinhassi, Jarone</author><author>Kahlmeter, Gunnar</author><author>Olsen, Bj?rn</author></authors></contributors><titles><title>Dissemination of Multidrug-Resistant Bacteria into the Arctic</title><secondary-title>Emerging Infectious Diseases</secondary-title></titles><periodical><full-title>Emerging Infectious Diseases</full-title></periodical><pages>70-72</pages><volume>14</volume><number>1</number><dates><year>2008</year></dates><publisher>Centers for Disease Control and Prevention</publisher><isbn>1080-6040
1080-6059</isbn><accession-num>PMC2600168</accession-num><urls><related-urls><url>;[25] provide ‘natural experiments’ that are ideal for studying patterns and processes in the ecology and evolution of AMR. Monitoring AMR genes within such pristine ecosystems (e.g. Arctic or nature reserves with tight biosecurity), or at their interface with human-influenced areas enables us to estimate the frequency with which genes encoding resistance are exchanged in microbial communities within human, domestic animal and wildlife populations, as well as the wider environment PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5BbGJyZWNodG92YTwvQXV0aG9yPjxZZWFyPjIwMTQ8L1ll
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ADDIN EN.CITE.DATA [25, 36].When working in the more contaminated ‘natural’ environments common to densely populated areas, distinguishing between AMR acquired from anthropogenic sources, such as a farm or sewage treatment plant, versus naturally occurring or naturalised ‘background’ AMR will be more challenging. One approach is to study the dispersal of relatively rare AMR determinants, currently associated only with human (or particular livestock) populations, through food chains. For example, fluoroquinolone resistance and extended-spectrum beta-lactamases (ESBL) (conferring resistance to newer antibiotics used in human medicine), are relatively unusual in livestock and, in our experience, incredibly rare in wildlife. Such resistance might be tracked through high risk ecosystems, for example from sewage treatment plants or livestock slurry pits into the surrounding environment, at multiple levels: phenotypic resistance, bacterial genotype, mobile elements and individual resistance genes. High-throughput next-generation sequencing, can rapidly provide such detailed forensic trails PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5Gb3JzYmVyZzwvQXV0aG9yPjxZZWFyPjIwMTQ8L1llYXI+
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ADDIN EN.CITE.DATA [13] and although targeted at a limited range of AMR, would provide a good understanding of the ecology of AMR genes and their ‘resistome’ context. Deeper, meta-genomic sequencing studies through these and/or less high risk ecosystems will be needed to place such targeted AMR studies in a broader perspective, through examining a range of AMR genes across taxa of host bacteria within the same samples. However, metagenomic studies have their own challenges, not least the volume and complexity of bioinformatic data analysis and the cost, which currently limits sample number and interpretation. Ecological models of AMR transmission involving wildlife need to incorporate indirect rather than just direct host-to-host transmission. Although AMR can be transmitted directly between hosts, for example through predation (food-borne in a clinical context) or grooming and faeco-oral transmission, there is a huge overlap between the microbiota of the normal gut and that of the external environment with horizontal transmission of AMR possible in both. Such models could be based on spatial movements in relation to a common environmental source of AMR contamination such as a refuse dump ADDIN EN.CITE <EndNote><Cite><Author>Rwego</Author><Year>2008</Year><RecNum>4195</RecNum><DisplayText>[26]</DisplayText><record><rec-number>4195</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">4195</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Rwego, Innocent B.</author><author>Isabirye-Basuta, Gilbert</author><author>Gillespie, Thomas R.</author><author>Goldberg, Tony L.</author></authors></contributors><titles><title>Gastrointestinal Bacterial Transmission among Humans, Mountain Gorillas, and Livestock in Bwindi Impenetrable National Park, Uganda</title><secondary-title>Conservation Biology</secondary-title><alt-title>Cons Biol</alt-title></titles><periodical><full-title>Conservation Biology</full-title></periodical><pages>1600-1607</pages><volume>22</volume><number>6</number><dates><year>2008</year><pub-dates><date>Dec</date></pub-dates></dates><isbn>0888-8892</isbn><accession-num>WOS:000261395700036</accession-num><urls><related-urls><url><Go to ISI>://WOS:000261395700036</url></related-urls></urls><electronic-resource-num>10.1111/j.1523-1739.2008.01018.x</electronic-resource-num></record></Cite></EndNote>[26]. Sewage treatment plants, for example, are hotspots of AMR, which can provide valuable pockets of semi-natural habitat for birds and bats, attracted by the invertebrates that themselves feed in the sewage ADDIN EN.CITE <EndNote><Cite><Author>Park</Author><Year>2006</Year><RecNum>2786</RecNum><DisplayText>[37]</DisplayText><record><rec-number>2786</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">2786</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Park, K. J.</author><author>Cristinacce, A.</author></authors></contributors><titles><title>Use of sewage treatment works as foraging sites by insectivorous bats</title><secondary-title>Animal Conservation</secondary-title><alt-title>Anim Cons</alt-title></titles><periodical><full-title>Animal Conservation</full-title></periodical><pages>259-268</pages><volume>9</volume><number>3</number><keywords><keyword>activated sludge</keyword><keyword>percolating filter</keyword><keyword>Pipistrellus</keyword><keyword>Diptera</keyword><keyword>conservation</keyword><keyword>PIPISTRELLUS-PIPISTRELLUS</keyword><keyword>VESPERTILIONID BATS</keyword><keyword>FILTER-BEDS</keyword><keyword>HABITAT</keyword><keyword>USE</keyword><keyword>CHIROPTERA</keyword><keyword>BRITAIN</keyword><keyword>SWEDEN</keyword><keyword>ECHOLOCATION</keyword><keyword>POPULATIONS</keyword><keyword>BEHAVIOR</keyword></keywords><dates><year>2006</year><pub-dates><date>Aug</date></pub-dates></dates><isbn>1367-9430</isbn><accession-num>ISI:000239112600006</accession-num><urls><related-urls><url><Go to ISI>://000239112600006 </url></related-urls></urls></record></Cite></EndNote>[37]. In fragmented landscapes, birds and bats often then move between isolated discrete patches of suitable habitat or food sources ADDIN EN.CITE <EndNote><Cite><Author>Lawton</Author><Year>2010</Year><RecNum>4248</RecNum><DisplayText>[38]</DisplayText><record><rec-number>4248</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">4248</key></foreign-keys><ref-type name="Report">27</ref-type><contributors><authors><author>Lawton, J.H., Brotherton, P.N.M., Brown, V.K., Elphick, C., Fitter, A.H., Forshaw, J., </author><author>Haddow, R.W., Hilborne, S., Leafe, R.N., Mace, G.M., Southgate, M.P., Sutherland, W.A., </author><author>Tew, T.E., Varley, J., & Wynne, G.R. </author></authors><tertiary-authors><author>Defra</author></tertiary-authors></contributors><titles><title>Making Space for Nature: a review of England’s wildlife sites and ecological network. </title></titles><dates><year>2010</year></dates><pub-location>UK</pub-location><publisher>Defra</publisher><urls></urls></record></Cite></EndNote>[38], such as gardens and farms, enabling the further dispersal of AMR. Ever more powerful and accurate electronic tracking devices and spatial modelling approaches provide the potential to map the movements of animals in both space and time relative to potential sources of AMR pollution and points of contact with humans and livestock ADDIN EN.CITE <EndNote><Cite><Author>Craft</Author><Year>2011</Year><RecNum>4695</RecNum><DisplayText>[39]</DisplayText><record><rec-number>4695</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">4695</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Craft, Meggan E.</author><author>Caillaud, Damien</author></authors></contributors><titles><title>Network Models: An Underutilized Tool in Wildlife Epidemiology?</title><secondary-title>Interdisciplinary Perspectives on Infectious Diseases</secondary-title></titles><periodical><full-title>Interdisciplinary Perspectives on Infectious Diseases</full-title></periodical><pages>12</pages><volume>2011</volume><dates><year>2011</year></dates><urls><related-urls><url>;[39]. By combining a range of tools including mark-recapture methods, epidemiological modelling, molecular sequencing, behavioural observations and high tech devices such as GPS trackers, we can start to test empirically hypotheses concerning the dissemination of AMR by wildlife.Consequences of AMR for wildlife The consequences for wildlife of the evolution of AMR in commensal, or even pathogenic, bacteria are untested ADDIN EN.CITE <EndNote><Cite><Author>Albrechtova</Author><Year>2014</Year><RecNum>5082</RecNum><DisplayText>[36]</DisplayText><record><rec-number>5082</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">5082</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Albrechtova, Katerina</author><author>Papousek, Ivo</author><author>De Nys, Helene</author><author>Pauly, Maude</author><author>Anoh, Etile</author><author>Mossoun, Arsene</author><author>Dolejska, Monika</author><author>Masarikova, Martina</author><author>Metzger, Sonya</author><author>Couacy-Hymann, Emmanuel</author><author>Akoua-Koffi, Chantal</author><author>Wittig, Roman M.</author><author>Klimes, Jiri</author><author>Cizek, Alois</author><author>Leendertz, Fabian H.</author><author>Literak, Ivan</author></authors></contributors><titles><title>Low Rates of Antimicrobial-Resistant Enterobacteriaceae in Wildlife in Tai National Park, Cote d'Ivoire, Surrounded by Villages with High Prevalence of Multiresistant ESBL-Producing Escherichia coli in People and Domestic Animals</title><secondary-title>Plos One</secondary-title></titles><periodical><full-title>Plos One</full-title></periodical><volume>9</volume><number>12</number><dates><year>2014</year><pub-dates><date>Dec 4</date></pub-dates></dates><isbn>1932-6203</isbn><accession-num>WOS:000346382500084</accession-num><urls><related-urls><url><Go to ISI>://WOS:000346382500084</url></related-urls></urls><custom7>e113548</custom7><electronic-resource-num>10.1371/journal.pone.0113548</electronic-resource-num></record></Cite></EndNote>[36], but probably small. The clinical issue with AMR in both human and livestock populations is not that it causes disease but that it threatens the ability to treat infections diseases with antimicrobials, a practice rare in wild-living populations. AMR could compromise the treatment of individual wild animals in captivity, e.g. in wildlife hospitals, or of highly managed populations , especially those immuno-compromised due to low genetic diversity (e.g. ADDIN EN.CITE <EndNote><Cite><Author>Morris</Author><Year>2013</Year><RecNum>3861</RecNum><DisplayText>[41]</DisplayText><record><rec-number>3861</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">3861</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Morris, Katrina</author><author>Austin, Jeremy J.</author><author>Belov, Katherine</author></authors></contributors><titles><title>Low major histocompatibility complex diversity in the Tasmanian devil predates European settlement and may explain susceptibility to disease epidemics</title><secondary-title>Biology Letters</secondary-title></titles><periodical><full-title>Biology Letters</full-title></periodical><volume>9</volume><number>1</number><dates><year>2013</year><pub-dates><date>February 23, 2013</date></pub-dates></dates><urls><related-urls><url> </url></related-urls></urls><electronic-resource-num>10.1098/rsbl.2012.0900</electronic-resource-num></record></Cite></EndNote>[41]). 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ADDIN EN.CITE.DATA [42].The biggest issue for wildlife populations is the management response should they be thought to be significant sources of AMR for humans or livestock (see also Table 2). The control of wildlife infections transmissible to humans and livestock relies on three main approaches – separation of, or at least reducing contact with, the wildlife source, vaccination, and wildlife population control, often by culling. Vaccination is not possible for AMR control, and the physical separation of wildlife from livestock is difficult, expensive and, except very locally (e.g. keeping rodents or birds out of feed stores) impracticable. Protecting the human food chain from AMR is important but challenging given that wild game, seafood and bushmeat are important both nutritionally and culturally in many human societies ADDIN EN.CITE <EndNote><Cite><Author>Greig</Author><Year>2015</Year><RecNum>5076</RecNum><DisplayText>[4]</DisplayText><record><rec-number>5076</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">5076</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Greig, J.</author><author>Rajic, A.</author><author>Young, I.</author><author>Mascarenhas, M.</author><author>Waddell, L.</author><author>LeJeune, J.</author></authors></contributors><titles><title>A Scoping Review of the Role of Wildlife in the Transmission of Bacterial Pathogens and Antimicrobial Resistance to the Food Chain</title><secondary-title>Zoonoses and Public Health</secondary-title></titles><periodical><full-title>Zoonoses and Public Health</full-title></periodical><pages>269-284</pages><volume>62</volume><number>4</number><dates><year>2015</year><pub-dates><date>Jun</date></pub-dates></dates><isbn>1863-1959</isbn><accession-num>WOS:000353055100004</accession-num><urls><related-urls><url><Go to ISI>://WOS:000353055100004</url></related-urls></urls><electronic-resource-num>10.1111/zph.12147</electronic-resource-num></record></Cite></EndNote>[4]. Furthermore, control and mitigation measures such as improved hygiene and restriction on movements cannot be easily implemented, if at all, for free living animals. For logistical, economic, historical and cultural reasons, culling is often the approach taken: however, the efficacy and efficiency of culling wildlife in controlling disease are at best controversial. Research and policy prioritiesWildlife clearly is shedding and therefore able to transport AMR PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5HcmVpZzwvQXV0aG9yPjxZZWFyPjIwMTU8L1llYXI+PFJl
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ADDIN EN.CITE.DATA [2, 4]. However, few studies have identified the likely selection factors (including, but not necessarily limited to, sources of antimicrobial exposure), origins of the resistance genes, or, importantly, the direction of transmission. Studying infection transmission in wildlife poses a number of challenges, particularly for a complex issue such as AMR that is present in, and can move between, multiple bacterial taxa in multiple hosts and the environment. Approaches used to study and control AMR transmission in the clinical setting are challenging to apply to wildlife systems. Contact between wildlife and sources of AMR and/or antimicrobials often cannot be measured directly but need to be inferred, for example from molecular ‘fingerprints’ of specific contamination. This can be supplemented with behavioural observations and electronic tracking devices fitted to wild animals. Interventions that minimise and mitigate the transmission of AMR from livestock or human populations to wildlife need researching alongside investigation of the risk itself, in order to develop both evidence-based and proportionate protocols and policies (Table 2). Pollution control and sewage treatment are likely priority areas for such research, particular in countries with few controls on either antibiotic usage or release of untreated wastes (which includes both developed and developing countries). Meanwhile ecologists studying wild populations, along with wildlife hospitals and existing programmes designed to monitor pollution, poisoning and diseases in wildlife (e.g. WILDCOMS ADDIN EN.CITE <EndNote><Cite><Author>Pereira</Author><Year>2015</Year><RecNum>5161</RecNum><DisplayText>[43]</DisplayText><record><rec-number>5161</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">5161</key></foreign-keys><ref-type name="Report">27</ref-type><contributors><authors><author>Pereira, M. Gloria</author><author>Chaplow, J.S.; </author><author>Shore Richard F.</author></authors></contributors><titles><title>WILDCOMS (Wildlife Disease & Contaminant Monitoring and Surveillance network) annual report 2013-2014</title></titles><pages>19</pages><number> CEH Project no. C04373</number><dates><year>2015</year></dates><pub-location>Lancaster, UK, </pub-location><publisher>NERC/Centre for Ecology & Hydrology</publisher><urls></urls></record></Cite></EndNote>[43]), might be recruited to collect samples for surveillance. This last approach might be particularly useful in identifying species, key individuals within populations or spatial locations that are ‘super spreaders’ of AMR transmission and could be targeted for focused surveillance, control or mitigation measures ADDIN EN.CITE <EndNote><Cite><Author>Craft</Author><Year>2011</Year><RecNum>4695</RecNum><DisplayText>[39]</DisplayText><record><rec-number>4695</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">4695</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Craft, Meggan E.</author><author>Caillaud, Damien</author></authors></contributors><titles><title>Network Models: An Underutilized Tool in Wildlife Epidemiology?</title><secondary-title>Interdisciplinary Perspectives on Infectious Diseases</secondary-title></titles><periodical><full-title>Interdisciplinary Perspectives on Infectious Diseases</full-title></periodical><pages>12</pages><volume>2011</volume><dates><year>2011</year></dates><urls><related-urls><url>;[39]. It is important to study AMR in wildlife as a potential hazard to human health and food security, especially given that about 40% of emerging human diseases are thought to have originated in wildlife ADDIN EN.CITE <EndNote><Cite><Author>Jones</Author><Year>2008</Year><RecNum>4696</RecNum><DisplayText>[1]</DisplayText><record><rec-number>4696</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">4696</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Jones, Kate E.</author><author>Patel, Nikkita G.</author><author>Levy, Marc A.</author><author>Storeygard, Adam</author><author>Balk, Deborah</author><author>Gittleman, John L.</author><author>Daszak, Peter</author></authors></contributors><titles><title>Global trends in emerging infectious diseases</title><secondary-title>Nature</secondary-title></titles><periodical><full-title>Nature</full-title></periodical><pages>990-993</pages><volume>451</volume><number>7181</number><dates><year>2008</year><pub-dates><date>02/21/print</date></pub-dates></dates><publisher>Nature Publishing Group</publisher><isbn>0028-0836</isbn><work-type>10.1038/nature06536</work-type><urls><related-urls><url>;[1]. Tropical ecosystems and areas in which humans live close to both livestock and wildlife are likely to present heightened, but to date poorly studied, risks for the evolution and transmission of AMR by wildlife (Table 2). Furthermore, studies of AMR in wildlife can have wider impact than simply public health risk. First, by stepping outside of the 'blame game' of livestock, veterinary and medical systems they can elucidate fundamental issues in the evolution and transmission ecology of antimicrobial resistant bacteria and resistance determinants that can be applied back into more clinical settings. Second, a better understanding of the role of wildlife in AMR dissemination should help us decide if control and mitigation strategies are required and where best to apply them. Finally, while wildlife might be long distance dispersers of AMR, they may also be sentinels for the abundance and distribution of pathogen pollution in our environment.EthicsAll work carried out conformed to the legal requirements of the country in which the work was carried out and to all institutional peting InterestsWe have no competing interests.Authors’ contributionsAll authors contributed to the writing of this review and gave final approval for publication.AcknowledgementsThank you to D. Graham for discussions about AMR and to L. Al Meslati for permission to reproduce a figure and part of a table from his PhD thesis. Some of the data shown in figure 2 and table 1 were collected through Defra-funded research projects.FundingNo specific funding was provided for the preparation of this paper.References ADDIN EN.REFLIST [1] Jones, K.E., Patel, N.G., Levy, M.A., Storeygard, A., Balk, D., Gittleman, J.L. Daszak, P. 2008 Global trends in emerging infectious diseases. 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Birmingham, BRITISH SOCIETY OF ANTIMICROBIAL CHEMOTHERAPY Figure and Table CaptionsFigure 1: Dispersal of AMR across the landscape: between human communities, hospitals, sewage treatment plants (STPs), farms and the wider environment including via wildlife (Modified from [6]). Figure 2: Antimicrobial resistance in wildlife on dairy farms in Cheshire, UK. The resistance patterns of E.coli from the faeces of cattle, rodents (mainly Myodes glaroelus and Apodemus sylvaticus), wild birds (mainly passerines) and other wild mammals (mainly badgers and foxes) were compared: 1A) Percentage of faecal samples containing E. coli resistant to at least one antibiotic on five different farms (A-F). 1B ) Percentage of E. coli isolated from each group of animals resistant to various antibiotics or multidrug resistant. Resistance to the following antibiotics was tested: ampicillin (amp), chloramphenicol (chl), tetracycline (tet), trimethoprim (trm) and nalidixic acid (nal) and also *MDR (defined as resistance to three or more of the antibiotics tested). All susceptibility testing was performed according to the British Society of Antimicrobial Chemotherapy guidelines ADDIN EN.CITE <EndNote><Cite><Author>Anon</Author><Year>2007</Year><RecNum>5143</RecNum><DisplayText>[44]</DisplayText><record><rec-number>5143</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">5143</key></foreign-keys><ref-type name="Standard">58</ref-type><contributors><authors><author>Anon</author></authors></contributors><titles><title>BSAC Methods for Antimicrobial Susceptibility Testing (Version 6.1)</title></titles><dates><year>2007</year></dates><pub-location>
Birmingham</pub-location><publisher>BRITISH SOCIETY OF ANTIMICROBIAL CHEMOTHERAPY </publisher><urls><related-urls><url>;[44]. Figure modified from ADDIN EN.CITE <EndNote><Cite><Author>Al-Tunesi</Author><Year>2009</Year><RecNum>5142</RecNum><DisplayText>[31]</DisplayText><record><rec-number>5142</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">5142</key></foreign-keys><ref-type name="Thesis">32</ref-type><contributors><authors><author>Al-Tunesi, Lutfi Abdelhamid</author></authors></contributors><titles><title>Prevalence of antibiotic-resistant Escherichia coli in faecal samples from domestic animals and wildlife : a cross-sectional study</title><secondary-title>Veterinary Pathology</secondary-title></titles><volume>Thesis Ph.D.</volume><dates><year>2009</year></dates><publisher>University of Liverpool</publisher><urls></urls></record></Cite></EndNote>[31].Table 1: Antimicrobial resistant E. coli in the faeces of wild rodents collected at sites in the UK varying in predicted exposure to livestock treated with antimicrobial drugs. Resistance to six antibiotics (ampicillin (amp), apramycin (apr), chloramphenicol (chl), tetracycline (tet), trimethoprim (trm) and nalidixic acid (nal)) was investigated ADDIN EN.CITE <EndNote><Cite><Author>Anon</Author><Year>2007</Year><RecNum>5143</RecNum><DisplayText>[44]</DisplayText><record><rec-number>5143</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">5143</key></foreign-keys><ref-type name="Standard">58</ref-type><contributors><authors><author>Anon</author></authors></contributors><titles><title>BSAC Methods for Antimicrobial Susceptibility Testing (Version 6.1)</title></titles><dates><year>2007</year></dates><pub-location>
Birmingham</pub-location><publisher>BRITISH SOCIETY OF ANTIMICROBIAL CHEMOTHERAPY </publisher><urls><related-urls><url>;[44]. Modified from ADDIN EN.CITE <EndNote><Cite><Author>Al-Tunesi</Author><Year>2009</Year><RecNum>5142</RecNum><DisplayText>[31]</DisplayText><record><rec-number>5142</rec-number><foreign-keys><key app="EN" db-id="5pwxf2a0pvwaadea9zs55tp2a5awxaxsxpv9">5142</key></foreign-keys><ref-type name="Thesis">32</ref-type><contributors><authors><author>Al-Tunesi, Lutfi Abdelhamid</author></authors></contributors><titles><title>Prevalence of antibiotic-resistant Escherichia coli in faecal samples from domestic animals and wildlife : a cross-sectional study</title><secondary-title>Veterinary Pathology</secondary-title></titles><volume>Thesis Ph.D.</volume><dates><year>2009</year></dates><publisher>University of Liverpool</publisher><urls></urls></record></Cite></EndNote>[31] Table 2: Summary of some of the key outstanding questions, mitigation measures and research approaches regarding the role of wildlife in the transmission of AMR based on the literature reviewed. Suggested research approaches draw on diverse disciplines including ecology, veterinary science and the social sciences. ................
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