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ANTIMICROBIAL RESISTANCE IN THE ENVIRONMENT ffirs 17November2011;11:10:34 ANTIMICROBIAL RESISTANCE IN THE ENVIRONMENT EDITED BY PATRICIA L. KEEN University of British Columbia Vancouver, British Columbia, Canada MARK H. M. M. MONTFORTS National Institute for Public Health and the Environment, Bilthoven, The Netherlands ffirs 17November2011;11:10:34 Copyrightr2012byWiley-Blackwell.Allrightsreserved. PublishedbyJohnWiley&Sons,Inc.,Hoboken,NewJersey PublishedsimultaneouslyinCanada Nopartofthispublicationmaybereproduced,storedinaretrievalsystem,ortransmittedinanyform orbyanymeans,electronic,mechanical,photocopying,recording,scanning,orotherwise,exceptas permittedunderSection107or108ofthe1976UnitedStatesCopyrightAct,withouteithertheprior writtenpermissionofthePublisher,orauthorizationthroughpaymentoftheappropriateper-copyfeeto theCopyrightClearanceCenter,Inc.,222RosewoodDrive,Danvers,MA01923,(978)750-8400,fax(978) 750-4470,oronthewebatwww.copyright.com.RequeststothePublisherforpermissionshouldbe addressedtothePermissionsDepartment,JohnWiley&Sons,Inc.,111RiverStreet,Hoboken,NJ07030, (201)748-6011,fax(201)748-6008,oronlineathttp://www.wiley.com/go/permission. LimitofLiability/DisclaimerofWarranty:Whilethepublisherandauthorhaveusedtheirbesteffortsin preparingthisbook,theymakenorepresentationsorwarrantieswithrespecttotheaccuracyor completenessofthecontentsofthisbookandspecificallydisclaimanyimpliedwarrantiesofmerchant- abilityorfitnessforaparticularpurpose.Nowarrantymaybecreatedorextendedbysalesrepresentatives orwrittensalesmaterials.Theadviceandstrategiescontainedhereinmaynotbesuitableforyour situation.Youshouldconsultwithaprofessionalwhereappropriate.Neitherthepublishernorauthor shallbeliableforanylossofprofitoranyothercommercialdamages,includingbutnotlimitedtospecial, incidental,consequential,orotherdamages. Forgeneralinformationonourotherproductsandservicesorfortechnicalsupport,pleasecontactour CustomerCareDepartmentwithintheUnitedStatesat(800)762-2974,outsidetheUnitedStatesat(317) 572-3993orfax(317)572-4002. Wileyalsopublishesitsbooksinavarietyofelectronicformats.Somecontentthatappearsinprintmay notbeavailableinelectronicformats.FormoreinformationaboutWileyproducts,visitourwebsiteat www.wiley.com. LibraryofCongressCataloging-in-PublicationData: Antimicrobialresistanceintheenvironment/PatriciaL.Keen&MarkH.M.M.Montforts,editors p. cm. Includesindex. ISBN978-0-470-90542-5(hardback) 1. Antibiotics–Environmentalaspects. 2. Drugresistanceinmicroorganisms. I. Keen,Patricia L. II. Montforts,M.H.M.M.(MarkH.M.M.) TD196.D78A582012 572.8u44–dc23 2011022714 PrintedintheUnitedStatesofAmerica 10 9 8 7 6 5 4 3 2 1 ffirs 17November2011;11:10:34 Patricia dedicates this book to the memory of her parents Leonard Percy Keen Margaret Ada Prescott Keen ffirs 17November2011;11:10:34 CONTENTS PREFACE xi CONTRIBUTORS xv PART I SOURCES 1 Chapter 1 Introduction 3 StuartB.Levy Chapter 2 Path to Resistance 7 VivianMiao,DorothyDavies,andJulianDavies Chapter 3 Antibiotic Resistome: A Framework Linking the Clinic and the Environment 15 GerardD.Wright Chapter 4 Ecological and Clinical Consequences of Antibiotic Subsistence by Environmental Microbes 29 GautamDantasandMortenO.A.Sommer Chapter 5 Importance of Adaptive and Stepwise Changes in the Rise and Spread of Antimicrobial Resistance 43 LuciaFernandez,ElenaB.M.Breidenstein,andRobertE.W.Hancock Chapter 6 Environmental Reservoirs of Resistance Genes in Antibiotic- Producing Bacteria and Their Possible Impact on the Evolution of Antibiotic Resistance 73 ParisLaskaris,WilliamH.GazeandElizabethM.H.Wellington vii ftoc 17November2011;15:29:1 viii CONTENTS Chapter 7 Mechanisms of Bacterial Antibiotic Resistance and Lessons Learned from Environmental Tetracycline-Resistant Bacteria 93 MarilynC.Roberts Chapter 8 Environmental Antibiotic Resistome: New Insights from Culture-Independent Approaches 123 IsabelS.Henriques,ArturAlves,MariaJose´Saavedra, MarkH.M.M.Montforts,andAnto´nioCorreia PART II FATE 149 Chapter 9 Environmental Pollution by Antibiotic Resistance Genes 151 JoseLuisMartinezandJorgeOlivares Chapter 10 Quantifying Anthropogenic Impacts on Environmental Reservoirs of Antibiotic Resistance 173 AmyPrudenandMazdakArabi Chapter 11 Antibiotic Resistance in Swine-Manure-Impacted Environments 203 JoanneChee-Sanford,ScottMaxwell,KristyTsau, KellyMerrick,andRustamAminov Chapter 12 Antimicrobial-Resistant Indicator Bacteria in Manure and the Tracking of Indicator Resistance Genes 225 ChristinaS.Ho¨lzelandKarinSchwaiger Chapter 13 Municipal Wastewater as a Reservoir of Antibiotic Resistance 241 TimothyLaparaandTuckerBurch Chapter 14 Strategies to Assess and Minimize the Biological Risk of Antibiotic Resistance in the Environment 251 ThomasSchwartz Chapter 15 Antibiotic Resistance in Animals—The Australian Perspective 265 OlasumboNdiandMaryBarton PART III ANTIMICROBIAL SUBSTANCES AND RESISTANCE 291 Chapter 16 Detection and Occurrence of Antibiotics and Their Metabolites in Pig Manure in Bavaria (Germany) 293 KatrinHarmsandJohannBauer Chapter 17 Fate and Transport of Antibiotics in Soil Systems 309 AlistairB.A.Boxall Chapter 18 Antibiotics in the Aquatic Environment 325 KlausKu¨mmerer Chapter 19 Residues of Veterinary Drugs in Wild Fish 337 ThomasHeberer ftoc 17November2011;15:29:1 CONTENTS ix Chapter 20 Role of Quaternary Ammonium Compounds on Antimicrobial Resistance in the Environment 349 UlasTezelandSpyrosG.Pavlostathis PART IV EFFECTS AND RISKS 389 Chapter 21 Human Health Importance of use of Antimicrobials in Animals and Its Selection of Antimicrobial Resistance 391 ScottA.McEwen Chapter 22 Antimicrobial Resistance Associated with Salmonid Farming 423 ClaudioD.Miranda Chapter 23 Effect of Veterinary Medicines Introduced via Manure into Soil on the Abundance and Diversity of Antibiotic Resistance Genes on Their Transferability 453 HolgerHeuer,ChristophKopmann,UteZimmerling, EllenKro¨gerrecklenfort,KristinaKleineidamm,MichaelSchloter, EvaM.TopandKorneliaSmalla Chapter 24 Tracking Antibiotics and Antibiotic Resistance Genes through the Composting Process and Field Distribution of Poultry Waste: Lessons Learned 465 PatriciaL.KeenandNancyDeWith Chapter 25 Environmental Microbial Communities Living Under Very High Antibiotic Selection Pressure 483 AndersJanzon,ErikKristiansson,andD.G.JoakimLarsson Chapter 26 Antibiotic Use During an Influenza Pandemic: Downstream Ecological Effects and Antibiotic Resistance 503 AndrewC.SingerandHeikeSchmitt Chapter 27 Use of Veterinary Antibacterial Agents in Europe and the United States 539 IngeborgM.vanGeijlswijk,NicoBondt,LindaF.Puister-Jansen, andDikJ.Mevius Chapter 28 Regulatory Research on Antimicrobial Resistance in the Environment 549 EmilyA.McVeyandMarkH.M.M.Montforts INDEX 569 ftoc 17November2011;15:29:1 PREFACE ItbeganwithBordeaux.Yes,thewineandyesthefabulouscityinFrance.Theeighth annualmeetingoftheSocietyofEnvironmentalChemistryandToxicologywasheld in the spring of 1998 in Bordeaux. Keen and Montforts met each other over a glass of Me´doc (or was it the Graves?) at the opening wine-tasting social. As environ- mental professionals and, at the same time, students with a common research focus of veterinary antibiotics as pollutants in the environment, the idea for this book germinated at that very first meeting. Early in our respective academic careers, we were inspired by some of the world’s leading scientific authorities on antibiotics andantimicrobialresistance.Withtime,ourrespectiveacademicjourneystooktheir course, but the bond that formed during the conversations commiserating over thetrialsandtribulationsofadoctoralstudyprogram,eventuallymorphedintothe shared vision to edit a unique book on the subject of our prime research interest. The past decade has witnessed the sustained growth of concern in the scientific communityandthegeneralpublicregardingthedevelopmentofantibioticresistance in bacteria. It is now well accepted that exposure of nontarget microorganisms to antibiotics as a result of human activities can promote resistance in pathogens that cancompromisetheefficacyofhumanandveterinarymedicine.Healthconsequences of exposure to methicillin-resistant Staphylococcus aureus (MRSA) and other Superbugs now receive regular media attention worldwide, and there is much concern that a portion of the arsenal of antibiotic drugs are losing their ability to successfully combat many critical bacterial infections. There are increasingly frequent reports of scientific evidence that underlines the importance of environ- mental transport pathways for distribution of antimicrobial-resistant bacteria via surface water, drinking water, and stream networks. The spread of antibiotic resistance in the environment depends on the presence andtransferofresistanceelementsamongmicroorganisms,onthegeneticmutations thatresult,andontheselectionpressuretoretainthesegeneswithinthepopulation. In essence, all substances can act as antibiotics—the distinction between those xi fpref 17November2011;12:32:41 xii PREFACE substances that can be classified as antibiotics and those that act as signaling moleculesisgovernedbythedose.Antibioticresistancegenesareclearlyrecognized aspotential environmental contaminants.The problem,however,withassessing the relative contribution of antibiotic resistance as contaminants is that the complexity and adaptive behavior of bacterial communities in natural ecosystems is not well understood. This intersection of human health risk assessment with ecological and environmental research and risk assessment is becoming more and more evident. There has been a fundamental shift in thought regarding the role of the environ- mentinthespreadofantimicrobialresistanceamongmicroorganisms.Theperceived boundary between an “ecosystem-based approach” and a “human-health-centered approach” to characterizing antimicrobial resistance as a health risk has somewhat dissolved. The sometimes independent and sometimes overlapping processes in ecosystemsserveasbothadistributionnetworkandapotentialsourceforthestressors that expose a broad range of microorganism species to antibiotics and antibiotic resistance genetic elements. This duality of the environmental role is an important considerationinthespreadofantibioticresistancegiventhattheresistancemechan- isms in some soil-dwelling microorganism mimic those seen in clinically relevant bacteria. The conceptual reference point of “environment” in exploring the health risk associated with development of antibiotic resistances in organism has expanded. Gradually, the process for risk assessment of health consequences related to developmentofantimicrobialresistanceinbacteriaviamultiplepathwaysisadapting to incorporate variability in temporal and spatial scales in the overall evaluation of the risk. The awareness of the importance of antimicrobial resistance as a health risk extends beyond the association with exposures to antimicrobial drugs. For example, the ever-improving biotechnological capabilities in manipulation at the geneticlevelallowtheinsertionofantibioticresistancemarkersintransgenicplants. Thishasimportantimplicationsforintroducingopportunitiesforbi-directionalgene flow among soil-dwelling microbes for which the role of antibiotic resistance in the naturalecosystem remainsincompletely understood.Recent studiesoftheeffects of antimicrobial properties associated with nanoparticles are also providing evidence that nanotechnology may offer some improvement in treatment of infections. Although several research teams are investigating the environmental risks linked to antibioticresistancegenesasmakersintransgenicorganismsandtheimplicationsfor antimicrobial resistance related to use of engineered nanoparticles, these issues are not discussed specifically in this volume. The overarching theme of this book is that the environment plays a crucial role in the development of antibiotic resistance traits in bacteria and the distribution of antibiotic-resistant microbial species, resistant genetic material, and antibiotic compounds. Resistance genes appear to be everywhere in nature—in pathogens, commensals, and environmental microorganisms. We invite you to gain a broader insight ofthe role oftheenvironmentinthemechanismsofresistance development, the dissemination of antimicrobial-resistant genetic elements, and the transport of antibioticresistancegenesorantibioticsasenvironmentalcontaminantsthroughthe presentations of our contributing authors in this book. Wewouldliketoexpressoursinceregratitudetoourcolleaguesfortheirfantastic contributionstothecreationofthisbook.Weappreciatethehardwork,thepatience, andthefriendshipthatwehavesharedwiththiscommunityofresearchersduringthe fpref 17November2011;12:32:41 PREFACE xiii completionofthebookproject.Aswell,therearemanyindividualswewishtothank for enabling its completion. The team at Wiley(cid:2)Blackwell led by Karen Chambers and Anna Ehler have guided us through this evolutionary process with understand- ing and finesse—for this we are very grateful. Patricia owes many thanks to several special friends and colleagues who have providedtheirsupportthroughoutthisprocess:CharlesKnapp,TeresaFrolek,Lisa Waddell, Debbie Angel, Marco Solinas, Annette Muttray, Heather Slater, David Brownstein, May du Monceau, Katia Freire, Charlene Knapp, Agnes MacDonald, PabloTrujillo,andJesseRead.PatriciaalsothanksherdoctoralsupervisorKenHall and the other members of her research committee, David Graham, Pierre Be´rube´, Les Lavkulich, and Bob Hancock, for their inspiration in the preparation of this book. Raphae¨l Fuge`re has played important roles in this project as well that have ranged from providing sympathetic critical review to volunteering his technical assistance in field sampling. None of this enterprise could be possible without the unfailing encouragement, patience, love, and technical support of Steve Clark. Thank you. PatriciaisparticularlygratefultoDanielPaulyandRashidSumailaandmanyof the fabulous researchers at the University of British Columbia Fisheries Centre for their kindness and support during the time she has shared with them as a visiting scholar. As artists, researchers, teachers, and, of course, friends, Belidson Dias and PhilippeRaphanelarePatricia’sever-growinginspiration,andweofferourthanksto PhilippeRaphanel fortheuseofhispaintingonthecover.Thespecialinfluencesof Henk de Wit and Ge´rard Faisandier are forever metaphorically etched in the conceptual foundations of most of Patricia’s scholarly and creative endeavors. Markwishestoacknowledgethesupport,critiques,and/orinspirationhereceived from Heike Schmitt, Bent Halling-Sørensen, Tore Midtvedt, Gerard Rijs, Hans Mensink (y), Han de Neeling, Ana Maria de Roda Husman, Saskia Rutjes, Hetty Blaak, Caroline Moermond, Jan Roels, Charles Bodar, Bart Hellings, Sybrand Landman, and literally last but certainly not least, Emily McVey. fpref 17November2011;12:32:41

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Examines effects of the environmental distribution of antimicrobial resistance genes on human health and the ecosystemResistance genes are everywhere in nature?in pathogens, commensals, and environmental microorganisms. This contributed work shows how the environment plays a pivotal role in the deve
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