Antimicrobial Resistance in the Environment

603 Pages·2012·5.77 MB·English

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
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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
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Patricia dedicates this book to the memory of her parents
Leonard Percy Keen
Margaret Ada Prescott Keen
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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
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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
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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
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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
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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
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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