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    Zoonoses(Project1)

    Wildlife/domesticlivestockinteractions

    AfinalreporttotheDepartmentforInternationalDevelopment,UK

    Submittedby:

    TheInternationalLivestockResearchInstitute,Nairobi

    &

    RoyalVeterinaryCollege,London

    Reporteditors:DeliaGraceandBryonyJones

    Reportauthors1

    BryonyJones DeclanMcKeever DeliaGrace DirkPfeiffer FlorenceMutua JemimahNjuki JohnMcDermott JonathanRushton MohamedSaid PollyEricksen RichardKock SilviaAlonso(Researchassistants:JarrahYoungandPernillevanGrieken)

    Date:

    September25th

    2011

    1Inalphabeticalorderoffirstname

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    Contents

    1. Executivesummary............................................................................................................................3

    2. Methodology....................................................................................................................................11

    3. Importanceofzoonosesandthelivestockwildlifeinterface..........................................................15

    4. Mappingzoonosesatthelivestockwildlifeinterface.....................................................................26

    5. Diseasetransmissionroutesandtherelativeimportanceofthewildlifelivestockroute..............33

    6. Pathogensofwildlifecapableofrecombiningwithanalogousorganismsindomesticlivestock...41

    7. Riskfactorsfordiseasetransmissionfromwildordomesticanimalstopeopleandbetween

    wildlifeanddomesticlivestock.............................................................................................................51

    8. Driversinfluencingtheinteractionbetweenwildlifeandlivestockandtheimplicationsfor

    zoonosestransmission..........................................................................................................................58

    9. Historicalchangesintransmission,factorswhichfosternoveltransmissionroutesandhosts,and

    wildanimalcandidatesforfuturediseasetransmission......................................................................68

    10. Keyfactorsinfluencingtheriskofthetransferofinfectionsbetweenlivestockandwildlifein

    developingcountries:productionandsocioeconomicfactors...........................................................88

    11. Managementofzoonosesatthelivestockwildlifeinterface........................................................95

    References..........................................................................................................................................111

    Annex1.AssumptionsaroundDALYcalculations...............................................................................126

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    1. Executivesummary

    Theobjectiveofthisstudywastosynthesisethebestavailablescientificknowledgeaboutzoonotic

    diseasetransmissionthroughlivestockandwildlifeinteraction(directorindirect),withemphasison

    risk factors, drivers and trajectories of transmission, as well as promising interventions for

    controllingimportantzoonoses,basedonmanagingtheinteractionbetweendomesticlivestockand

    wildlife.

    Amultidisciplinaryteam fromthe InternationalLivestockResearchInstitute,Kenya,andtheRoyal

    VeterinaryCollege,UnitedKingdom,withexpertiseinzoonoses,epidemiology,socioeconomics,and

    wildlife,undertookthereview.Adatabaseofimportantzoonoseswascompiledandusedtodevelop

    a list of priority zoonoses with a livestockwildlife interface for developing countries. Spatial

    relationships between important zoonoses and land use and human population density were

    explored.Asystematicreviewwascarriedout focussingon:diseasetransmissionroutes,riskfactors

    fordisease transmission,driversofwildlifelivestock interactions,pathogensofwildlifecapableofrecombining with organisms in livestock, wildlife species that are potential sources of zoonotic

    pathogens, production and socioeconomic factors influencing the risk of transmission, and risk

    management and control interventions. The main findings are summarized in this executive

    summary.

    Zoonosescanbebroadlydefinedasdiseasesthatarenaturallytransmissiblebetweenanimalsand

    people.Zoonosesareofconcernfortwomainreasons;thehealthandeconomicburdenscausedby

    zoonoseslongknowntocausediseaseinanimalsandpeoplethatpersist invulnerablegroups,and

    the potential for emerging zoonoses to give rise to novel disease outbreaks. The burden of

    persisting

    zoonoses

    is

    mainly

    borne

    by

    poor

    people

    in

    developing

    countries,

    whilst

    emerging

    zoonosesareofmoreconcerntotherichindevelopedcountrieswithlargereconomiesandfewer

    otherinfectiousdiseaseproblems.

    Aszoonosesarebydefinition transmissiblebetweenanimalsandhumans, it isnotsurprising that

    most are also transmissible between wildlife and domestic animals. Transmission depends upon

    contact (direct or indirect) between livestock, domestic animals and people and transmission

    opportunities are subject to various, sometimes opposing drivers. The unprecedentedly large

    human population and the associated increases in demand for land, food (and use of natural

    resourcesistherootcauseofincreasedtransmissionopportunities.However,developedcountries

    havehighanimalandhumanpopulationsbutzoonosesareoflowhealthsignificancesuggestingthe

    high level of zoonoses in developing countries is not due to absolute population size but other

    factors. These could include the speed of increase in human and animal populations driving a

    livestock revolution2 with rapid yet poorlyregulated changes in livestockkeeping systems, and

    massiveintensificationinparallelwithcontinuedhighlevelsoflivestockownershipandclosecontact

    betweenhumansandlivestock.However,theorigin,distributionandimpactofemergingzoonoses

    islessskewedtowardspoorcountriesthanisthecaseforpersistingzoonoses.

    2TheLivestockRevolutionistherapid,demanddrivenincreaseinlivestockproductionandtradeindevelopingcountries.

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    Threeimportantproximaldriversofincreasedzoonosestransmissionandextensionofthelivestock

    wildlife interfacearerapidly increasing livestocktrade,agriculturalexpansionwith incursion into

    newareas,andculturalconsumptionpractices(especiallyconsumptionofbushmeatinAfricaand

    Asianforbuyingfromwetmarketsselling livedomesticanimalsandwildlife inAsia). Indeveloped

    countries,recreationandconservationcan leadto locally increasedriskbuttheassociateddisease

    burdenisnotimportantincomparisontoothercausesofsicknessanddeath.

    Agriculture intensification is not always a risk amplifier but the rapid and poorly regulated

    intensificationassociatedwiththelivestockrevolutionindevelopingcountries,is.Whileincreasing

    thenumbersof livestockkeptwillof itself increaserisk,theeffectsof intensificationare lessclear.

    Highlivestocknumbers,highstockingdensities,poorhusbandry,andinappropriateuseofantibiotics

    associated with intensification in developing countries all favour disease transmission and

    emergence. However, reductions in the proportion of the population keeping livestock,

    improvements inbiosecuritythatareeasierto implementandregulateon largefarms,andbetter

    surveillance and disease control are characteristics of agriculture intensification in developedcountries and are risk mitigating. On the other hand, the increasing genetic homogeneity of

    livestockassociatedwith intensification(monoculture) inbothdevelopedanddevelopingcountries

    isprobablyanimportantfactorinspreadandamplificationofdisease.

    For both persisting and emerging zoonoses, it appears that a broad range of pathogens can be

    acquiredfromamanydifferenthostsunderawiderangeofcontexts,whichmayormaynotinvolve

    awildlifelivestockinterface.Itisespeciallydifficulttomakepredictionsaboutthefewandunusual

    emergingpathogensthatgoontohavemassiveimpact.MadcowdiseaseinBritainsadvancedwell

    regulateddairy sector, SARS3with links towildlife inAsiasbusywetmarkets,avian influenza in

    intensiveand littleunderstoodproductionsystems inChina,andRiftValleyFeveremerging in low

    density,traditionallivestocksystemsinAfricahavefewcommonfeatures,althoughallfourdiseases

    havealivestockwildlifeinterface.Thedifficultyofgeneralisingfromsmallnumbersofcasesmeans

    that predicting high impact zoonoses is challenging. Nonetheless, some hotspots in terms of

    geographicareasandonestowatch intermsofpathogensandhostscanbetentativelyidentified

    andtheseshouldbesubjecttohighersurveillancealongwithevaluationofthecostsandbenefitsof

    thisrisktargeting.

    In developed countries, management of persisting and emerging zoonoses has been relatively

    successful (although often expensive). Successful control is less likely where wildlife have a

    substantialroleintransmission.Eliminationofwildlifepopulationsisgenerallynotafeasiblecontrol

    strategy; reducing wildlife numbers can be useful but smallscale and shortterm programs are

    generally ineffective andmaybeharmful;physical separationof livestock andwildlife isdifficult,

    expensiveandcanhaveunwantedsideeffects.Inpoorcountries,managementhasbeenmuchless

    successful.However, thehistorically recent,massive,unplanned reduction inwildlifepopulations

    especially inAfricanandSouthAmericahasaffectedzoonosesprevalence,positivelyornegatively

    dependingonthecontextandtemporalscale(ecosystemincursionoftenincreasesriskintheshort

    term,whiledecreasing in the long term).The major deficit in current management of zoonoses

    3SevereacuterespiratorysyndromeisarespiratorydiseaseinhumanswhichiscausedbytheSARScoronavirus

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    withalivestockwildlifeinterfaceisthatprogrammesarenotbasedonadequateepidemiological

    orsocioeconomicunderstanding.

    Inthenextsectionwesetoutthekeymessagesidentifiedbyexperts inthisstudyalongwiththeir

    strength of supporting evidence, and identify the associated evidence gaps and the possible

    contributionofresearch.Thequestionsarethosesetoutinthereviewtermsofreference.

    What is theextentof theproblemofzoonoses, the contextand the relative importanceof the

    wildlife/domesticlivestocktransmissionroute?

    Zoonoses are absolutely and relatively more important in lowincome countries compared tohighincomecountries(evidencestrong Chapter3).Inlowincomecountries,infectiousdiseases

    areresponsiblefornearly40%oftheburdenofhumansicknessanddeath,and onefifthofthisis

    attributable to zoonoses or diseases recently emerged from animals, with recently emerged

    disease (mainlyAIDS4)abouttwiceas importantaszoonoses (evidencemedium Chapter3). In

    highincomecountries, infectiousdiseasesaremuch less important (4%oftotalburden).Whilediseasesemergingrecentlyfromanimalsandfoodbornezoonosesareanimportantpartofthis

    smallburden,otherzoonoseshaveminor impacts(Evidencestrong Chapter3).Manyofthese

    zoonoses,inbothrichandpoorcountries,havealivestockwildlifeinterface.

    Thetotalimpactofzoonoseswithalivestockwildlifeinterface,goesfarbeyondhumansicknessanddeathandincludesmultipleotherburdens,suchas:monetarycostofillness;costtolivestock

    sector;opportunitycosttoeconomies;negativesocialandpsychological impacts;and,negative

    impactsonwildlifeandecosystems(Evidencestrong Chapter3).

    TheGlobalBurdenofDiseaseassessment ledbytheWorldHealthOrganisation(WHO)suggestsfoodbornezoonoses,humanAfricantrypanosomosisand leishmaniasisarethemost important

    zoonosesgloballyallhavealivestock/wildlifeinterface(evidencemedium Chapter3).

    Publishedexpertopinionconsidersbrucellosis,humanAfrican trypanosomosisandtuberculosisto be the most important zoonoses all have a livestock/wildlife interface (Evidence weak

    Chapter3).

    Inthestudyconductedforthisreport,weidentified292importantzoonosesfromtheliterature:82%ofthesehadawildlifereservoir,74%hadadomesticanimalreservoirand60%hadbotha

    wildlifeandadomesticanimalreservoir(Evidencemedium Chapter3).

    Keyevidencegaps:

    There isa lackofsystematicsurveillancedataforzoonoses ingeneral,andforzoonoseswithalivestockwildlife interface inparticular.Studiesareneededtodeterminepresence,prevalence,impactsandriskfactors.

    Thereislackofevidenceonthemultipleburdensofzoonoticdiseaseandmeasuringtheburdensand mapping the occurrence of zoonotic disease is a first step for prioritization and rational

    management inresourcescarcecontexts.Many importantzoonosesaremissingfromtheWHO

    GlobalDiseaseBurdenwhich isnowthe leadmetric forguidinghumanhealth interventions; in

    addition complementary metrics are needed to capture economic, social and environmental

    burdensofdisease.

    4Acquiredimmunedeficiencysyndromeoracquiredimmunodeficiencysyndrome(AIDS)isadiseaseofthehuman

    immunesystemcausedbythehumanimmunodeficiencyvirus(HIV)

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    Thereisalackofevidenceontheapplicationofinnovationstosurveillance,modellingandgeospatialmappingwithpotentialtoimproveassessmentandhencemanagement.

    Possibleresearchcontributions

    Crosssectionalstudiestomappresenceandprevalenceofimportantzoonoses. Burdenofdisease(DALYs)estimatesforneglectedandhithertounmeasuredzoonoses. Metricsthatcapturetheotherimpactsofzoonoses(multipleburdensofdisease). Frameworksforprioritisationforinvestmentinzoonoses(researchanddevelopment). Novelrapidandlowcostdiagnosticssuitableforfielduse. Surveillancesystemsthatuseinnovativeapproachese.g.riskbased,participatory,mobilephone,

    HealthMap,molecular,etc.

    Surveillancesystemsthatimprovelinksbetweenhuman,livestockandwildlifediseasedata. Betterlinkingofsurveillancetoaction. Rigorousimpactassessmentsofdifferentsurveillancemodelsincludingaccordingtoestablished

    frameworkse.g.CDC.

    Prioritisation of research on wildlife origin zoonosis and key species presence/prevalence todeterminerisk.

    Whichwildlife specieshavebeen implicated in the transferofdiseasefrom livestock tohumans

    andwhatarethekeyfactorsthatinfluencetheriskoftransmission?

    Manydifferentwildlifespeciesare implicatedashostsforthe importantzoonoses identifiedbyourstudy(n=292).Ofthehosts(663)listedinourdatabase,51%weredomesticatedanimalsand

    36%werewildanimals,withtheremainderbeingunspecifiedorlikelytoincludebothdomestic

    and

    wild

    species

    (e.g.

    hosts

    listed

    as

    birds

    or

    herbivores)

    (Evidence

    weak

    Chapter

    3).

    There are few studies on risk factors for transmission from wild and/or domestic animals topeople and between wildlife and domestic livestock in the literature, and studies are biased

    towardscertainspeciesandorders(evidencestrong Chapter7).

    Consumptionofbushmeatrepresentsoneofthemoresalientways inwhichhumanscome inclosecontactwithwildlifeandtheirpathogens.Itisanimportantsourceofzoonotictransmission

    fromwildlife(Evidencemedium Chapter5).

    Environmental contamination with pathogens by livestock and/or wildlife is another majortransmissionroute(evidencemedium Chapter5).

    Agroecosystemchange,especiallyforestfragmentationandedgeeffects,canincreasepathogenflowsbetweenpeople, livestockandwildanimals,and increasediseaserisk (Evidencestrong

    Chapters5,7and8).

    Agroecosystem change can also decrease disease risk, and a shift from wildlife to domesticanimalhostscanselectfordecreasedpathogenicity(Evidencemedium Chapter7).

    Socioeconomic determinants of health can be more powerful determinants of risk thanbiologicalfactors(Evidencemoderate Chapter7).

    Whetherthereareotherwildlifespeciesthatcouldbecomekeycandidatesfortransferofdisease

    inthefutureandwhy?

    Viruses

    are

    more

    likely

    to

    be

    emerging

    than

    other

    types

    of

    pathogen.

    A

    wide

    host

    range

    is

    associatedwithpathogenemergence(Evidencemedium Chapter9).

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    Dataonmultispeciespathogentransmissionandadaptationofvirusesislimitedtoafewfamilies,mostlyRNAviruses:notablycoronaviruses, lentiviruses, flaviviruses,paramyxovirusesandavian

    influenzaviruses(Evidencestrong Chapter6).

    Theputativeoriginalhosts forthesevirusesare:bats (3viruses),primates (2viruses)andcats,cattle, horses, birds and rabbits (1 virus each). However, there are many other potential

    candidate pathogens and hosts, that have not been properly evaluated. (Evidence medium

    Chapter6).

    Whilemanyorganismshavethepotentialto infectmanyspecies,thekeytochanges indiseasetransfer is contact rates and host opportunities (often anthropogenically driven) (Evidence

    medium Chapter6).

    Batshaverecentlybeenthesourceofanumberofemergingzoonoticdiseases,someofwhichhaveinvolveddomesticanimalsintransmissionandamplification.Encroachmentofhumansand

    livestock into bat habitat and disturbance of bat populations due to hunting and habitat

    destruction,aswellasbatbehaviouranddemography is increasing the likelihoodofpathogen

    spilloverandfuturediseaseemergence.(Evidencemedium Chapter9).

    Keyevidencegaps

    Many zoonoseshavemultiple transmission routesandmultiplehost reservoirs thatarepoorlyunderstood;assessingthe importanceofdifferenttransmissionroutesandtherolesofhosts in

    specificcontextsisaprerequisiteforeffectiveandefficientcontrol.

    Lack of understanding of the human behavioural determinants of livestock and wildlifeinteraction and exposure through, for example, hunting, harvesting, consumption, recreation,

    andagriculturalintensification.

    Lackofevidenceonputativetransmissionhotspots,including;livestockmarkets;urbanandperiurbanwildlifeand farming; fragmentsandedges;wildlifeconservationareasandbufferzones;

    wildlifevaluechains;aswellasdynamichotspotscausedbynaturaldisastersandconflict.

    Possibleresearchcontributions

    Reviewsofexistingevidenceonattribution,transmissionroutesandepidemiology. Conventional and molecular epidemiology to map pathogen flows, especially in suspected

    hotspots(staticanddynamic).

    Wildlifesurveystodetectpathogensandhostranges,focusingonthespeciesandpathogensthatshow greatest potential for zoonotic transmission and emergence (peridomestic species,

    rodents,bats,viruses). Transmissionexperimentstounderstandinfectivityandhostranges. Case control and risk factor studies to investigate links between human illness and livestock,

    wildlife,food,waterandotherfactorsincludingsocioeconomic,toinformdiseasemanagement.

    Human behavioural and socioeconomic studies to understand the institutional environmentwithin which people make decisions and the underlying anthropogenic drivers of disease

    transmission.

    Modelling(multidimensional,interdisciplinary)tobetterunderstanddiseasedynamics. Applicationofvaluechainanalysistowildlife,foodandproductsystems. Surveyofperidomesticattributesthatare importanttobringingwildlife incontactwithpeople

    andlivestockandassessmentofrisks.

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    Whatarethemaindrivers(globalandgenericwithinregions)changingthedegreeofinteraction

    betweenwildlifeanddomestic livestock andwhat are the key characteristics (e.g. geographic,

    political, economic, demographic, gender etc) which they affect in influencing the risk of

    transmission?

    Thegrowth inhumanpopulationandconsumption isdrivingwidespreadenvironmentalchange(urbanisation,agriculturalexpansionand intensification,andwildlifehabitatchange),whichhas

    led to zoonoticdisease emergence and reemergence.However therehavebeen few studies,

    (and fewer in developing countries), that quantify or identify causal links for this probable

    association.(Evidencemedium Chapters5,6,8,10).

    Changing landuseandagriculturalexpansiondisruptswildlifehabitatsandbringshumansandtheir livestock into closerproximity towildlife resulting in changes inhostpathogendynamics

    andincreasedriskofspillover.(Evidencestrong Chapters5,6,8,10).

    Livestock production intensification increases the population and density of livestock andincreases the likelihoodof livestockbecoming an amplifyinghost,or sourceofenvironmentalcontamination.(Evidencemedium Chapters8,10).

    Livestock and wildlife movements, marketing and trade increase the risk of local andinternationalmovementofpathogensandspillovertohumans.(Evidencestrong Chapters5,8,

    10).

    Wildlifemanagement forconservationor recreationalhuntingcan increase thepopulationsizeanddensity resulting inhigherdiseaseprevalence inwildlifeand increased riskofspillover to

    livestock.(Evidencemedium Chapters5,8).

    Disease emergence is influenced by human behaviour including decisions driven by lack ofinformationandrulebreakingbehaviour.(Evidencemedium Chapter10).

    Climate change ispredicted toaffect thegeographicaldistributionandpopulationdensitiesofwildlifespecies,whichwill interactwithmanyother factorstohavevariableeffectsondisease

    dynamics.(Evidenceweak Chapters8,9).

    OthercommonlycitedfactorsthatinfluenceemergenceorreemergencewithvaryingdegreesofevidencearedetailedinChapter9;theseinclude:deteriorationofpublichealthservices,human

    migrants (often associated with war and conflict or disaster), urbanization, natural disasters,

    globalization,watermanagementprojects,useof fertilizers,deforestation, lossofbiodiversity

    andextremeclimaticeffects.(EvidenceweaktomediumChapter9).

    It is the context in which potential pathogens exist and evolve that matters most to diseaseemergenceandnotmolecularmechanisms,whichhavealwaysexistedandareprimed to takeadvantageofopportunitiesastheyarepresented(Chapter6).

    Keyevidencegaps

    Morestudiesofcontextualaspectsofthewildlifelivestockinterfaceareneeded,andondriverswithinspecies(susceptibilities)forpathogenevolutionandamplification.

    Work isneededonunderstandingmore specificallyhow thechangingbiomassofhumansanddomesticanimalsandbiodiversitydeclinewillaffectpathogenemergenceandevolution.

    Thereislimitedunderstandingofrapidlychanginginstitutionalenvironmentswherepeoplefromruralandurbanareasandnationaland internationalgroupsaremixing,and rule systemsand

    their associated enforcement (household, community, private, legal) are constantly being

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    modified with pockets of activities that are poorly monitored, allowing for rule breaking

    behaviour.

    Possibleresearchcontributions

    Frequencyandlikelihoodofpathogenflowacrossspeciesunderdifferentcontexts. Keyecologicalchangeswhichdrivepathogenemergenceandtransmission. Specificresearchintomechanismsofamplificationandpersistence. Longitudinalstudiestounderstandchangesindynamicsovertime. Researchintonaturaldiseaseandinfectionprocessesinbiodiverseanimalcommunitiesandhow

    thesesystemsselectforandmaintainlowpathogenicitymicrobialcommunities.

    Foresight ormodelling to understand possible trajectories of disease dynamics in the face ofanthropogenicdriverssuchasclimatechangeanddemography.

    Developingwaysofquantifyingtheanthropogenicdriversofchangesindiseasedynamics. Groundtruthingassumptionsaroundimpactsofdriversonemergence. Developmentofmethodsforassessingruleandenforcementstructuresacrossfoodandproduct

    systems

    What are thepossible interventions (and associatedgovernance structure) that could limit the

    interactionofkeywildlifespecieswithdomesticlivestockandthepotentialeconomicandsocial

    impacts(atbothstateandhouseholdlevel)ofthoseinterventions?

    a)Whatistheevidenceregardinginterventionmethodsthatreducecontactbetweenwildlifeand

    livestock?

    Riskfactorsarecontextspecific,andtheeffectivenessofan interventionstrategywillvarywithcontext. Interventions based on risk are more effective and efficient than conventional

    management.(Evidencemoderate Chapter7).

    Eliminationofwildlifepopulationsasameanstoreducecontactisnotdesirableandinanycaseprobablynotfeasible(Evidencemoderate Chapter11).Reducingwildlifepopulationcanreduce

    risktolivestock,butsmallscaleandshorttermcontrolisineffectiveandcanevenspreaddisease

    (Evidencestrong Chapter11).

    Separationoflivestockfromwildlifebyfencinggenerallyreducesrisksofdiseasetransferbutthelossofheterogeneityinthelandscapeincreasesriskofstochasticdiseaseeventsthroughlossof

    endemism and immunity. Few barriers are impermeable. Environmental, social and economic

    costsoffencingarehighandunacceptableincountrieswithstrongwildlifeeconomiesandwith

    migratingwildlife.(Evidencestrong Chapter11).

    Innovationsmayradicallyimprovecontroleveninpoorcountries.(Evidenceweak).b)Associatedgovernancestructures

    Both topdown and communitybased programs have had little longterm success in tacklingepidemiologically complex disease at the humanlivestockwildlife interface in developing

    countries(Evidencemedium).

    IntegratedandOneHealthapproachesleadtobettercontrol(Evidenceweak/medium). Propoordevelopmentisoneofthemosteffectivewaysofreducingzoonoses(Evidencestrong).Keyevidencegaps

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    Currentassessmentandmanagementis,forthemostpart,notbasedongoodsurveillanceorriskdata.Riskbasedmanagementoffersagreatopportunityforimprovingmanagementofzoonoses.

    Thisinvolvesbasingmanagementoncontextspecificepidemiologyandriskfactors.

    Peoples reaction to thepresenceof disease is inadequatelyunderstoodmaking itdifficult totailorinterventionsthatcreatesynergiesforhouseholdandcommunityactions.

    Thecosts,benefitsandbroaderimpactsofzoonosesmanagementareimperfectlyunderstoodaswellastheincentivesneededforsustainablecontrol.

    Adapting innovations: promising technological, organizational and social innovations exist butneedtobebetteradaptedtodevelopingcountrycontexts.

    Possibleresearchcontributions

    Systematicreviewstoidentifyinterventionsforwhichcredibleevidenceexists. Identifyingriskfactorstoguidezoonosesmanagementinspecificcontexts. Developing integrated interventionpackages to target risk factors, incorporating technological,

    socialandeconomicinnovations.

    Randomisedcontrolledtrialsofinterventionpackagesassessingefficacy,appropriateness,equity,sustainabilityandimpactsofinterventions.

    Developmentofadatabaseonlocalandcommunityresponsestodiseasepresence. Comparing successful and failed interventions in order to develop guidelines for policy and

    practice.

    Economic and social experiments to better understand incentives arounddisease control andsustainability.

    OneHealthmethodsforlinkingdifferenttypesofinterventions.

    Socio

    ecological

    approaches

    to

    determining

    optimal

    control

    methods

    based

    on

    reducing

    risk

    and

    increasingresilience.

    Research intonovelcontrol technologiesandapproaches suchasvaccines,population control,diseaseresistance,biosecurity,husbandryandecosystembasedinterventions.

    Modellingofdifferentcontroloptions(epidemiology,ecology,economics).

    Note:Thestrengthofevidencesupportingthevariousstatementsisassignedbyexpertsresponsible

    forthereviewusingcriteriasetoutinthemethodology.

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    2. Methodology

    Overview

    Amultidisciplinaryteam fromthe InternationalLivestockResearchInstitute,Kenya,andtheRoyal

    Veterinary

    College,

    United

    Kingdom,

    with

    expertise

    in

    zoonoses,

    epidemiology,

    socio

    economics,

    and

    wildlife,undertookthereview.Adatabaseofimportantzoonoseswascompiledandusedtodevelop

    a listofpriorityzoonoseswitha livestockwildlife interface fordevelopingcountries.Collaboration

    withHealthMap andAUIBARpermittedinitialexplorationofspatialrelationsbetweenzoonosesof

    importance, landuse andhumanpopulationdensity.A systematic reviewwas carriedout in line

    withthescopesetoutintheTermsofReference.

    Identificationofzoonoseswithawildlifelivestockinterface

    We considered that zoonoses appearing in standard textbooks couldbe classified as important.

    Thisisanimportantpointofdeparturefromotherstudiesthatincludeallzoonoticpathogens,even

    those that are extremely rare. One of our hypotheseswas that important zoonoses might have

    differentcharacteristics intermsoftypeandhost.Threestandardtextbookswereusedto identify

    these zoonoses of importance (PAHO, 2003, Goldsmid, 2005, MVM, 2008). Information was

    extracted from the textandentered intoanExceldatabase. Initially343diseaseswere identified,

    which reduced to 292 diseases after removing duplicates and standardising names. The disease

    name, the specific causative agent, type of agent (bacteria, virus, protozoa, helminth, fungus,

    arthropod,other), region (developing,developed), reservoirs (wildlife,domestic), andhostswere

    recordedforeachdisease.

    Fromthedatabaseof292 importantzoonoses,theresearchteamselected61zoonosesthatboth

    hadalivestockwildlifeinterfaceandwereimportantindevelopingcountries.Additionalinformation

    wasaddedtothedatabaseonthemode(s)oftransmissionforeachdiseaseandtheinvolvementof

    largemammals.

    Mappingofzoonoses

    Weinvestigatedtheuseofwebbasedmappingandgeoreferencedmapsformappingdiseasesand

    relating the spatial distribution of disease to human demography, environment (land cover) and

    wildlife distribution. One webbased disease mapping system that we explored was HealthMap

    (www.healthmap.org),whichisanautomatedsystemthatgathersinformationfordiseaseoutbreak

    monitoringandrealtimesurveillanceofemergingpublichealththreatsfromnontraditionalsourcessuchasonlinenewsoutletsandexpertdiscussionforums,aswellasgovernmentwebsites(Major,

    2008). HealthMap was developed as a freely accessible and automated system that monitors

    information on emerging diseases in real time. It currently gathers reports from 14 sources,

    includingGoogleNews,whichsummarisesinformationfrommorethan20,000differentwebsites.It

    uses search criteria that includediseasenames, symptomsand keywords.The system collectsan

    averageof300reportsperday,mostofwhich(85%)comefromnewsmediasources(Major,2008).

    Outofthelistofdiseases,diseasesyndromesortypesofdiseaseforwhichHealthMaphaddatawe

    requested dataforAfrica on15zoonoticdiseasesordiseasesyndromesortypesthatweremainly

    zoonotic fortheperiodofJanuary2006toApril2011.Thediseasesandsyndromeswereanthrax,avian influenza, botulism, bovine tuberculosis, brucellosis, Clostridium difficile infection,

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    Cryptosporidium,diarrhoea,dysentery,foodborne illness,gastroenteritis, leptospirosis,salmonella,

    trichinosis,andwaterborne illness.HealthMap provideddataondiseaseoutbreakbydiseasetype,

    globalpositioningsystem(GPS)coordinatesandsourceofinformation.

    Wegeneratedmapsofindividualzoonoticdiseasesandspeciesrichnessforall15zoonoticdiseases.

    Thespeciesrichnessmapwasderivedbyaddingdiseasesoutbreaksinanareaofonebyonedegree

    grid.Thesemapswereoverlaidwithhumanpopulationmaps andwederived statistics from the

    numberofpeoplethatwerewithintheareaofdiseasesoutbreaks.Nextweoverlaidwithprotected

    areas to find how many outbreaks occurred inside and outside protected areas. The human

    populationdatawassourcedfromILRIanddataontheprotectedareasfromWDPA(WDPA,2010).

    EvaluationoftheHealthMapdatabaseindicatesthatanumberofdiseasesdidnothavefullcoverage

    for the period used in this study, which may be because HealthMap relies on reported disease

    outbreak information from theprintmedia (Major, 2008).BetweenOctober2006 to July 2007 a

    wide variety of pathogens were detected with information on 141 unique infectious disease

    categories that was based on data sourced from Google News feed alone (Major, 2008). The

    pathogensmostreportedwereavianinfluenza(877reports),Escherichiacoli(733),andSalmonella

    spp. (479). Over the study period reports of outbreaks of infectious disease occurred in 174

    countries,with the greatest number from theUnited States (4351 reports), theUnited Kingdom

    (1018), Canada (880), and China (737). However, there was an underreporting of disease for

    developing countries. The information shows a clear bias to countries with more media outlets,

    moredevelopedpublichealthresourcesandgreateravailabilityofelectroniccommunication(Major,

    2008). Major (2008) reports that the research group at HealthMap is now developing ways to

    improvecoverageforAfricaandSouthAmerica,whichhavethehighestriskandburdenofemerging

    infectiousdiseases.Theprojectintendstomonitorotherinternetsources,suchasblogs,discussion

    sites,andlistservstoincreaseitscapacitytocapturemorediseasesandalsoextendsitscoverage.

    Asecond sourceofdatawas theAfricanUnion InterafricanBureauofAnimalResource (AUIBAR)

    Animal Resource Information System (ARIS), which has recently been upgraded to capture and

    transfer animal disease data in real time (AUIBAR, 2010). This information is sourced from the

    monthly reportsof thenationalveterinaryservicesofAUmemberstates.Thenumberofnational

    monthlyreportshasincreasedfrom10 in2000to47in2009andthequalityofspatialinformation

    hasalsoimprovedwiththeuseofGPS(AUIBAR,2010).Weextractedadatasetofanthraxoutbreaks

    recorded in2009 toexaminehow thegeocodeddata couldbemodelled inaglobal information

    system(GIS)platform.Itwasnotspecifiedwhichspeciesof livestockorwildlifewereaffected.We

    conducted an explanatory analysis to explore the association between the spatialdistribution of

    anthrax and human population density, land cover, and species richness of wildlife (mammals,

    ungulates,primatesandcarnivores).ThelandcovermapwasderivedfromtheGLC2000(Fritzetal.,

    2004), thehumanpopulationdensity from the ILRIGISdatabaseand thewildlife species richness

    fromtheAfricanMammalianDatabank(Boitanietal.,1999).Themammalianspeciesrichnesswas

    derivedasaproxyforwildlifehostspeciesrichness(Jonesetal.,2008).Thespeciesrichnessmaps

    weregeneratedfromgeographicalrangedistributionmapsforterrestrialmammalianspeciesfound

    inAfrica(Boitanietal.,1999).Speciesrichnesswascalculatedasthenumberofspecies inanarea.

    Wealsogeneratedspeciesrichnessmapsforungulates,carnivoresandprimatesandrelatedthem

    toanthraxoutbreaks.

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    Systematicreview

    Thesystematicreviewwasthemainpartofthestudyandfollowedastandardapproach,comprising

    thefollowingactivities:

    Thematic areas within the scope of the TOR were identified, and team members wereassignedtodifferentthemes

    Asetofsearchcriteriawasdevelopedforeachtheme relevantliteraturedatabaseswereidentified Asearchforpaperswasconductedforeachtheme Thepaper titleswere screenedby research assistants for relevance to the themeand the

    abstractswereobtainedforsuitablepapers

    Theabstractswereblindreviewedforrelevancetothethem byatleasttwoteammembersandabstractsselectedbytwoormorepeoplewereretained

    Fullpaperswereretrievedfortheselectedabstractsandreadbyatleastoneteammember:thequalityofeachpaperwasevaluatedandthe keyfindingsfromeachpaperwasrecorded

    usingastandardtemplate

    For each theme, the findings from the selected paperswere collated andpresented as achapterinthisreport

    Seventhemeswereidentifiedbytheteamandteammemberswereassignedtoeachthemebased

    ontheirexpertise:

    Disease transmission routes and relative importanceof the livestockwildlife route (leaderSilviaAlonsosupportedbyDeliaGraceandothers).

    Pathogensofwildlifecapableofrecombiningwithanalogousorganismsindomesticlivestock(leaderRichardKocksupportedbyDeclanMcKeeverandothers).

    Risk factors for disease transmission from wild/domestic animals to people and betweenwildlifeanddomesticlivestock(leaderDeliaGracesupportedbySilviaAlonsoandothers).

    Drivers influencing interactionbetweenwildlife/livestockand the implications forzoonosestransmission(leadersDirkPfeiffer,BryonyJonessupportedbyRichardKock,MohammedSaid

    andothers).

    Historicalchangesintransmission,factorswhichfosternoveltransmissionroutesandhosts,and wild animal candidates for future disease transmission (leaders Dirk Pfeiffer, Bryony

    JonessupportedbyRichardKockandothers).

    Productionandsocioeconomicfactors influencingtheriskoftransmissionbetweenwildlifeand domestic livestock and from wildlife/livestock to people (leader Jonathan Rushton

    supportedbyRichardKock,JemimahNjuki,MohamedSaidandothers).

    Riskmanagement and control interventions and their successor failurewith emphasisoninterventions based on managing interaction between hosts (wildlife/livestock/humans)

    (leaderDeliaGracesupportedbySilviaAlonsoandothers).

    To identify papers relevant to each theme, the team generated a list of search criteria for each

    theme.Twoformsofsearchesweredone,generalanddiseasespecific,forpaperspublishedinthe

    past5yearsusingPUBMEDandCABDIRECTdatabases(AfricanJournalOnlinewasusedinitiallybut

    waslaterabandonedbecauseityieldedveryfewhits).Fordiseasespecificsearches,teammembers

    identifiedimportantzoonosesrelatedtoeachthemeandthediseasenamewasaddedtothesearch

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    termsusedforthegeneralsearchesEveryeffortwasmadetoobtainthepapersthatwereselected

    forfullpaperreview,althoughthiswasnotpossibleineverycase.

    The paper reviewers assessed the strengthof evidence for each paper basedon the following

    criteria: credibility of researchers; adequacy of study design (original studies); thoroughness of

    review(reviewpapers);possiblebias;populationscovered;overall importance.Systematicreviews

    usually involve setting strict criteria on quality of evidence to screen for highly credible original

    studies; however, in this reviewwhen strict criteriawere applied insufficientor no studieswere

    obtained. Using less strict criteria, review articles and discussion papers were included, and

    additionalpapersobtainedfromreference listsofselectedpapersorknowntotheteammembers

    butnotobtainedthroughthesystematicsearchwerealsoobtained. Thislargeandfuzzy literature

    onthereviewtopic,meantwritersreliedextensivelyontheirownknowledgeandexpertise.

    Table2.1.SummaryofpapersreviewedduringthesystematicreviewTheme No. papers

    selected asrelevantbased ontitle

    No. papers

    selectedbased onabstractreview

    No. papers

    that wererelevantbasedon fulltextreview

    Number of

    additionalpapersused

    Total number

    of paperscontributingto themechapter

    Disease transmission routes andrelative importance of thewildlifelivestockroute

    98 28(ofwhich8

    originalstudies)

    11 5 16

    Pathogens of wildlife capable ofrecombining with analogousorganismsinlivestock

    171 30 30 36 66(ofwhich45

    originalstudies)

    Risk factors for diseasetransmission from wild/domesticanimals to people and betweenwildlifeandlivestock

    153 13 4 8 12

    Drivers influencing interactionbetween wildlife and livestockandtheimplicationsforzoonosestransmission

    124 30 15 27 42(ofwhich19original

    studies)

    Historical changes intransmission,factorswhichfosternovel transmission routes andhosts,andwildanimalcandidates

    for

    future

    disease

    transmission

    182 86 43 37 80(28original

    studies)

    Production and socioeconomicfactors influencing risk oftransmission between wildlifeand livestock and fromwildlife/livestocktopeople

    ? 33

    Risk management and controlinterventionsandtheirsuccessorfailure with emphasis oninterventionsbasedonmanaginginteractionsbetweenhosts.

    94 24 22 7 29

    Total number of papers (some

    papers were relevant to morethanonechapter)

    239

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    3. Importanceofzoonosesandthelivestockwildlifeinterface

    Thefirstpartofthispaperdiscussessomeoftheconceptsaroundunderstandingzoonosesandwhat

    ismeantby a livestockwildlife interface;wegoon to summariseevidenceon the importanceof

    zoonoses(withreferencetothe livestockwildlife interface) intermsofhumanhealth impactsand

    othersocietalconcerns;thethirdpartpresentsasystematicapproachtoidentifyingandprioritising

    zoonoseswitha livestockwildlife interfaceofrelevance todevelopingcountriesanddiscussesthe

    characteristicsofthesediseases.

    Summaryofmainmessages

    There isnoclearconsensusordefinitionofwhatconstituteszoonosesatthe livestockwildlifeinterface. Inthissystematicreview,werefertozoonoses,ordiseasescommontoanimalsand

    humans, the epidemiology of which involves domesticated and nondomesticated animals

    (includingfish).

    In lowincome countries, infectiousdiseases are responsible fornearly 40%of theburdenofhumansicknessanddeath.Onefifthofthis(or8%ofthetotaldiseaseburden)isattributableto

    zoonoses or diseases recently emerged from animals (7% and 13% respectively). Evidence:

    medium.

    In highincome countries, infectious diseases are much less important (4% of total burden);diseasesemergingrecentlyfromanimalsandfoodbornezoonosesareanimportantpartofthis

    smallburden,butotherzoonoseshaveminorimpacts.Evidence:strong.

    Zoonoses are absolutely and relativelymore important in lowincome countries compared tohighincomecountries.Evidence:strong.

    Aswellashumanhealthimpacts,zoonoseswithalivestockwildlifeinterfaceareresponsibleformultipleburdens including:costof illness;costto livestocksector;costtoeconomies;negative

    social andpsychological impacts; andnegative impactsonwildlife andecosystems.Evidence:

    strong.

    TheGlobalBurdenofDiseaseassessment ledbytheWorldHealthOrganisationsuggestsfoodborne zoonoses, human African trypanosomosis and leishmaniasis to be the most important

    zoonosesglobally;allhavealivestockwildlifeinterface. Evidence:medium.

    Publishedexpertopinionconsidersbrucellosis,humanAfricantrypanosomosisandtuberculosistobethemostimportantzoonoses;allhavealivestockwildlifeinterface.Evidence:weak.

    Weidentified292importantzoonosesfromtheliterature:82%ofthesehadawildlifereservoir,74% had a domestic animal reservoir and 60% had both a wildlife and a domestic animalreservoir.Evidence:medium.

    3.1Whatarezoonosesandwhatisalivestockwildlifeinterface?

    Zoonoses are usually defined as diseases and infections that are naturally transmitted between

    vertebrateanimalsandpeople(WHO,1959).Alandmarkpapershowedthatthemajorityofhuman

    diseases (61%)aresharedwithanimals (Tayloretal.,2001).However, thissummarystatisticgoes

    onlypartwaytounderstandingdiseasesatthe interfaceofhumans,animalsandtheenvironment.

    Thedifficultyofattributionmakesitdifficulttounambiguouslydescribediseasesaszoonosesatthe

    livestockwildlifeinterface:manydiseaseshavemultiplecauses,someofwhicharezoonoses;many

    pathogenshavemultipletransmissionpathways(someofwhicharezoonoses)andinmostcasesthe

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    relative importance of zoonotic pathways is not known; some diseases that are classified as

    zoonosesareprobablybetterthoughtofascommunicablediseasescommontoanimalsandpeople;

    and the categoriesof livestockandwildlifeareartificialandnotalwayshelpful.Moreover,hosts,

    pathogens and transmission paths are not fixed but are constantly evolving. Lastly, the disease

    centricmodelofpathogenandhostwhichhas longdominatedmedicalthinking, isgivingwaytoa

    perspective that includes health issues at infrapathogen scale (transmission of drug resistance

    betweenbacteriabyplasmids)andsuprahostscale(ecosystemservicesforhealthprovision).Some

    of these issues are discussed in greater depth in Box 3.1. The commonly encounteredmodel of

    wildlifeasreservoirsofdiseaseonlycapturessomeofthecomplexityofinteractionsatthelivestock

    wildlifeinterface.Table3.2givesatypologyofzoonosesatthewildlifelivestockinterface.

    Forthepurposesofthissystematicreview,zoonosesatthe livestockwildlife interface,aredefined

    as: diseases that are common to animals and humans, the epidemiology of which involves

    domesticatedandnondomesticatedanimals.

    Box3.1Conceptualissuesaroundidentifyingzoonosesatthelivestockwildlifeinterface

    Attribution:Diseasesmaybecausedbymultiplepathogens,someofwhicharezoonotic

    Tuberculosisisoneofthemostseriousdiseasesofpeople.ThemajorityofcasesareduetoMycobacteriumtuberculosis, transmitted almost entirely by humantohuman transmission. (M. tuberculosis is a reversezoonosesandtherearedocumentedcasesofanimalsbeinginfectedbypeople,butthisisunlikelytoplayanimportantroleintransmission.)However,aproportionofhumantuberculosiscasesarecausedbyM.bovisthe cause of cattle tuberculosis. In developed countries where cattle tuberculosis is well controlled thisproportion isvery low (around0.11%ofcases),butbeforemilkpasteurizationM.boviswasan importantcauseofhumantuberculosis,especiallyintestinaltuberculosisinchildren.Therearefewstudiesofzoonotic

    tuberculosis in developing countries and poor communities; those that exist have shown proportions ofhumantuberculosisduetoM.bovisofupto45%insomepopulations(Rodwelletal.,2008),althoughfrom520%ismoretypical(Cosivietal.,1998).

    Table3.1.Humandiseasescausedbymultiplepathogens

    Examplesofzoonoticspecies

    Examplesofnonzoonoticspecies

    Proportionofdiseaseduetozoonoticpathogens

    Tuberculosis Mycobacteriumbovis M.tuberculosis 10%(20%)

    Leishmaniasis Lmajor;mostotherspecies

    L.tropica;Ldonvani Unclear,perhaps75%

    Lymphaticfiliariasis Bmalayi,Btimori Wuchereriabancrofti 10%

    Shistosomiasis S.japonicum S.mansoni,S.

    haematobium

    10%

    Malaria P.knowlesiandothers P.falciparum andothers

    Very small

    Attribution:Pathogensmayhavemultipletransmissioncyclessomeofwhicharezoonoticandothersnot

    Manyarboviruseshaveasylvaticcycle,whilstsomealsohaveanurbancycleandanintermediatecycle.

    Sylvaticcycle(sometimesknownasthejunglecycle):theviruscyclesbetweenanarthropodandanonhuman mammalian host. Humans are usually deadend hosts that are infected by thearthropod.

    Intermediate cycle: occurring in agroecosystems with both human and nonhuman mammalianhosts.

    Urbancycle:theviruscyclesbetweenhumansandanarthropodspecies.In the case of dengue, a high burden disease, almost all transmission is urban (human to human or

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    anthroponotic)andmanypeoplewouldnotconsiderittobeazoonoses.However,theexistenceofasylvaticcyclemeansthatitisbydefinitionazoonoses,andmayhaveimplicationsforpersistenceandresurgenceofdisease,asdiseaseswithasylvaticcyclearemoredifficulttocontrol.

    Many diseases are transmissible through different sets of hosts. For example, dairy cattle are a majorreservoir for Escherichia coli O257:H7, but once a person is infected (typically through milk, meat or

    vegetables contaminatedwith cattle faeces) thenpersontoperson transmission is also possible. There isgenerallylittleinformationontheimportanceofdifferenttransmissionroutes,whichmakescontroldifficult.

    Attribution:Commonsourcecommunicablediseases

    Zoonosesareoften conceptualised in termsofdiseaseswith reservoirsof infections inanimals.Formanyzoonoses,thereservoiristheenvironmentandhumans,wildlifeandlivestockmayallbeaffected.Thesearesometimes referred to as communicable diseases common to humans and animals and are not alwaysconsideredaszoonoses.Tetanussporesarepresentubiquitouslyintheenvironmentaswellastheintestinesofanimalsandhumans.Whilehuman infectionfromananimalbite ispossible,orfromapplicationofcowdungtotheumbilicus,muchofthehighburdenofhumantetanusisfromtheenvironmentandnotdirectlyfromanimals.

    Attribution:Arbitrary

    distinction

    between

    livestock

    and

    wildlife

    There are many different classifications of the animals with which humans share ecosystems. Livestock,domesticanimals,peridomesticanimals, foodanimals,workanimals,companionanimals, feral,pest,andwildlifeoverlapand varyby context.Dependingon the contextdogsmaybe foodanimals,workanimals(guarddogs),companions,orferal. Nichelivestocksuchasguineapigs,rabbits,pigeonsandgiantsnailsareimportant insomeareasandoftenharbourspecificdiseasesandzoonoses.Wildlifeare increasinglybeingdomesticated (deer,elk)ormanaged. In some contexts feral livestock (pigs, camels,goats)occupy similarnichestowildlife.

    Transmissionpathwaysarenotstaticbutshiftaccordingtoevolutionarypressure

    Ashift fromwildlifetowildlife, towildlifetodomesticanimal, todomesticanimaltohuman (zoonotic), tohumantohuman(anthroponotictransmission)wouldbeanexpectedevolutionaryresponseofpathogensto

    increased transmission opportunities. Numerous investigators believe that visceral leishmaniasis wasoriginally an infection that circulated among wild animals (canids and perhaps rodents), and that later,domesticdogswere included in itscycle;eventually,thediseasebecamean infectiontransmittedbetweenhumanswithoutthe interventionofananimalreservoir,as isthecaseofkalaazar in India.This isalsothepatternforhumaninfluenzapandemics.Influenzavirusescirculateinwildbirds,somevirusesthenevolvetobeabletoaffectdomesticbirdsandpigs,thentovirusesthatoccasionallyaffectpeople,andthentovirusesthatarehighlycontagiousbetweenpeople.

    Animalsconditioningagroecosystemsinwaysthatfosterorreducedisease

    Animals may alter ecosystems in ways that increase and decrease the risk of disease in people. Someexamplesare: histoplasmosis,adiseaseofhumans,dogs,cats,cattle,sheep,horses,andmanywildmammals.Thefungus

    causingthediseasegrows insoilenrichedwithavianorbatfaeces;birdsthemselvesarenotsusceptibletothedisease,buttheirfaecesplayacentralroleincreatingareservoirforthedisease. Clostridiumtetaniisanormalinhabitantoftheintestinesofhorsesanddomesticruminantsandruminantfaecescontributestocontaminationofsoilwithtetanusspores,especiallywhereanimalmanure isusedasfertiliser. C.difficile,a common causeof infectiousdiarrhoea inhospitalisedhumans, ispartof themicrofaunaofdomesticanimals.Useofcephalosporinsinanimalsisincreasingtheriskofresistantstrainsenteringthefoodchainandenvironment,potentiallyleadingtoanincreaseofcasesinthecommunityratherthanthecurrentnosocomialincidence. HPAIH5N1 isassociatedwithspecificagroecologicalconditionsthatarepresent inSouthEastAsia,Chinaand Egypt. The role of backyard poultry and domestic ducks in wetland systems contributing to thepersistenceofinfectionandwildbirdreservoirsissuggestedfromavailableliterature,butequivalentstudyofthecontributionof intensivepoultryproductionsystemshasbeenresistedbythe industryandwidespreadvaccinationhasreducedsurveillanceandepidemiologicalinvestigation.

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    Table3.2Differentepidemiologicalpatternsforzoonoseswithalivestockwildlifeinterface

    Patterns Definition Example

    People

    in

    the

    parasite

    developmentcycles Humans

    are

    final,

    intermediate

    or

    aberranthostsfordiseaseswithmultihostlifecycles Humans

    are

    final

    host

    and

    aberranthostsforpigtapeworm

    Wildlifereservoirforlivestockandhumaninfection

    Infectioncirculatesinwildlifemakingeradicationfromlivestockdifficultandhenceposingrisktohumans

    Brucellosisinbison;tuberculosisinbadgers

    Diseasesinecosystems Diseasesexistinsylvatic(wildlifeonly),domestic(domesticanimals)orurban(humanonly)cycles,specifictoecosystems,thatmayconnect

    dengue(sylvaticandurban);trichinella

    Communicablediseases

    commontohumansandanimals

    Livestock,wildlifeandhumansare

    susceptibletoadiseasethatiscommonintheenvironmentbutanimalsarenotinvolvedintransmissiontohumans

    Manyfungaldiseases

    Animalsastransportersfacilitatingpathogenspread

    Animalsallowspreadofdiseasebytransportingpathogensinfleasorticks

    Dogsandanimalstransportfleaswithbubonicplague

    Animalsconditioningecosystemstobettersupportpathogens

    Wildlifeorlivestockcontaminateenvironmentwithpathogensorcreateconditionsthatfosterpathogengrowth

    Ruminantgutsandfaecesarereservoirsforanthraxandbotulism

    Pigeonandbatfaecesarereservoirsforhistoplasmosis

    Agricultureasariskfactorforzoonoses

    Agricultureincreasesriskbyprovidinghostsorenvironmentalconditionsforpathogens

    Foodbornezoonoses

    EmergingpathogenssuchasC.difficileandavianinfluenza

    Reversezoonoses Wildlifeordomesticanimalsareatriskfromhumandiseasesbutdonotplayaroleintransmissionorspread

    Humantuberculosisindogs

    Measlesinmonkeys

    4.2Importanceofzoonosesatthelivestockwildlifeinterface

    4.2.1Importancetohumanhealth

    4.2.1.1ContributiontoGlobalHealthBurden

    TheunitofDisabilityAdjustedLiveYear(DALY)hasrevolutionisedassessmentandprioritisationof

    humanhealthburden (Mathersetal.,2002). Introducedby theGlobalBurdenofDiseasestudy in

    theearly1990s,DALYsarethepresentvalueoffutureyears lostduetoprematuredeathorbeing

    alive with poor health. The Global Burden of Disease (GBD) provides a comprehensive and

    comparableassessmentofmortalityand lossofhealthdue toover150diseases, injuriesand risk

    factors forallregionsof theworld.Of33diseases listed inthesectioncovering infectiousdisease

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    and respiratory infections,onethirdarezoonosesorhaveazoonoticcomponent,andallofthese

    haveawildlifeinterface.

    TherearethreeproblemswithusingtheGBDtoassesstheimportanceofzoonoses.Firstly,several

    zoonoseswithconsiderableburdensarenotincludedintheGBDassessment.Forexamplerabiesis

    estimated to cost 1.7millionDALYsper year inAfrica andAsia alonebut isnot considered as a

    nameddiseaseor illness(Maudlinetal.,2009).Other importantzoonoseswithawildlife interface

    and largeburdens thatarenot includedare cysticechinococcosis, cysticercosis, leptospirosisand

    brucellosis. Secondly, zoonoses (especially in poor countries) are systematically underreported

    relativetootherdiseases(Schellingetal.,2007,Maudlinetal.,2009)and,astheGBDreportisbased

    onnationalinformationonlevelsofmortalityandcause,thisbiasisreflectedintheGBD.Thethird

    problemisoneofattribution.TheGBDis,asthenamesuggests,organisedarounddiseasesandnot

    pathogensortransmissionpathways. Forexample,diarrhoealdiseases,amongstthehighestcauses

    of morbidity and mortality in poor countries, comprise one category. Although the majority of

    important diarrhoeal pathogens are zoonotic (Schlundt et al., 2004) and many of these have awildlifeinterface,itisnotcurrentlypossibletoidentifythezoonoticcomponentfromGBDfigures.A

    promisinginitiativeisunderwaytoattributefoodbornediseasetopathogenlevel(Kuchenmlleret

    al.,2009)whichwillassistinbetterunderstandingofthezoonoticburden.

    Despitethesecaveats,DALYsrepresentauniversallyagreedwayofassessingtheburdenofdisease

    tohumanhealthandalogicalapproachtoatleastroughlyestimatingthehealthburdenofzoonoses

    at the livestockwildlife interface.We apply this to the assessmentof zoonoseswith a livestock

    wildlifeinterfaceinTable3.3(detailsofthecalculationsareprovidedinAnnex1).

    Table3.3

    Burden

    of

    zoonoses

    in

    terms

    of

    death

    and

    disability

    Highincome countries Lowincomecountries

    TotalDALY %Total TotalDALY %Total

    Allcausesofsicknessanddeath 122,092,000 100% 827,668,844 100%

    Infectiousandrespiratorycauses 4,128,000 3.4% 319,905,538 38.7%

    Zoonosesanddiseasesrecentlyemergedfrom

    animals

    768,770 0.6% 64,951,636 7.8%

    Diseasesrecentlyemergedfromanimals 631,600 0.5% 44,727,571 5.4%

    Zoonoses 140,770 0.12% 22,084,983 2.7%

    Zoonoticfoodbornedisease 131,400 0.11% 17,762,144 2.1%

    Themost important zoonoses in lowincome countries inorderofdecliningburden are: zoonotic

    foodborne disease, human African trypanosomosis, zoonotic leishmaniasis, zoonotic lymphatic

    filiariasis,Japaneseencephalitis,zoonoticschistosomiasisandzoonotictuberculosis.

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    Inhighincomecountries,zoonosesanddiseasesrecentlyemergedfromanimalsconstitute18.6%of

    theburdenof infectious and respiratorydiseasebutonly 0.6%of the totalburden:mostof this

    burden is due to HIV/AIDS. Zoonoses make upjust 3.4% of the total burden of infectious and

    respiratorydiseaseandnearlyallofthisisduetozoonoticfoodbornedisease.

    Inlowincomecountries,thetotaldiseaseburdenismuchhigherthaninhighincomecountriesand

    theshareof infectiousandrespiratorydiseasesmorethan tenfoldhigher.Zoonosesanddiseases

    recentlyemerged fromanimalsconstitute20.3%of the infectiousandrespiratorydiseaseburden;

    zoonoses are relatively more important than in highincome countries, making up 6.9% of the

    infectiousandrespiratorydiseaseburdenwhereasinhighincomecountriestheyconstitute3.4%of

    the infectious and respiratory disease burden. Moreover, while the proportion of infectious and

    respiratory disease is 13 times higher in lowincome countries than highincome countries, the

    proportion of zoonoses is 23 times higher. This supports the common perception that zoonotic

    diseasesarerelativelymoreimportantinlowincomecountries.

    3.2.1.2Expertopinion

    Theonlysystematicglobalprioritisationofzoonoseswithapropoor,developmentperspectivewas

    carriedoutbyILRIin2002(Perryetal.,2002).Inthisstudy,brucellosis,whichisnotincludedinthe

    GBD,was considered tobeby far themost important zoonosis, followedby trypanosomosis and

    tuberculosis(Figure3.1).

    Diseaseswererankedinorderofthosewiththegreatestimportancetothelivelihoodsofthepoorin

    eachlivestockproductionsystemintheirregion.Thediseaseswerethenrankedbytheidentification

    and quantification of their impacts on the poor. Then, three major impacts of each disease or

    syndrome were identified and scored. These were socioeconomic impacts (primarily production

    lossesandcontrolcostsincurredbythepoor),zoonoticimpactsandnationalimpacts(acombination

    ofmarketing impactson thepoorwithpublicsectorexpenditureondiseasecontrol).Aweighting

    wasapplied to thescores foreachdisease relating to the importanceofdifferent impactson the

    poor(forexample,socioeconomicimpactwasgivenaweightingof85%andnationalimpact,15%).

    Zoonoticdiseaseswererankedseparatelyduetothedifficultyofmeasuringthemonetaryvalueof

    humanhealthimpacts.

    Sixdifferentsetsofrankingsofanimaldiseasesbyexpertsandfarmers,withoutaspecificfocuson

    zoonoses,aresummarised inPerryandGrace(PerryandGrace,2009).Theauthorsnoteastriking

    lack of consensus between the lists; however, brucellosis, tuberculosis and human African

    trypanosomosisappearonseverallists.

    Wefoundonlyonesystematiccomparativestudyofthedirectcostsofanimaldiseasesatnational

    level (GreatBritain) (Bennettand Ijpelaar,2005).Partof thestudy lookedat thecostsandhealth

    impactsoftenzoonoses;enterotoxigenicE.coli,salmonellosis,fascioliasis, leptospirosis(L.hardjo),

    pasteurellosis, salmonellosis and tuberculosis in cattle; psittacosis (enzootic abortion), orf and

    toxoplasmosisinsheep;StreptococcussuisTypeIImeningitisinswine;andsalmonellosisinpoultry.

    Salmonellosisrelatedtopoultryhadbyfarthehighesthumanhealthcoststogetherwiththehighest

    humanwelfare impactscore.ThiswasfollowedbysalmonellosisrelatedtocattleandE.coliO157

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    23

    Experts identified61diseasesatthe livestockwildlife interface indevelopingcountriesconsidered

    importantbecauseofactualorpotentialnegativeimpactsonpeople,domesticanimals,wildlifeand

    ecosystems.Whilemost were confirmed zoonoses, somewere considered important because of

    possible or potential (though not proven) zoonotic transmission or because understanding the

    disease had implications for zoonoses at the livestockwildlife interface. Among these diseases,

    virusespredominated as the causative agent, followedbybacteria thenprotozoa andhelminths.

    Nearlyhalfofthesediseaseshadmultipletransmissionroutes(39%).Amongstthosewithonlyone

    transmission route,16werevectorborne,11were transmittedbydirectexposure,8were food

    borneandonewastransmittedbyaerosol.

    Table3.4Importantzoonosesatthelivestockwildlifeinterfaceindevelopingcountries

    DiseaseName CausativeAgent Typeofagent

    Acariasis(mange)Sarcoptesspp,Cheyletiellaspp,Dermanyssusspp,Ornithonyssusspp

    Arthropod

    Myiasis Hypodermabovis Arthropod

    Anthrax Bacillusanthracis Bacteria

    Botulism Clostridiumbotulinum Bacteria

    Bovinetuberculosis Mycobacteriumbovis Bacteria

    Brucellosis Brucellaabortus Bacteria

    Campylobacterenteritis Campylobacterjejuni,C.coli Bacteria

    Haemolyticuraemicsyndrome Escherichiacoli(0157:H7) Bacteria

    JohnesDisease Mycobacteriumaviumsubspppseudotuberculosis Bacteria

    Leptospirosis Leptospirainterrogans Bacteria

    Lymedisease Borreliaburgdorferi Bacteria

    Plague Yersiniapestis Bacteria

    Relapsingfever Borreliarecurrentis Bacteria

    Salmonellosis Salmonellaeenterica Bacteria

    Tuberculosis Mycobacteriumtuberculosis Bacteria

    Tularemia Francisellatularensissubspturalensis Bacteria

    Actinomycosis Actinomycesisraelii Fungal

    Cryptococcosis Cryptococcusneoformans Fungal

    Clonorchiasis Clonorchissinensis(Chineseliverfluke) Helminth

    CutaneouslarvamigransAncylostomabraziliense,A.caninum,Uncinariastenocephala

    Helminth

    Alveolarechinococcosis Echinococcusmultilocularis Helminth

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    24

    Cysticechinococcosis Echinococcusgranulosus Helminth

    Fascioliasis Fasciolagigantica Helminth

    Schistosomiasisjaponica Schistosomajaponicum Helminth

    Intestinalschistosomiasis Schistosomamansoni Helminth

    Trichinellosis Trichinellaspiralis Helminth

    Amebiasis Entamoebahistolytica Protozoa

    BabesiosisBabesiacanis,B.microti,B.divergens,B.bovis,B.equi

    Protozoa

    Cryptosporidiosis Cryptosporidiumparvum Protozoa

    Giardiasis Giardialamblia Protozoa

    Leishmaniasis Leishmaniadonovani,otherspp Protozoa

    Malariaofnonhumanprimates Atleast20speciesofPlasmodium Protozoa

    Toxoplasmosis Toxoplasmagondii Protozoa

    Trypanosomiasis(Africansleepingsickness)

    Trypanosomabrucei,T.bruceirhodesiense, T.bruceigambiense

    Protozoa

    Anaplasmosis Anaplasmaphagocytophilum Rickettsia

    Qfever(Queryfever) Coxiellaburnetii Rickettsia

    Chikungunya Alphavirus Virus

    Cowpox Cowpoxvirus Virus

    CrimeanCongoHaemorrhagicFever Nairovirus Virus

    Denguefever Denguefevervirus Virus

    Ebolahaemorrhagicfever Ebolaviruses Virus

    FootandmouthdiseaseFootandmouthdiseasevirus(aphthovirustypesA,O,C,SAT1,SAT2,SAT3andAsia)

    Virus

    Hantaviral

    diseases

    Hanta

    virus

    Virus

    Hemorrhagicfeverwithrenalsyndrome

    Hantaanvirus,Dobravavirus,Puumalavirus,Seoulvirus

    Virus

    Hendravirusinfection Hendravirus(paramyxovirus) Virus

    HepatitisE HepatitisE virus Virus

    InfluenzatypeA(swine/avian/Hong Kongflu)

    Influenzavirus(myxovirus) Virus

    JapaneseBencephalitis Japaneseencephalitisvirus(flavivirus) Virus

    Lassafever Lassavirus(arenavirus) Virus

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    25

    MarburgHF Filovirus Virus

    Monkeypox Flavivirus Virus

    Newcastledisease Newcastlediseasevirus(paramyxovirus) Virus

    Nipahvirusinfection Nipahvirus Virus

    Orf(contagiousecthyma) Poxvirus Virus

    Rabies Rhabdovirus Virus

    RiftValleyfever Phlebovirus Virus

    Rotavirus Rotavirus Virus

    Severeacuterespiratorysyndrome(SARS)

    Coronavirus Virus

    Tickborneencephalitis Flavivirus Virus

    WestNilefever WestNilevirus(Flavivirus) Virus

    Yellowfever Flavivirus Virus

    Ourexpertbaseddiseaseselectionbroadlysupportstheliteraturecitedinconfirmingthe

    importanceofvirusesandmultihostpathogensasmostproblematicagentsandbats,carnivores

    anddomesticherbivoresasmostproblematichosts.

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    26

    4. Mappingzoonosesatthelivestockwildlifeinterface

    Introduction

    Epidemiologists have traditionally used maps when analyzing associations between locations,

    environmentanddiseases(Clarkeetal.,1996).Ostfeldetal.,(2005)pointsoutthatmapshavebeen

    used for two distinct purposes in epidemiology. The first involves retrospective analyses of

    spatiotemporallydynamicepidemicstounderstandwhatfactorsgovernthespatialpatternandrate

    of spread of diseases. The second major use of maps in epidemiology is to characterize spatial

    variation in contemporaneous (static) ecological risk of infection and potential causes of that

    variationandthatspatialdataondiseaseincidencecanbeusedtoextrapolatetheriskofexposure

    from currentdistributions tonew geographical areas.The ability tomakemaps interactivelyhas

    increased thepotential formanyusers touse the information.Coupledwith increasinganalytical

    functionalityofGeographical InformationSystem (GIS) that ranges fromvisual toexploratoryand

    modelling, the uses of GIS in epidemiology has increased significantly (Pfeiffer and HughJones,2002,Ostfeldetal.,2005).

    The output generated by GIS in map format has the particular advantage of showing implicit

    representation of spatial dependence relationships in an intuitive manner. The technology is

    becoming an essential component of modern diseases surveillance systems (Pfeiffer and Hugh

    Jones,2002,Jonesetal.,2008).Theopportunitiesforepidemiological investigationhave increased

    withwebbasedmappingtools,useofGlobalPositioningSystem(GPS)inmappingdiseaseoutbreaks

    andincreasedprecisionandfrequencyofcollectingtheinformation.

    Results

    UsingHealthMapdata,Figure4.1ashowsthespatialdistributionof15zoonoticdiseasesorgroups

    ofdiseases inrelationtohumanpopulationdensity.Theoutbreaksoccurred inboth lowandhigh

    humanpopulationdensityareas (Figure4.1b).Majorcitieshadoutbreaksofzoonoticdisease.The

    highdensity reported cases includedCairo andAlGiza in Egyptwhere avian influenzaoutbreaks

    werereported,andinWestAfricaavianinfluenzawasreportedinKano.Alsofoodborneillnesswas

    reported in Safaga and El Manial in Egypt. These areas have population densities of more than

    10,000peopleperkm2.Examplesofotherbigtownswithpopulationdensititiesoflessthan10,000

    people per km2 that reported outbreaks of disease included Kampala (outbreaks of dysentery,

    diarrhoeaandbotulism),andCocody,Abidjan(outbreakofavianinfluenza).

    This type of spatial analysis provides us with potential information on risks of diseases to a

    population.Asthesediseasedatabasesbecomemorepopulatedwithinformation,itwillstrengthen

    thebasisformodellingandalsoprovideinsightsonwhattypeofthreatsthesediseasescanhaveon

    humanpopulations.

    Thenext stepof theanalysiswas toderiveahotspotmapon the15 zoonoticdiseases,which is

    shown in Figure4.1c.. As indicated inthemapthehotspotswere located inEgyptalongtheNile,

    centralandwesternKenya,centralUganda,Zimbabwe,andnorthwesternSouthAfrica.Theanalysisindicates that West Africa is also an area with a high number of zoonotic disease reports. The

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    fspeciesin

    axin

    relatio

    0 50 60 70

    MALS

    10 15

    ATES

    nrelationt

    anarea.

    nto

    specie

    00.0

    0.1

    0.2

    0.3

    0.4

    0.5

    Proportion

    perBar

    0

    10

    20

    30

    40

    50

    60

    70

    Numberofanthraxo

    utbreaks

    00.0

    0.1

    0.2

    0.3

    0.4

    0.5

    0.6

    Proportion

    perBar

    0

    20

    40

    60

    80

    100

    120

    Numbero

    fanthraxoutbreaks

    mammals

    richness

    o

    0 10

    UNGU

    5 10 15 2

    CARNI

    eciesrichn

    mammals,

    20 3

    ATES

    0 25 30 3

    VORA

    ss. Species

    ungulates,

    00.0

    0.1

    0.2

    0.3

    Proportion

    perBar

    50.0

    0.1

    0.2

    0.3

    0.4

    0.5

    Proportion

    perBar

    31

    richness

    rimates

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    Theoccurrenceofanthraxinrelationtomammalspeciesrichnessshowshighoccurrenceofanthrax

    in high mammal rich areas (Figure 4.4a). Similar, patterns are exhibitedwith species richness of

    ungulatesandcarnivora(Figure4.4b).However,theoutbreaksofanthraxoccurred inareasof low

    species richness forprimates.Manyof theprimates are found in verydensewooded vegetation

    whereanthraxoutbreaksmighthavebeendifficulttodetect.

    Mostoftheanthraxoutbreakswereoutsideprotectedareas,butasindicatedinthemapthespecies

    richnessofanimalsgoesbeyondtheparkandmanyoftheseanimalswillbeincontactwithlivestock

    andpeople.Manyoftheseparksaresmall insizeandinmanycountriesweredryrangerefugefor

    livestock.Aspeopleandlivestockincrease,therangeforwildlifeisbecomingsmallerandthecontact

    between livestock andwildlife is increasingwhichwill increase transmissionofdiseasesbetween

    wildlifeandlivestock.

    Conclusions

    Explanatoryspatialanalysiswiththedatasets(pointdata)showsthegreatpotentialincharacterizing

    thespatialvariationofdiseasesinrelationtoanumberofenvironmental(landcover),social(human

    population)andwildlife (species richness)variables.Thepotentialofspatialtemporalanalysishas

    increaseddue to the resolutionofdata (georeferencingusing theGPS) in thatmanydiseasesare

    mappedwheretheydidoccur.

    Toolsdeveloped todealwith suchdatahave improved thedata integration, correlation analysis,

    hypothesissettingandalsocommunicationofthe informationtothepublic.However,asmanyof

    the organizations are just starting to develop geodatabases on diseases we still have under

    reportingofdiseases. Jonesetal (2008)suggestthatthere isacriticalneed forhealthmonitoring

    andidentificationofnew,potentiallyzoonoticpathogensinwildlifepopulations.Theyalsoadvocate

    forreallocationofresourcesforsmartsurveillanceofemergingdiseasehotspotsinlowerlatitudes

    suchastropicalAfrica,LatinAmericaandAsia.

    The major hurdle in geospatial data on zoonotic diseases is data accessibility. Many of these

    programsarejuststartingandmany institutionsfind itdifficulttosharedata. Itwillbehelpfulfor

    these institutions todeveloppolicyandregulationsondataacquisitionanddatause.Globalscale

    dataonenvironment(landcoverandvegetationindicesfromsatelliteimages),socioeconomicand

    humandemographyarenowwidelyavailablecomparedto2030yearsago.Many institutionsare

    making their data available through the internet and also through institutional agreements.

    Improvementinthemodellingofdiseaseswillbepossiblewithaccessibilityandavailabilityofthese

    datasets.

    Lackofreliablegeoreferenceddataonzoonosesprevalenceorevenpresencehinderedmapping;

    thiswaspartiallyovercomebycollaborationwithHealthMap.However,dueto limiteddata itwas

    notpossible to carryoutdetailed investigationof the linksbetweengeoreferencedenvirosocio

    economicgeoreferenceddataanddiseases,but in thenear future this is likely tobepossibleas

    thesehealthdatabasesgatherandconsolidatetheinformationthatisscatteredinmanyplacesand

    organizations.

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    5. Diseasetransmissionroutesandtherelativeimportanceofthewildlife

    livestockroute

    Summaryofmainmessages

    Human habitat expansion, for habitation or agriculture, has contributed to greater contactbetweenhumansandwildlifeand resulted in theemergenceofpreviouslyunknown zoonotic

    diseasesfromwildlife.Evidence:high.

    Livestock movements (seasonal or all year round) and wet markets provide importantmechanismsforzoonoticdiseasespread.Evidence:high.

    Consumptionofbushmeatrepresentsoneofthemostobviouswaysinwhichhumanscomeintoclose contactwithwildlifeand theirpathogens. It isan important sourceof zoonoticdisease

    transmissionfromwildlife.Evidence:medium.

    Keepinglivestockmaypotentiallyincreasetheriskofzoonoticdiseasetransmissionfromwildlifetohumansbecause livestockmay create anew linkbetweenwildlife andhumans thatwere

    otherwisenotconnected.Evidence:medium.

    Introduction

    Understanding thediverse transmission routesof infectiousdiseases fromwildlife tohumans isa

    first step in the assessment of any potential risks associated with wildlife. A large number of

    infectiouspathogensareknowntobeharbouredbywildanimals,andmanyhavetheabilitytojump

    from wildlife to humans and livestock. Many different transmission routes exist for infectious

    diseases ingeneral, includingdirecttransmission,airborne,vectorborneand indirecttransmission

    via fomites (including food). In the case of zoonoses related to wildlife, there is still no clear

    understandingofwhicharethemostimportanttransmissionmechanismsandwhetherprioritization

    ispossibleasawaytoinformallocationofresources.Mostzoonoticpathogensfoundinwildlifeare

    not exclusive to these animals but are also found in domestic animals. The degree of contact

    betweenhumansanddomesticanimals is inmost cases greater thanwithwildlife.