Developing a progressive control pathway for African animal trypanosomosis

Opinion

Developing

a

Progressive

Control

Pathway

for

African

Animal

Trypanosomosis

$

Oumar

Diall,

1,y

Giuliano

Cecchi,

1,

*

,y

Gift

Wanda,

2

Rafael

Argilés-Herrero,

3

Marc

J.B.

Vreysen,

3

Giovanni

Cattoli,

4

Gerrit

J.

Viljoen,

4

Raffaele

Mattioli,

5

and

Jérémy

Bouyer

6,7

Progressivecontrolpathways(PCPs)arestepwiseapproachesforthe reduc-tion,elimination,anderadicationofhumanandanimaldiseases.Theyprovide systematic frameworks for planning and evaluating interventions. Here we outlinea PCP for tsetse-transmittedanimal trypanosomosis,the scourge of poor livestock keepers in tropical Africa. Initial PCP stages focus on the establishmentofnationalcoordinationstructures,engagementof stakehold-ers,developmentoftechnicalcapacities,datacollectionandmanagement,and pilot field interventions. The intermediate stage aims at a sustainable and economicallyprofitablereductionofdiseaseburden,whilehigherstagestarget elimination. The mixed-record of success and failure in past efforts against Africananimal trypanosomosis(AAT) makes thedevelopmentofthis PCPa highpriority.

WhyaProgressiveControlPathwayforAAT?

Progressivecontrolpathways(PCPs)(seeGlossary)andtherelatedroadmapsarestaged approachesincreasingly used for the reduction,elimination, anderadication ofa rangeof humanandanimaldiseases,includingfoot-and-mouthdisease(FMD)[1,2],pestedespetits ruminants(PPR)[3],brucellosis[4],andrabies[5].WithinthePCPacronym,theword‘control’ canberegardedasencompassingthefullrangeofstrategiesagainstdiseases,fromreduction ofthediseaseburdentoeliminationanderadication.

AAT,alsoknownas‘nagana’,isafamilyofparasiticdiseasescausedbydifferentspeciesof unicellularorganisms,thatis,Trypanosomavivax,T.congolense,T.brucei,T.simiae,andT. suis.AATiscyclicallytransmittedbyblood-suckingtsetseflies(Diptera,genusGlossina). Somespeciesoftrypanosomes,inparticularT.vivax,canalsobetransmittedmechanicallyby otherbiting flies (most notablyTabanus and Stomoxysspp.)[6,7]. AAT affects ruminants, swine,camels,equines, andcarnivores, but theheaviest burden onsubsistence livestock keepersinsub-SaharanAfricaiscaused bybovinetrypanosomosis[8].Tsetse-transmitted trypanosomosisisalsolistedbytheWorldOrganisationforAnimalHealth(OIE)asanotifiable disease(i.e.,a diseasethat,as soonas suspectedor detected,shouldbebroughtto the attentionofOIE).

Forovera century,effortsto studyandcontrol AAThave beensubstantial. Despitethese efforts,thediseaseremainstodaythemajorconstrainttothedevelopmentofmoresustainable and cost-effective crop–livestock agricultural systems in those areas of Africa having the greatest untapped potential [9]. The overall objective of the PCP for AAT is to promote

Trends

Whilstgreatstridesarebeingmadein the elimination of tsetse-transmitted humanAfricantrypanosomosis(HAT orsleepingsickness),progressinthe controlofAfricananimal trypanosomo-sis(AATornagana)ispatchyatbest. Progressive pathways (or stepwise, staged approaches)are increasingly usedforthecontrolofa numberof humanandanimaldiseases,including foot-and-mouth disease, peste des petits ruminants, brucellosis, and rabies.

Arangeoftoolsarecomingofage, which enable an evidence-based prioritization,planning,andmonitoring ofinterventionsagainstAAT,including geographicinformationsystems(GIS), species distribution models, and populationgenetics.

Whilstthedevelopmentofnoveldrugs againstAATlagsbehind,thearrayof techniquesforvectorcontrolhas broa-dened,andknowledgeontheiroptimal fieldofapplicationhasimproved. Among growing concerns on the capacityofsub-SaharanAfricatofeed itselfinthecomingdecades,removing theconstraintsposedbyAATappears moreurgentthanever.

1

FoodandAgricultureOrganizationof theUnitedNations(FAO), Sub-RegionalOfficeforEasternAfrica, AddisAbaba,Ethiopia

2

AfricanUnion–PanAfricanTsetse andTrypanosomosisEradication

interventionsthatalleviatepoverty,increaseincome,andimprovethelivelihoodsandresilience ofsmallholderfarmersbycreatingandprogressivelyexpandingareasfreeoftheAATburden. The PCP builds on many decades of research and on numerous technical and political achievements. Cost-effective tools against tsetse [10,11] and reliable diagnostics for AAT

[12] areavailable.Successstories ofsustainable tsetseandAAT controldo exist [13–15]. Technicalexpertiseispresentwithinmostendemiccountriesandfrominternational develop-mentandresearchinstitutions.InaOne-Healthframework,synergiescanbeexploitedforthe eliminationofhumanAfricantrypanosomosis(HAT)[16] andforthecontrolofotheranimal diseases(e.g.,tick-bornediseases[17]).Commitmentisstrongatthenationalandinternational level,asdemonstratedbythePanAfricanTsetseandTrypanosomosisEradicationCampaign (PATTEC),anAfricanUnion(AU)initiative[18],andbytheProgrammeagainstAfrican Trypa-nosomosis(PAAT),whichbringstogethertheeffortsoftherelevantUnitedNationsagencies(i. e.,FoodandAgricultureOrganizationoftheUnitedNations(FAO),InternationalAtomicEnergy Agency(IAEA)andWorldHealthOrganization(WHO))[19,20].

Manychallengesalsoexist.ThereisnovaccineforAAT.Chemotherapyandchemoprophylaxis remainthemainstayofdiseasecontrol,butavailableveterinarytrypanocides areoutmoded

[21],substandardandcounterfeitproductsare widespread[22,23],and drugresistanceis increasing[21,24].ThepresenceofawildlifereservoirmakesAATeliminationverychallenging, ifatallpossible,unlessthevectorsareremovedinasustainableway.Inturn,thesustainable removal of tsetse populations has been achieved in less than 2% of the 10 million km2 estimatedtobeinfested[25],andAATintegratedmanagementhasveryrarelybeensustained

[26].Thediseaseisoftenneglectedbybothendemiccountriesanddonors,asitmostlyaffects poorsmallholdersinruralareas,itdoesnotengagecity-dwellingdecisionmakers,itposesno immediatethreattowealthynations,anditdoesnotdirectlyinfluenceinternationallivestock trade.Finally,while acountry canself-declare,under its ownresponsibility,that theentire territoryorazoneisfreefromAAT[27],thereisnoOIEofficialrecognitionof‘freedomfromAAT’ statussofar.

ThepresentopinionprovidesafirstoutlineofthePCPforAAT,aimingtocontributetothe rationalizationofinterventionsagainstthispersistentandperniciousdisease.Thedevelopment ofthePCPappearsparticularlytimelyatajuncturewhenHATeliminationisprogressingsteadily whilstAATcontrollagsbehind.

PCPforAAT

ThePCPforAATincludesfivestagesandapre-entrylevelnamed‘belowStage1’(Figure1).A regularstep-wiseprogressionistherule(i.e.,fromStageNtoStageN+1)butfast-trackingis possibleinspecificcircumstances.Tomovefromonestagetothenext,aset ofminimum requirementsmustbemetandadetailedplantobeimplementedinthefollowingstagesmust beprepared.Independentvalidationisrequired.

‘BelowStage 1’and ‘Stage1’focus oncreating the necessarypolitical, institutional, and technicalenvironment,andassessingdiseaseriskandimpact.Stage2looksatsustainable reductionoftheAATburden,whilethefollowingstages(i.e.,from3to5)targetelimination.The PCPisconsistentwiththephasedconditionalapproachrecommendedbyFAO/IAEAforthe implementationofarea-wideintegratedpestmanagementprogrammesthatmightincludethe SterileInsectTechnique(SIT)[26].

‘BelowStage1’and‘Stage1’aremainlynational-levelendeavours,whilstsubsequentstages willnormallytargetselectedinterventionareas. Asaresult,withinacountry,different AAT-affectedareascanbeatdifferentPCPstages(Figure2).

Campaign(AU-PATTEC),Addis Ababa,Ethiopia

3

JointFAO/InternationalAtomic EnergyAgency(IAEA)Programmeof NuclearTechniquesinFoodand Agriculture,InsectPestControl Sub-Programme,Vienna,Austria

4

JointFAO/IAEAProgrammeof NuclearTechniquesinFoodand Agriculture,AnimalProductionand HealthSub-Programme,Vienna, Austria

5

FAO,AnimalProductionandHealth Division,Rome,Italy

6

UnitéMixtedeRecherche INTERTRYP,CentredeCoopération InternationaleenRecherche AgronomiquepourleDéveloppement (CIRAD),Montpellier,France

7

UnitéMixtedeRecherche“Animal, Santé,Territoires,Risqueset Ecosystèmes”(ASTRE),CIRAD, Montpellier,France

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Foodand AgricultureOrganizationoftheUnited Nations.PublishedbyElsevierLtd.

y_{Theseauthorscontributedequally.}

*Correspondence:

Glossary

AATelimination:reductiontozero ofAATincidenceinadefined geographicalareaasaresultof deliberateefforts.Continued measurestoprevent re-establishmentoftransmissionmay berequired.Theconceptfinds applicationatStages3to5ofthe PCPforAAT.

AATeradication:permanent reductiontozerooftheworldwide incidenceofAATasaresultof deliberateefforts.Intervention measuresarenolongerneeded. AATextinction:infectiousagents causingAATnolongerexistinnature orinthelaboratory.

AATsustainablereduction: reductionofAATincidence, prevalence,morbidity,mortality, burden,orimpacttoalocally acceptable,economically-profitable levelasaresultofdeliberateefforts. Continuedinterventionmeasuresare requiredtomaintainthereduction. Theconceptfindsapplicationat Stage2ofthePCPforAAT.‘AAT control’isusedbycertainauthorsin lieuof‘AATsustainablereduction’. Africananimaltrypanosomosis (AAT)or‘nagana’:afamilyof parasiticdiseasescausedbydifferent speciesoftsetse-transmitted trypanosomes,thatis,Trypanosoma vivax,T.congolense,T.brucei,T. simiae,andT.suis.

Baselinedata:epidemiological, entomological,socioeconomic,and environmentaldatacollectedpriorto thestartofinterventionsagainst tsetseandAAT.Baselinedata constitutethereferenceagainst whichtheimpactofinterventionsis measured.

Cyclicaltransmission:AAT transmissionbytsetseflies,whereby trypanosomespathogenicfor livestockundergomultiplication cycleswithinthemouthparts,midgut and/orsalivaryglandsofthevector. Fasttracking:possibilityofskipping certainstagesofthePCP,if conditionsallow.InthePCPforAAT, fasttrackingispossiblefromStage1 toStage3,andfromStage1to Stage5.

Insecticide-treatedcattle(ITC): epicutaneousapplicationof insecticidesoncattle,alsoknownas thelive-baittechnique.Animalscan betreatedwithpour-onformulations, sprayingordippingwithaqueous formulations.Theinsecticidecanbe AtallstagesofthePCP,varioustechnicalandmanagerialareasrequireattention(Figure3),

althoughemphasisandspecificactivitiesdifferfordifferentstages.

ThemaintargetgroupfortheproposedPCParethenationalauthoritiesinchargeoftsetseand AATcontrol,buttheapproachcanbeappliedtomultinationalandregionalinitiativesaswell. ThePCPforAATshouldalsocontributeto,andbenefitfrom,ageneralreinforcementofthe veterinaryservicesintheaffectedcountries,andallpossiblesynergiesinthecontrolofother diseasesshouldbeexploited. Importantly, thePCP provides donors witharobust tool to monitorandevaluateprogressandimpacts,andgivesthemconfidenceinsupporting AAT-endemiccountries.

LayingtheGroundwork:BelowStage1,andStage1

BelowStage1

Afew minimumrequirementshave to bemetto enter thePCP.Prior tothat, acountryis consideredtobe‘belowStage1’,meaningthatithasnotformallyenteredthePCP. OnekeyrequirementtoenterStage1ispoliticalandfinancialcommitmentatthenationallevel, which is translated into adequate core funding to establish and support a Specialized NationalStructure(SNS)dedicatedtotsetseandAATcontrol.AnSNSmustbeendowed withcoretechnical and managerial competencies,although the strengthening ofthe SNS capacitiesisaddressedtoalargerextentinsubsequentstages.Politicalcommitmentisalso signalledthroughnationallevelengagementintheAU-PATTECinitiative.

Thesecondrequirementrelatestoself-assessmentandplanning.Countriesneedtoappraise theirexistingcapacities,epidemiologicalknowledge,institutionalarrangements,humanand financialresources.Subsequently,aworkplanmustbedeveloped,whichwillbeimplemented inthesubsequentStage1.

Stage1

ThefocusofStage1istodeveloptechnicalcapacitiesandtogainasufficientunderstandingof AATdistribution,risk,andimpactforanevidence-basedplanningoffieldactivities.Thelatter willbeimplementedinStage2andbeyond.

Essentialcapacitiesincludeprojectmanagement,veterinaryandentomologicalcompetencies inparasitologicalandserologicalsurveillance,trappingandidentificationofvector spe-cies,andAATandvectorcontrol.SkillsindatamanagementandGIStoenablemapping,risk assessment,andmonitoringarealsoneeded[7,28].

EssentialcapacitiesmustbebuiltwithintheSNS,butmoreadvancedones(e.g.,molecular diagnosis[29],geospatialmodelling[30]),canbeavailablefromnationalorregionalcentresand laboratories,aswellasfrominternationalinstitutions.

Theestablishmentofanational-levelinformationsystemisanotherpillarofStage1.Allrecent epidemiologicalandentomologicaldatashouldbeassembled,harmonized,geo-referenced, andcentralized.Nationalatlasescanbedeveloped[7],alsousingmethodologiesfromtheFAO continentalAtlasoftsetseandAAT[31,32].Targetedfieldinvestigationsshouldbeconducted wheregapsexist orwhereavailable informationistoooldtoinformdecisionmaking.More generally,allnecessarydataforanevidence-based,rationalselectionofinterventionareasand strategiesneedtobecollectedinStage1. Inparticular,ifafast-trackingtotheelimination pathway is envisaged (Stage 3 and beyond), genetics studies are likely to be needed to establishthedegreeofisolationofthetargettsetsepopulations[33,34]andtherelatedrisk ofreinvasion(Box1).

Socioeconomicinformation onthe burden ofAAT isessential to justify investmentand to prioritizeareasforintervention.Spatiallyexplicitbenefit-costanalyses[8,10,11],tsetseandAAT distributionmaps[7,31,32],andmodelsoftsetsedistributionandisolation[30,35]aretoolsthat shouldsupportarationalselectionofinterventionareasandstrategies(Box1).Theoccurrence andriskofHAT[36–38]shouldbeconsidered,asinterventionspromotingOne-Healthbring broaderbenefitsandaremorelikelytoattractresources[16,39,40].Securityconstraints(i.e., civilstrife,armedconflicts,etc.)shouldnotbeoverlooked.

appliedeithertothefullbodyor restrictedlyonthelegsandbelly(by sprayingordipping).

Insecticide-treatedtargets(ITT): insecticide-impregnateddevices usedtokillpests.Tsetsetargetscan usebothvisual(i.e.,shape,size, colours)andolfactorycues(i.e., naturalorartificialodours)toattract flies.

Livestockprotectivefences(LPF): insecticide-incorporatednettingthat reducestheimpactofnuisanceand bitingfliesonlivestock.Thenetis normallyinstalledaroundpens, kraals,sheds,orsties,inwhich livestockspendasizablepartofthe day.Attractedbythelivestockhosts, bitingfliesareinterceptedandkilled bytheinsecticide-treatednet. Mechanicaltransmission:AAT transmissionbybitingfliessuchas TabanidaeandStomoxynae, wherebytrypanosomespathogenic forlivestockdonotundergocycles withinthevector,orbyveterinary agentsusingthesameneedleduring vaccinationcampaignstargeting otherdiseases.

Parasitologicalsurveillance:an activityinvolvingthecollection, analysisandinterpretationof parasitologicaldata,thatis,data collectedbymeansofparasitological diagnostictechniques.ForAAT,the techniquesincludewetbloodfilms, Giemsa-stainedthickandthinblood films,centrifugationtechniquessuch astheHaematocritcentrifuge technique,andtheBuffycoat technique,andPCRdetectionofthe parasites’DNA.

Progressivecontrolpathway (PCP):stepwise,stagedapproach forthesustainablereduction, eliminationanderadicationofa disease(i.e.,withinthePCP acronym,theword‘control’canbe regardedasencompassingthefull rangeofstrategiesagainstthe disease).

Roadmap:strategicplanand programmaticframeworktoadvance intheprogressivecontroland eliminationofadisease.Roadmaps canbedevelopedatthenational, regionalandgloballevels.

Rolling-carpetapproach:aphased approachwherebythetargetpest populationandtheareaitoccupies aresubdividedintoaseriesof adjacentblocks.Blocksaretreated sequentially,withaviewtocreating andprogressivelyexpanding pest-freeareas.Generally,elimination Box1.NovelToolsforOptimizingthePrioritizationofInterventionAreasandtheExecutionofAAT

Control

AtlasesofTsetseandAAT

VirtuallyallAAT-endemiccountrieslackanational-level,centralizedsystemtomanagefielddataontsetseandAAT. Datacollectedovertheyearsaregenerallyscatteredbetweendifferentagents,locationsorinstitutions,andtheymay evenbecomelostaltogether.Thisgapdasheshopesforanevidence-baseddecisionmaking,asitmakesitimpossible tohaveasynopticpictureoftheepidemiologicalsituationatthecountrylevel.NationalatlasesoftsetseandAAT,such astheonerecentlysetupinSudan[7],arenowbeingdevelopedinmanycountries.Theyprovideasystematic,spatially explicitframeworkfordatacollation,storage,harmonization,andmanagement.Theseinitiativesbenefitfromthe FAO-ledcontinentalatlasoftsetseandAAT[31,32],asthemethodologiesitdevelopedcanbeadaptedandappliedatthe countrylevel.National-levelinformationsystemsontsetseandAAT,suchastheatlases,oughttounderpindataanalysis anddecisionmakingthroughoutthePCP;theyshouldbesetupinStage1andcontinuouslyupdatedinthefollowing stagesasnewdataarecollected.

DistributionModels

SpeciesdistributionmodelsenableustomapAATrisk[64]andoptimizetsetsecontroloperations[30].Theycanbe usedtogeneralizepointdataontsetsepresenceanddensityandAATprevalence,suchasthosecollectedduring Stages1and2ofthePCP.Theentomologicalinoculationrate(EIR)ortsetsechallengecanbemodelledinspaceand timeusingarangeofenvironmentaldata[64].Thisallowsafine-scalepictureofthedynamicsofAATrisktobe generated.Suchmodelscanbeveryusefultoselectthepriorityinterventionareasandtoinforminterventionsduring Stage2.

WhenanAATeliminationstrategyisselected(Stage3andbeyond),speciesdistributionmodelscanalsobeusedto informoperations.IntheNiayesareainSenegal,modelsoftsetsedistributionwereusedthroughoutthecampaignto optimizethetargetingandcost-effectivenessofoperations,includingdeploymentofITT,releaseofsterilemales,and positioningoftsetsemonitoringtrapstoassessprogress[30].

TsetsePopulationGenetics,FrictionandIsolation

AnewmethodologycombiningGISandpopulationgeneticswasrecentlydevelopedtoidentifynaturalbarriersthat isolatetsetsepopulations[35].Themethodologyisbasedontheconceptoflandscaperesistancetotsetsegeneticflow (i.e.,‘friction’).Astatisticalmodelofthegeneticdistancebetweentsetsepopulationsisfittedusingasetofpredictors(i. e.,remotely-sensedenvironmentaldata).Bycombiningthemodelledgeneticdistancewithaspeciesdistribution model,thetoolallowspotentiallyisolatedpopulationstobeidentified,andtheirgeneticdistancetothemaintsetse populationtobeestimated.DuringStage1ofthePCP,thismethodologycouldinformthechoiceonthemost appropriateinterventionstrategies.Forexample,potentiallyisolatedtsetsepopulationscouldbetargetedforStage3 eliminationactivities,whilstfornonisolatedpopulationsaStage2integratedmanagementapproachmightbemore appropriate.Themostfavourableareastodeployartificialbarrierstoreinvasioncouldalsobeidentified,thusoptimizing sequentialeliminationprogrammesbydividingthetargetpopulationintopartiallyisolatedsubunits.

SpatiallyExplicitBenefit–CostAnalysis

TheburdenofAAT,andthepotentialbenefitsthatcanaccruefromitsremoval,arenotevenlydistributedacross endemiccountries.RecentworkonbovinetrypanosomosisinEasternAfricageneratedasuiteofmethodologiesto estimateandmapthecosts[11],benefits[8],andbenefit–costratios[10]ofdifferentinterventiontechniques.This spatiallyexplicitinformationonthecostsandbenefitsofdifferentstrategiescanbeavaluableaidtodecisionmaking,in particularintheprioritizationofinterventionareasandtheselectionofthemostcost-effectivetools.

withinoneblockandsuppressionin theadjacentonearecarriedout simultaneouslytoavoidtheriskof reinvasionoftheclearedblocks.In theprocess,temporarybarriersmay alsoberequiredbetweenblocksto preventreinvasion.

Sequentialaerosoltechnique (SAT):theapplicationinsequenceof severalultra-low-volumespraysof nonresidualinsecticides,usuallyby aircraft.

Serologicalsurveillance:anactivity involvingthecollection,analysisand interpretationofserologicaldata,that is,datacollectedbymeansof antibodydetectiontechniques.For AAT,theenzyme-linked

immunosorbentassay(ELISA)isthe mostcommonlyappliedserological test.

SpecializedNationalStructure (SNS):dedicatedentitywithnational levelmandateforAATcontroland elimination.ExamplesofSNSinclude specializedunitswithinthemandated ministries,dedicatedinstitutes, coordinationstructures,andstatalor parastatalbodies.

Steeringcommittee:abodysetup toorientandsupervisethe SpecializedNationalStructureandits activities.Membershipshouldinclude nationalstakeholders(i.e.,all concernedministriessuchas livestock,agriculture,health, environment,etc.),aswellas regionalandinternationalactors(e. g.,regionaleconomiccommunities (RECs),internationalorganizations andresearchinstitutions). Sterileinsecttechnique(SIT):a methodofpestcontrolusing area-wideinundativereleasesofsterile insects.Sterilemalesreduce reproductioninafieldpopulationof thesamespeciesbyinducingsterility inwildfemales.

Tsetseelimination:complete removalofatsetsespeciesfroma definedgeographicalarea.The conceptfindsapplicationatStages3 to5ofthePCPforAAT.‘Local eradication’,oreven‘eradication’ tout-court,areusedbycertain authorsinlieuof‘elimination’. Tsetseeradication:removalofall wildpopulationsofagiventsetse speciesfromthewholeplanet. Tsetsesuppression:deliberate reductionofflynumbersasa precursortoelimination.Theconcept findsapplicationatStage3ofthe PCPforAAT.

Whilesubstantivefieldinterventionsarethefocusofsubsequentstages,pilotfieldactivities againsttsetseandAAT shouldbecarriedoutin Stage1.Their aimis to developnational capacities, fine-tune and optimize intervention tools, and motivate donors. Furthermore, throughoutthe PCP, fieldinterventions may be neededto tackle possibleAAT epidemics

[24],includinginStage1.

Stage 1 shouldalso look at coordination. A steering committee should be set up, for orientationandsupervisionoftheSNSanditsactivities.Membershipshouldincludenational stakeholders(i.e.,allconcernedministriessuchaslivestock,agriculture,health,environment, etc.),aswellasregionalandinternationalactors(e.g.,regionaleconomiccommunities(RECs), internationalorganizations,andresearchinstitutions).

Stage 1 culminates in the choice of priority interventionareas [41] and most appropriate strategiesfortheselectedareas(AATsustainablereductionorelimination).Importantly,the mostlikelystrategyforsubsequentstagescan,tosomeextent,influenceactivitiesinStage1. Forexample,requirements interms ofdata andcapacities differ between thesustainable reductionandeliminationscenarios,andthiscouldaffectactivitiesandthedurationofStage1. SustainableAATReduction:Stage2

ThefocusofStage2isasustainableandeconomically-profitablereductioninAATriskand burdenbycreatingareasoflowAATincidenceandimpact,wherebyonlysporadictreatments withtrypanocidesareneededandtheriskofemergenceand/orspreadofdrugresistanceis minimized[21,24].

TheinterventionstrategyhingesontheintegratedmanagementofAAT[24,25],acommunity/ farmer-basedapproachthatreliesonthecollaborationoflocalveterinaryservicesandfarmers associations,takingintoaccounteco-epidemiologicalsettings,livestockproductionsystems

[42],andcattle breeds.Effectivestrategies willrequirethe combineduseoftsetse control methods,diagnostictests,andtrypanocidaldrugs.Improvednutritionandthecontrolofother parasiticdiseaseswouldalsobebeneficial[43,44].

Baselineandmonitoringdata,includingparasitological,entomological,andsocio-economic data,needtobecollectedintheinterventionareastoguidefieldactivities,fine-tuneintervention strategies,andmeasureprogressandimpact.Thepossiblepresenceofdrugresistanceshould beconsidered,andifnecessaryinvestigated.

Regardingcapacitydevelopment,allactorsinvolvedintheintegratedAATmanagementshould betargeted,includinglivestockkeepersandfarmingcommunitiesatlarge,publicandprivate veterinaryservices,aswellastheSNS.Emphasisshouldgoonthecorrectuseoftrypanocides tolimittheemergenceandspreadofdrugresistance[21]andonefficientandcost-effective vectorcontroltechniques, particularly insecticide-treatedcattle (ITC)[45,46],livestock protectivefences(LPF)inthecaseofzero-grazingrearingsystems[47],and insecticide-treated targets (ITT), especially where tsetse pressure from protected areas has to be prevented[48].

ThemainchallengeinStage2issustainability,whichwillhavetorelyonthesensitizationand trainingofveterinaryservices,farmer associations,andindividualfarmers.Funding mecha-nismsmustbeputinplacetoensurethatinterventionsaresustainedwithminimalsupportfrom extensionservices[49].Thelattershouldfocusonmaintainingawarenessandsecuringthe availabilityandappropriateuseof affordable, efficientand cost-effectivecontrol tools[22]. Importantly, farmer communities must be fully involved in the devolvement of the integrated disease management strategies to ensure that they are adapted to the target

livestock–agriculturalproductionsystemsandmoregenerallytolocalconstraints.Adoptionof newtechnologies,suchastinytargets,LPF,restrictedapplicationofinsecticideonanimalsand repellent–insecticideassociations,normally requiresexternalsupport,agoodknowledgeof localsociotechnicalnetworks,astrongparticipatory approachandcolearningprocessesto adjustthetechniquestotheusers[25].Thedegreeofadoptionoftheproposedstrategyby stakeholderswill depend ontheir appreciation of the benefits and risks derived from the interventionactivitiesandtheassociatedchangesrequiredwithintheirfarmingsystem[50]. Stage2couldbesustainedindefinitely,withAATmanagementbecomingafixedproduction cost[10].However,thestrategyshouldbereassessedatregularintervals(3–5years).Should the epidemiological andsocioeconomicconditions become favourable,ashift towardsan eliminationstrategy(Stage3)canbeenvisaged.

EliminatingAAT:Stages3to5,andbeyond

ThefocusofthePCP’sfinalstages(3to5)istocreatesustainableAAT-freeareas.Modelsfor AATtransmission, aswellas forothervector-bornediseases, indicatethat incertain agro-ecologicalsettings(i.e.,endemicAATcyclewherewildfaunaareabsent[48])thediseasemight beeliminatedthroughasubstantialandsustainedreductionintsetsedensities[51]. How-ever,real-lifeexamplesofthisapproacharelacking,andAATeliminationnormallyrequiresthe localeliminationofthetsetsevector.ThisistheapproachdescribedinthisPCP.

Intheselectionoftargetareasfortsetseelimination,thelevelofisolationshouldbeassessed

[33,34], and isolatedpopulations shouldbe given priority.In principle, larger, nonisolated populationscouldbetackledsequentiallythroughtherolling-carpetapproach[52],which hasbeenusedverysuccessfullyforotherinsectpests[53,54].However,real-life,sustainable examples of the approach for tsetse flies are rarer. A recent example is the sequential eliminationof a sizable belt ofGlossina morsitanscentralis,which cutsacross Botswana, Angola, and Zambia; the programme was largely based on aerial spraying, namely the sequentialaerosoltechnique(SAT)[15,55].

Tsetsesustainablereduction: deliberatereductionofflynumbersto locallyacceptablelevels;the reductionismaintainedbycontinued intervention.Theconceptfinds applicationatStage2ofthePCPfor AAT.‘Tsetsecontrol’isusedby certainauthorsinlieuof‘tsetse sustainablereduction’.

Workplan:detailedplanofaction forspecificinterventionareasandfor awelldefinedtimeperiod(ingeneral, ofafewyears),aimedatadvancing intheprogressivecontrolofAAT.

1

2

3

4

5

Eliminaon of AAT transmission

AAT eliminated All AAT control measures suspended

Below

Stage 1

Integrated management of AAT(community/ farmer-based, supervised by veterinay services) Expression of naonal-level commitment Creaon of a naonal structure specialized in AAT control Establishment of core capacies and funding

Capacity development Understanding AAT risk and impact Selecon of priority intervenon areas and intervenon strategies Pilot field acvies

Sustainable and economically profitable reducon in AAT burden

Progressive control pathway for African animal trypanosomosis (AAT)

Stage 1

Stage 2

Stage 3

Stage 4

Stage 5

AAT eliminated Some AAT control measures maintained

Stage3

ThefocusofStage3istheinterruptionofAATtransmission.Manyactivitiesalreadydescribed forStage2havetobecarriedout(orcontinued)inStage3,butemphasisdiffers.Thecollection ofbaselineandmonitoringdataismoreintensivethaninStage2,soastoaddressthehigher informationrequirementsofaneliminationcampaign[56,57].Focusisontsetsedata,including longitudinalmonitoringoftsetsedensities[30],agestructure,andnaturalabortionrates(the latteronlyneededtomeasureSIT-inducedabortionrates,ifanSITcomponentisplanned)[26]. At very low tsetse densities, advanced statistical analysis of tsetse catches is needed to measuretheprobabilityofhavingachievedtsetseelimination[30].Despitetheemphasison tsetsedata,essentialAAT[29,58,59]andsocioeconomicdata[60]arestillneeded.

Panel A

Roadmap for the progressive control of AAT in Country X

Panel B

Example of work plan for a 5-year period Country X PCP stage Below stage 1 Stage 1 Stage 3 Stage 4 Stage 5 Stage 2 Year N+4 A A A F H C B B C DD E E F H G G Year N A A F H C D E E H G G B C D F A B C D E F G H 40 1 1 1 1 10 6 40 Zone name Zone area

% of country area Year N Stage 5 Stage 3 Stage 5 Stage 4 Stage 3 Stage 3 Stage 4 N+1 N+2 N+3 N+4 Stage 2 Stage 2 Stage 2 Stage 1 Stage 1 Stage 1

Figure2. Examples ofGeographically-ExplicitRoadmap(Panel A) and Work Plan (Panel B)forthe Progressive ControlofAfrican Animal Trypanosomosis(AAT)inOneHypotheticalCountry(CountryX).InpanelA,CountryX’sinitialsituationisshowntobe‘BelowStage1’;itthenmoves to‘Stage1’atthenationallevel,andsubsequentlycontrolactivitiesarecarriedoutinselectedzones,thusenablingtheseselectedzonestoadvancetohigher progressivecontrolpathways(PCP)stages.InpanelB,onespecificworkplanbyzoneisillustrated(inthisexample,itisa5-yearworkplan).ZoneAisanAAT-freearea, inwhichtheabsenceofAATwasconfirmedthroughsurveyscarriedoutinpreviousstepsoftheroadmap.ZoneBisanareawhereAAToccursandwhichhasbeen prioritizedforAATelimination;eliminationactivitiesareplannedtostartinyearN+3.ZoneCisanareawhereAATisintheprocessofbeingeliminated,andwhereAAT transmissionisplannedtobeinterruptedbytheyearN+4;somecontrolmeasuresareplannedtobemaintainedafteryearN+4.ZoneDisanareawhereAAT transmissionhasbeeninterrupted,butsomecontrolmeasuresarestillinplace;allcontrolmeasuresareplannedtobesuspendedasofyearN+3.ZoneEisanarea whereAAThasbeenreduced,andwhichhasbeenprioritizedforAATeliminationasofyearN+3.ZoneFisanareawhereAAThasbeenreduced,andwherethe reductionisplannedtobesustainedduringthe5-yearperiod.ZoneGisanareawhereAAToccurs,andwhichhasbeenprioritizedforAATreduction/integrated managementasofyearN+2.ZoneHisanareawhereAAToccurs,butwhichhasnotbeenprioritizedforeitherreduction/integratedmanagementorelimination activitiesduringthepresent5-yearworkplan.

In orderto eliminate tsetseflies in thetarget area, asuppression phase focuses onthe reductionoftsetsedensities,whileasecondmop-upphasecompletestheelimination.Arange oftoolscanbeusedintheprocess,eitheralonebutpreferablyincombinationfollowingan integrated pest-management approach. These include the methods alreadymentioned in Stage2,suchasITCandITT.However,moreexpensivemethodscanbeusedinanelimination context[10],suchasSAT[15]andSIT[14,61].Someofthetsetsecontrolmethodsaremore appropriateforsuppression,whileothersaremoreeffectiveforelimination.Forexample,SITis theonlytechniquewithinversedensitydependentefficiency(i.e.,itworksbestwhenwildtsetse densitiesareverylow),soitisparticularlyefficientforelimination[62].

Oncetsetsefliesareeliminated,theneedtocleartheparasitereservoirinlivestockshouldbe evaluated. A blanket treatment may beparticularly important to eliminateT. vivax,whose mechanicaltransmissioncanoccurintheabsenceoftsetse.Controlandsurveillanceof livestockmovementmayalsobenecessarytoreducetheriskofdiseasereintroduction. ComparedwithStage2,AATeliminationrequiresmorecentralized,top-downmanagement andcoordination.Despitethis,farmers’sensitizationandinvolvementremainscrucial.Public information campaigns (e.g., radio, TV, etc.) ensure the engagement and support of the beneficiaries,whocanalsocontributedirectlytothecampaign(e.g.,ifITCisused).

PCP technical and managerial areas Development of technical capacies AAT control acvies Coordinaon and stakeholders involvement Establishment and maintenance of an enabling environment Data collecon, management and analysis

Figure3.ProgressiveControlPathway(PCP)TechnicalandManagerialAreas.WhilsteachPCPstageis characterizedbyspecificgoalsandactivities,fivecomponentscutacrossallstages,albeitwithdifferentemphasis. CoordinationandstakeholdersinvolvementpointstothenotionthatAfricananimaltrypanosomosis(AAT)controlmustbe acollectiveendeavour,whichshouldmobilizeandharnessthecommitmentofdonors,decision-makers,farmers,and extensionservicesalike.CapacitydevelopmentplaysamajorroleintheearlystagesofthePCP,butitmustbesustained throughout,soastoaddressthespecifictechnicalrequirementsofthevariousstages.Epidemiologicaland socio-economicdataarecrucialforanevidence-baseddecisionmaking,startingfromthefeasibilityassessmentand prioritiza-tion,andculminatinginthedemonstrationoftheimpactofinterventions.Thecreationofanenablingenvironmentmust ensurethatthenormative,legal,andtechnicalframeworksareconducivetoasuccessfulandsustainableroll-outofAAT controlinterventions.Finally,AATcontrolinthefieldbeginswithpilotactivitiesinStage1,continuesindifferentways throughthefollowingstages,untilitisinterruptedinStage5.

TransitionfromStage3toStage4islinkedtotheinterruptionofAATtransmission(i.e.,not directlytotheeliminationofthetsetsevector).

Stages4and5

ThefocusofStage4istheeliminationofAATtransmissionandtheestablishmentofAAT-free areas.InStage4themaintenanceofsomeofthecontrolmeasuresdeployedinStage3isstill required.InStage5allcontrolmeasuresarelifted,andthefree-statusshouldbemaintainedin theirabsence.

Amonitoringsystem,includingsentinelherdstoassessAATincidence,isrequiredtoensure theabsenceofcirculationofparasitesandtheabsenceoftsetse(whentsetseeliminationwas targetedinStage3).Serologicaltestsforthedetectionofantibodiesagainsttrypanosomes[12]

ortsetsesalivaantigens[63]couldbeusefultodemonstratetheabsenceofparasitecirculation ortheabsenceoftsetse.

BeyondStage5

ExitfromthePCP(i.e.,‘BeyondStage5’)shouldbelinkedtothedemonstrationofAAT-free status.TheOIEhasdevelopedaprocedurefortheofficialrecognitionofdisease-freestatus.To date, six diseasesareincluded inthis procedure(i.e.,bovine spongiformencephalopathy, FMD,contagiousbovinepleuropneumonia,Africanhorsesickness,PPR,andclassicalswine fever);AATisnotoneofthesesix,meaningthattheOIEdoesnotofficiallyrecognize‘freedom fromAAT’.However,byprovidingtherelevantepidemiologicalevidence,acountrycanprove toapotentialimportingcountrythatitsentireterritoryorazoneisfreefromAAT.Thiswouldbe consideredasaself-declaration.TheOIEmembercountriescanrequestOIEtopublishtheir self-declarationofAATfreedom,recognisingthatthisself-declarationremainsunderthefull responsibilityofthecountryinquestion.

ConcludingRemarksandFuturePerspectives

ThePCPforAATprovidesaffectedcountriesandstakeholderswitharationaltooltoplanand implementstepwiseAATcontrolcampaigns.Inthisopinionpaper,focusisonStages1to3, becausemostcountriesandaffectedareaswillhavetotackletheseearlystages.Also,taking sound initial decisions is crucial in a stepwise approach, especially regarding the choice betweensustainablereductionoreliminationofAAT.Researchhasrecentlyprovidedimproved toolsandmethodologiesto prioritizeinterventionareasandtoselectthe mostappropriate interventionstrategyforeachofthem,takingintoaccounttheenvironmental,epidemiological, andsocioeconomicalsettings(Box1).Inthiscontext,thedevelopmentofupdatedmapsof tsetseandAATatarangeofscalesappearsparticularlyrelevant[7,30–32].

Based onthe presentoutline, a detailed PCP will bedeveloped, also by drawing onthe expertise from AAT-affected countries and a broader range of experts. In particular, the requirementsfortransitionbetweenstageswillbediscussedandmoreaccuratelydefined. TheoverallPCPapproachwaspresented anddebatedintwoworkshopsforAAT-affected countriesinEasternAfrica,organizedbyFAOincollaborationwithAU-PATTEC.Interactions withcountryrepresentativesandotherstakeholdersenabledtheapproachtobeimprovedand tentativeroadmapstobedeveloped.Thetoolwasappreciatedforitscapacitytosupportthe formulationofrationalnationalpoliciesandtopromoteregionalintegration.

ThemaingoalofthisPCPistohelplifttheburdenofAAT.Inthislight,theexistingnormative gaps(e.g.,OIEAAT-specificTerrestrialAnimalHealthCodeChapterandofficialAATstatus recognition)arenotconsideredasmajorhurdles,andaneffectiveroll-outofthePCPappears bothattainableandeminentlydesirable.Toachievethisgoal,thesupportofallstakeholders,

OutstandingQuestions Howcanarationaluseofexisting try-panocides be more effectively pro-motedinthefield?

Howcan investmentinthe develop-mentofnovelveterinarydrugsagainst suchneglected diseasesasAATbe stimulated?

Howcanweimprovethequality assur-anceofAATcontroltoolsavailablein thefield?

Howcannoveldecisionsupporttools be scaled up and more broadly adopted(i.e.,nationalandcontinental atlasesofAATandtsetse,distribution models,mapsoflandscaperesistance to tsetse dispersal, spatially explicit benefit-costanalyses;seeBox1)? Howcanweinvolvethesocial scien-cestofosterinnovationinthecontext offarmer-basedintegratedAAT man-agement(i.e.,Stage2ofthePCP)? Whatmechanismsneedtobeputin place toensure the sustainabilityof farmer-basedintegratedAAT manage-ment(i.e.,Stage2ofthePCP)?

including resource partners, will be crucial. In particular, funding AAT-endemic countries throughthe early stages ofthe PCP will be criticalbefore thebenefits of more advanced PCPstagescanbefullyreaped.

Disclaimer

Theviewsexpressedinthispublicationarethoseoftheauthorsanddonotnecessarilyreflect theviewsorpoliciesoftheFoodandAgricultureOrganizationoftheUnitedNations.

Acknowledgments

ThispaperisaninitiativeofFAO,implementedintheframeworkoftheProgrammeagainstAfricanTrypanosomosis (PAAT).TheinitiativewassupportedbytheFAOsubregionalOfficeforEasternAfricaandbytheGovernmentofItaly(FAO Project‘Improvingfoodsecurityinsub-SaharanAfricabysupportingtheprogressivereductionoftsetse-transmitted trypanosomosisintheframeworkoftheNEPAD’,codesGTFS/RAF/474/ITAandGCP/RAF/502/ITA).J.B.wassupported byCIRADandtheIAEA’sDepartmentofTechnicalCooperation.TheauthorsaregratefultotheOIE,andinparticularto GregorioTorres,fortheguidanceonOIEnormsandprocedures.

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