1.Introduction
WhileCOVIDhasbeenspreadingaroundtheworld,killingatleast7millionhumans,anotherdeadly virushasalsobeenspreading,killingmillionsofbirds.Highpathogenicityavianinfluenza(HPAI)viruses ofsubtypeH5havebeencirculatingsince1996inpoultryandsince2002inwildbirds,infectingmore than300wildbirdspeciesandpoultryinEurope,Africa,AsiaandAmerica.Theyhavealsoinfected thousandsofmammals,includingafewhundredhumans.
ThroughCOVID-19,peoplehavecometounderstandvirusesasrelentlessinnovatorsandadapters.The emergenceofHPAIH5hasmanyoverlapswiththatofCOVID–spillover fromwildanimals,rapidspread intonewdomains,prolificmutationsandgeneticshuffling,leadingtomultiple wavesofinfection.Like coronaviruses,avianinfluenzavirusesarebeneficiariesofglobalisation.Thetransformationoflocal infectionsintoaglobalpanzootichasbeendrivenbyaboomingpoultryindustry,withpoultrynow makingupanestimatedthree-quartersoftheworld’sbirdbiomass[1].
TheonlycontinentsapparentlyfreeofHPAIH5areAustraliaandAntarctica.NewZealandhasalsonot beenaffected.TheconsequencesifitdoesarriveinAustraliaarehardtopredictbut,basedonoverseas experience,couldbedevastatingforwildbirds,aswellaspoultry,andpotentiallyalsoforsome mammals.
HowwellpreparedisAustraliaforitspotentialarrivalandmassinfectionandmortalityofwildbirdsand mammals?Here,wereviewtheglobalorigins,spreadandimpactsofHPAIH5.Wethenconsider Australia’sstateofpreparednessandrecommendmeasuresforboostingAustralia’scapacitytorespond tothegrowingriskstowildlifepopulations.
Box1.Howavianinfluenzavirusesareclassified
AllavianinfluenzavirusesareclassifiedasinfluenzaA.Ofthe4typesofinfluenzaviruses–knownasA,B,Cand D–onlyinfluenzaAisknowntohavecausedpandemics(inhumans)andpanzootics(inanimals)[2].
InfluenzaAviruses(species Alphanifluenzavirusinfluenzae,familyOrthomyxoviridae)areRNAvirusesand classifiedintosubtypesbasedon2typesofproteinonthevirus surfaceandfurtherclassifiedaccordingto whethertheycausesevereormilddiseaseinchickens[2].
TheoutersurfaceofinfluenzaAvirusesisalipidenvelopederivedfromthemembraneofthehost’srespiratory cellfromwhichthevirusbudded.Thisenvelopeisstuddedwiththeproteinshaemagglutinin(H)and neuraminidase(N)[2](Figure1).Haemagglutininisessentialforthevirustoattachtothesurfaceofthehost’s respiratorycellswhileneuraminidaseisessentialforthereleaseofthevirusfromthosecellsandalsofacilitates itspenetrationofmucus[2].
Wildbirds,particularlyducks,geese,swans,shorebirdsandgulls,arereservoirsfor16ofthe18knownH subtypesand9ofthe11knownNsubtypes [1].Morethan130subtypecombinationshavebeenidentifiedin naturesofar,mainlyinwildbirds[2].
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Figure1.Arepresentationofaninfluenzavirus,showingthesurfaceproteinshaemagglutinin(red)and neuraminidase(red)andRNA(green).
Source:USCentersforDiseaseControlandPrevention[3]
Avianinfluenzavirusesarefurtherclassifiedashighorlowpathogenicitybasedontheirabilitytocausedisease inpoultry.SubtypesH5andH7aretheonlyoneswiththecapacitytomutatefromlowtohighpathogenicity formswhenintroducedintopoultry[4].ThecurrentpanzooticwasinitiatedbyavirusclassifiedasH5N1,which emergedasahighlypathogenicformafterinfectingdomesticgeese[5](section2).
InfluenzaAvirusesarehighlyadeptatmodifyingtheirHandN proteins–by(a)mutationand(b)genetic reassortment–whichhelpsthemavoidimmunedetectionbyhosts[6].Theyhaveahighrateofmutations becausetheinfluenzaAenzymethatcopiesRNAforvirusreplicationispronetoerrors [2].Naturalselectionfor andaccumulationofthesemutationscausesgradualchanges intheHandNproteins.AninfluenzaAviruscan alsomodifyitsHandNproteinsbyswappinggeneticmaterialwithotherinfluenzaAviruses.Thisisfacilitatedby thesegmentationofthegeneticmaterialinto8separatebits,eachcodingfor1–3proteins.Virusesthatinfect thesamecellatthesametimecaneasilyswapsegments.
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2.TheoriginsandspreadofHPAIH5
AdiversegroupofinfluenzaAvirusesnaturallyinfectwildaquaticbirdsallovertheworld–mainly ducks,geese,swans,shorebirds,ternsandgulls–andcauseonlymildsymptomsornoneatall [4,7]. Sometimes,thesevirusesspilloverto domesticpoultry,wheretheytypicallyalsocausemildorno disease.But,occasionally,thevirusesofsubtypesH5andH7mutateinpoultryintodeadlystrains,killing upto100%ofinfectedbirds.
Untilrecently,highpathogenicitystrainsofH5andH7werethoughttobe ariskonlyforpoultry.Of42 conversionsoflowpathogenicitytohighpathogenicitystrainsfrom1955to2019,40wererecordedonly inpoultry,whichmeantthatoutbreakscouldbecontrolledbycullingorvaccinatingpoultryflocks[8]. The2exceptionswerea1961eventinSouthAfricathatspilledoverinto ternsandthecurrent panzootic,eachinvolvingtheH5N1subtype[5].
In1996ahighpathogenicitystrainofH5N1emergedindomesticgeese inGuandong,China,killingmore than40%ofinfectedbirds [5].ThefollowingyearitinfecteddomesticchickensinHongKong,andalso peopleworkingwithchickens,resultingin6humandeaths.
Fiveyearslater,H5N1killedwaterbirdsintheHongKongparklands–overturningpresumptionsthatit wasnotariskforwildbirds.Byearly2004ithadspreadto8otherAsiancountries[5].FromMaytoJuly 2005itkilledmorethan6,000wildmigratorybirdsatQinghaiLakeinnorth-westChina[9].By2009it hadbeenreportedfrom38countriesinAfrica,Asia,EuropeandtheMiddleEast [5].
Inthe2010sthethreatescalatedwiththeemergenceofanewlineage(2.3.4.4)thatgaverisetoseveral newNsubtypes(H5N2,H5N6,H5N8)andbecamebetteradaptedtowaterbirdsandmorecapableof infectingmammals[7].Inlate2014H5N1arrivedinCanadaandtheUnitedStatesprobablyviamigratory waterbirds.Asitspread,newvariantsemergedasgeneswereexchangedwithexistinginfluenzastrains inwildbirds.Inmid-2015alargeoutbreakkilledanunknownnumberofwildbirdsandmorethan50 millionpoultrybirds(whichdiedfromdiseaseorwereculled)[7].
OutbreakscontinuedinAsiaandEurope,andsporadicallyinAfrica,sometimeskillingmorethan10,000 birdsatatime [5].From2016to2017,morethan100massmortalityeventsinwildbirdswerereported acrossEurope[4],andfrom2016to2018,massmortality,particularlyofseabirds(ternsandpenguins), wasreportedinAfrica[10].
SinceOctober2021thesituationhasdramaticallyworsened.TheWorldOrganizationforAnimalHealth reportedan‘unprecedentednumberofoutbreaks’with‘analarmingrateofwildbirddie-offs’and infectionsofseaandlandmammals[11].Some400,000wildbirdswerereportedtohavediedinthe8 monthsfromOctober2021toJune2022in2,600outbreaks,althoughthetruetollislikelytohavebeen muchhigher–‘onlyafractionofcasesinwildbirdsarediagnosedandreported’[12,13].
Inlate2022,HPAIreachedCentralandSouthAmerica,spreadingthrough9countrieswithin4months [14].InPeru,morethan60,000seabirdsandsome3,500sealionshavedied[15,16].Thesealionsmay havebeeninfectedduetoclosecontactwithinfectedbirds,buttransmissionbetweensealionshasnot beenruledout[15].
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Figure2.AdeadSouthAmericansealioninPeruduringanoutbreakofavianinfluenzainlate2022 Source:PeruvianNationalForestandWildlifeService[17]
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Figure3ThedistributionofHPAIH5intheUnitedStatesin2021–2022
Source:NationalWildlifeHealthCenter[18]
Thebirdspeciessofarinfectedarehighlydiverse–waterbirdssuchasgeese,ducks,herons,cranesand swans;seabirdssuchasterns,pelicans,gullsandskuas;raptorssuchas eagles,vulturesandowls; shorebirdssuchasknotsandstints;andpasserinessuchascrows[19–22].HPAIH5hasalsoinfected numerousmammalslikelytohavefedoninfectedbirds,including badgers,foxes,bears,wildcats,pigs, dolphins,sealsandsealions [12,23,24].InOctober2022,thevirusprovedapparentlycapableof spreadingbetweenmammalswhenitinfectedalarge(50,000)minkfarminSpain[25].Sofar,onlyabout 900humanshavebeenreportedinfected,abouthalfofwhomdied[23].
TherearenowmanygeneticallydistinctHPAIH5viruscladesincirculation,displayingvaryingdegreesof virulenceandhostrangespecificity.Wildbirds‘areinatransientstatetowardsbecomingareservoir’ [26].ThetrajectoryofHPAIisunpredictable.Numerouslow-andhigh-pathogenicityH5strainsare co-circulatingandavailableforreassortmentwitheachother.Atanytime,strains‘mayarisewith enhancedabilitytotransmittoandamongmammals’[26].
Table1.ThespreadandimpactsofHPAIH5aroundtheworld
1996–2004 Initialoutbreaks
1996 Outbreakindomesticgeese,Guangdong,China
1997 Outbreaksindomesticchickens,HongKong.Alsoinfectshumans.
2002 Outbreakinwildandcaptivewaterbirds,HongKongparklands
2005–10 Wave1
Spread 38countriesinAsia,Europe,Africa,MiddleEast.MainlyaffectedAsia.
Variants H5N1,clade2.2
Wildbirds China(2005):>6,000birdsatQinghaiLakedied,particularlygeese,gullsandcormorants
Poultry >55millionbirdsdied/culled
2011–19 Wave2
Spread Asia,Europe,Africa,NorthAmerica(2014).
Variants Emergenceofclade2.3.4.4,withmultipleH5subtypes
Wildbirds NorthAmerica(2015):Largeoutbreak,unknownnumbers Europe(2016–17):112massmortalityeventsreported,including13,600of71speciesin theNetherlands
SouthAfrica:(2017–18):>7,500of20seabirdspecies,mainlyterns,gannetsandpenguins.
Poultry 140millionbirdsdied/culled
2020–ongoing Wave3
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Spread Asia,Europe,Africa,NorthAmerica(2021),SouthAmerica(2022)
Variants
Wildbirds
Emergenceofclade2.3.4.4b.MainlyH5N1,H5N8subtypes.
Europe(2021–22):3,500detections,37countries,63species.
UK(2021–22):>300outbreaksinseabirdcolonies,30,000–50,000diedonFarneIslands, 13,000barnaclegeesediedonSolwayFirth.
Netherlands(2022):Of18,000breedingpairs,8,000adultsandwichternsdiedandveryfew chicksfledged
France(2022):10%ofthebreedingpopulationofsandwichternsdiedin1week Israel(Dec2021–Jan2022):8,000Eurasiancranesdied
SouthAfrica(2022):24,000Capecormorants,>200Africanpenguinsdied
Peru(2022):60,000seabirdsdied
Poultry
194millionbirdsdied/culled(toNovember2022)
Wildmammals US(2021):bears,seals,raccoonsdied
Peru(2022):3,500sealionsdied
Farmedmammals Spain(2022):>50,000minkdied/culled(probableanimal-to-animaltransmission)
Sources:[4,5,9,10,27–33]. Note:Thedivisioninto3‘waves’isbasedon[27].
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3.TherisksofHPAIH5toAustralianwildlife
3.1RisksofentrytoAustralia
Themainmeansofspreadofavianinfluenzavirusisthrough‘themovementoflivebirds,birdproducts (suchaseggs),fomites[contaminatedobjects],peopleandequipment’[19].Themainpathwaysforthe spreadofHPAIaroundtheworldhavebeenthemigrationofaquaticbirdsthat arereservoirsforavian influenza,aswellasthepoultrytrade[34,35].
TheriskforAustraliaalongboththesepathwayshaslongbeenconsidered‘low’[4]–theonlypoultry meatpermittedforimportationisready-to-eatcookedchickenmeatfromNewZealand[36]and waterbirds(ducks,geeseandswans)donotmigratetoAustralia[37].Themostlikelypathwayfor introductionisshorebirdsandseabirdsmigratingfromAsiaandNorthAmerica[1,37].
Everyspring(fromAugusttoNovember),some8millionshorebirdsofsome 50speciesflytoAustralia alongtheEastAsia/AustralasiaFlyway,whichencompasses37countriesfromArcticRussiaandNorth AmericathroughlargepartsofEastAsiaandallofSoutheastAsia[38,39].Normally,theriskofavian influenzaenteringAustraliaviashorebirdsisconsideredlow[4].Andthusfarthereisnoevidencethat HPAIH5viruseshaveenteredAustralia[37,38].Butwiththeincreasedfrequencyandrangeofoverseas outbreaks,wildlifehealthexpertswarnthattherisksofentrytoAustraliahaveincreased[4,38].
TheunderstandingofHPAIH5infectioninshorebirdsis‘extremelylimited’,butthereisevidencethey ‘couldbeexposed,surviveinfection,andpotentiallydisperse’thevirus overlongdistancesduring migration[38].Researchershaveshownthatred-neckedstintsinAustraliahavepreviouslybeenexposed toHPAIH5viruses–1.5%ofsamplescollectedbetween2011and2018 hadHPAIH5antibodies[38]. Theyrecommendthatthepotentialformigratoryshorebirdstointroduce HPAIH5viruses‘informfuture avianinfluenzasurveillance’.
Thereisalsoariskofmigratoryseabirdsintroducingavianinfluenza toAustralia’sAntarcticand sub-Antarcticterritories[40].NoHPAIoutbreakshavebeenrecorded intheSouthernOcean,butseveral speciesimpactedinthenorthernhemisphere,suchasskuasandterns,migratetoAntarctica.Thearrival ofmigratoryseabirds,mostlybetweenSeptemberandNovember,coincideswiththearrivalofpenguins andotherseabirdsforbreeding[40].
Box2.OutbreaksofhighpathogenicityavianinfluenzainAustralianpoultry
Australiahasrecorded8HPAIoutbreaksinpoultry,allH7subtypes–in1976,1985,1992,1994,1997,2012, 2013and2020[4].Theyareallthoughttohaveresultedfromthe mutationoflowpathogenicityvirus introducedbydirectorindirectcontactwithwildbirds[41].
ModellingofAustralia’soutbreakhistoryindicatesthere areprobablyregularincursionsofavianinfluenzainto poultryflocks,butthatspreadbetweenbirdsandmutationtothehighpathogenicityformoccursonlyrarely. Thisisprobablybecausetheindustryisdominatedbymeatproduction–Australia’sestimated2,000poultry farmsholdcloseto200millionmeatchickensatanytimecomparedwith20millionlayerchickens[42,43]–and
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theproductioncycleinmeatenterprisesisshort(about7weeks),limitingthepotentialforvirusspreadand mutation[41].
WhilelowpathogenicityH7circulatesnaturallyinAustralianwildbirds,theonlydetectionofahigh pathogenicityH7strainhasbeeninaEurasianstarlingtrappedinsideapoultryshedduringthe1985outbreak [4].
ForexoticavianinfluenzavirusesintroducedtoAustraliawithmigratoryshorebirds,thelikelypathwaytopoultry isviawaterbirdsinfectedwhilemixingwithshorebirdsinshorelineorwetlandhabitats.Migratoryshorebirds mostlydonotcomeintocontactwithpoultryfarms[41].
3.2RisksofHPAIH5infectingAustralianwildlife
BecauseHPAIhaspreviouslybeenregardedasadiseaseriskonlyforpoultry,therehasbeenlimited focusontherisksofthecurrentpanzooticforAustralia’swildbirdsandmammals.Noformalrisk assessmentforwildlifehasbeenconducted(asfarasweknow).
The8outbreaksofHPAIinAustralianpoultry,allinvolvingH7subtypes,didnotresultininfectionofwild birdsexceptforasingleEurasianstarling(Box2)[4].Lowpathogenicityavianinfluenzaviruses,including theH5subtype,havebeendetectedinwildbirdsinAustralia,butnotHPAIviruses[19].However,the risksofspreadfrompoultrytowildbirds(andviceversa)haveincreased astheAustralianpoultry industryhasexpanded,particularlyfree-rangeproduction[42].
WildlifeHealthAustraliaadvisesthatallAustralianbirdspecies shouldbeassumedtobesusceptibleto infectionbyHPAIH5[44].SpeciesinfectedelsewherehaveincludedthosenativeorendemictoAustralia (e.g.blackswans,peregrinefalconsandredknots).Thousandsofredknots(listedasendangeredin Australia)havedied–in2021morethan3,000inanoutbreakinGermany[45]andseveralhundred washedashoreintheNetherlands[46].ButthepatternsofdiseaseinAustraliacouldbedifferentfrom elsewhereduetoAustralia’sdistinctiveecologyandphylogeneticdifferences[4].Species’differencesare exemplifiedbyblackswans,whichareconsideredtobe‘atsignificantperil’duetogeneticallycoded differencesintheirimmuneresponsetoviruses[47](Box3).
Since2022,therehasbeenamajorincreaseinoutbreaksofHPAIinseabirdsandseamammals[40]. Colonialnestingseabirdsmaybeathighriskofdiseasespreadbecauseoftheirproximitytoeachother overextendedperiods.Antibodiesagainstavianinfluenzaviruseshavebeen detectedinbirdsin Antarcticaandonsub-Antarcticislands,buttheirpathogenicitywasnotassessed[48].
GiventhelikelyhighsusceptibilityofAustralianwildbirdsandmammalstoHPAIinfectionifH5strains arriveinAustralia,werecommendtheAustralianGovernmentcommissionanexpertassessmentofthe riskstoAustralianwildlife,includingidentifyingspeciesatpotentialhighrisk.TheUnitedNations EnvironmentProgramrecommendsthatallcountriesundertaketransparent,structured,and science-basedriskassessments,makinguseofallavailableknowledge[49].
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Recommendation
❖ TheAustralianGovernmentcommissionanexpertassessmentoftherisksofHPAIforAustralian wildbirdsandmammals,includingthreatenedorhighlysusceptiblespecies.
Box3.TherisksofHPAIforblackswans
Blackswansarelikelytobeatsignificant‘peril’fromHPAI[47].Infectedblackswansincaptivityoverseashave died[50]andthoseinfectedexperimentallywithHPAIalldiedwithin2–3daysafterbecominginfected[51].
Geneticresearchhasrevealedtheylackimmunegenesthathelpswanspeciesfromthenorthernhemisphere andotherwaterbirdscombatcertainviralinfections[47]. Itappearsthatblackswanshavelostsomegeneswith immunefunctionsfromtheancestortheysharedincommonwith otherswanspecies–presumablydueto ‘limitedpathogenchallenge’inAustralia.Theresearchers predictthat‘shouldHPAIbecomemoreprevalentin theOceaniaregion,theongoingsurvivaloftheblackswanwouldbeatsignificantrisk’[47].
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4.Australia’spreparednessforavianinfluenza
Australiahasanationalplanforavianinfluenzafocusedprimarilyonpoultry,aviaryandzoobirds[19]. Therearealsoguidelinesforapublichealthresponsetoavianinfluenzainfectionsinhumans[52].But thereisnonationalresponseplanforHPAIinfectionsinwildbirdsormammals.
4.1Nationalstrategyforavianinfluenza
Australia’s2022 Responsestrategy:Avianinfluenza –anAustralianVeterinaryEmergencyPlan,knownas anAUSVETPLAN–setsoutthe‘nationallyagreedapproach’forrespondingtoavianinfluenzainpoultry, orcage(aviary)orzoobirdssoas‘toensurethatafast,efficientand effectiveresponsecanbe implementedconsistentlyacrossAustraliawithminimaldelay’[19].‘Poultry’meanschickens,turkeys, guineafowl,ducks,geese,quail,pigeons,pheasants,partridges,emusandostrichesrearedorkeptin captivity,includingcommercialandbackyard.
Strategiesforpoultry
Forpoultry,theAUSVETPLANspecifiesapolicyto[19]:
usestampingouttocontrolspreadofHPAI(anysubtype)andLPAI(H5/H7),andtoreducethe potentialformutationofLPAI(H5/H7)virustoHPAIvirus.
Strategiesthatmaybeusedtoachievethisinclude:
● destruction,disposalanddecontaminationofinfectedbirdsandcontaminatedproducts
● biosecuritycontrols(e.g.quarantine,declaredareas,movementcontrols)
● declarationofrestrictedandcontrolareas,withrestrictions onmovementsofbirds,avian productsandassociateditems
● flockorareadepopulationbypre-emptiveslaughter
● increasedbiosecurityatpoultryestablishments(suchasmandatoryhousingof free-range poultry)andpremisesholdingcageorzoobirds.
TheresponseplansaysthatvaccinationofpoultrymaybeconsideredifanH5orH7outbreakislikelyto spreadorhasbecomewidespread.Whilevaccinationwillreducespread,there isconcernbysome expertsthatitcouldincreasetherisksforwildbirdsbyfacilitatingtheemergenceofnewvariants(Box 4).Risksrecognisedintheresponseplanarethatvaccination‘mayfavourtheemergenceofmore virulentvariantsthroughindirectselectionofviruses’and‘couldpossiblymasklowlevelsofcirculating fieldvirusbynotfullypreventingvirusexcretionandbymaskingclinicalsignsinsusceptibleanimals’.We recommendthatthepotentialrisksforwildlifeofpoultryvaccinationbe thefocusofanexpertreview andthatvaccinationofpoultryberuledoutifthereisanincreasedriskforwildlife.
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Strategiesforcageandzoobirds
Thepolicyforhighpathogenicityinfectionsissimilartothatforpoultry– ‘stampingout’.Forlow pathogenicityH5/H7infections,theplanspecifies‘modifiedstampingout’(notimplementedinfull), basedonariskassessment.Theplansaysthatvaccinationmaybeconsideredforcertaincaptivebirdsat riskofinfection,suchas‘captiveendangeredspecies’.
Althoughit’snotclearintheAUSVETPLAN,weassumethestrategyof‘pre-emptiveslaughter’wouldnot applytoaviaryorzoobirds.TheScientificTaskForceonAvianInfluenzaandWildBirds(convenedbytwo UnitedNationsbodies,theConventionontheConservationofMigratorySpeciesofWildAnimalsand theFoodandAgricultureOrganisation)says,‘Thereisnojustificationforanypre-emptivecullingof zoologicalcollections’and‘onlywhennecessary,limitedcullingof affectedbirds’maybewarranted [53].
Strategiesforwildbirds
Effectivebiosecuritybythepoultryindustry–includingtopreventinteractionsbetweenpoultryandwild birdsandrespondeffectivelytooutbreaks–isessentialforprotecting bothwildbirdsandpoultryfrom HPAI.Apartfromthat,thereislittlefocusintheAUSVETPLANonmanagingthe risksandimpactsforwild birds.
IfHPAIinfectionisdetectedinwildbirds,theConsultativeCommitteeonEmergencyAnimalDiseaseswill conveneandcommissionanepidemiologicalriskassessment.Noaction willberequiredunlesstherisk assessmentindicatesan‘unacceptablethreat’topoultryorpublichealth. HPAIinfectionsinwildbirds ‘arenotconsideredtoposeanimmediatethreattoAustralia’sdomesticor zoobirds,ortopublichealth’, sowillnotbetreatedasan‘emergencyanimaldisease’(forthepurposes oftheAUSVETPLAN).Ifa responseisconsiderednecessarytoprotectpoultryorhumanhealth,itmayinclude:
● declarationofrestrictedareas
● surveillancetodeterminetheextentofinfection
● enhancedbiosecurity
● apublicawarenesscampaigntocommunicateriskandpromotecooperationfromindustry,zoos, cagebirdownersandthecommunity
● protectionofpublichealthinconsultationwithhumanhealthauthorities.
Theplanrulesoutdestructionofwildbirdsasbeing‘neitherpracticalnorenvironmentallysound’,other thanforreasonsofanimalwelfare.AnappendixintheAUSVETPLANlistsactionstoconsiderinresponse toHPAIinwildbirds(seesection4.2).
Recommendation
❖ Aspartoftherecommendedriskassessmentforwildlife,reviewthe potentialbenefitsandrisks forwildbirdsofthevaccinationofpoultryagainstavianinfluenza.Donot permitvaccinationof poultryifitwillincreasetherisksforwildbirds.
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Box4.Wouldvaccinationofpoultryincreasetheriskforwildbirds?
Thereisconsiderableglobaldebateaboutwhetherthevaccinationofpoultryagainstavianinfluenzacould increasetherisksforwildbirds[54,55].Poultryvaccinestypicallyreducediseasesymptomsinchickensbutdo notwhollypreventvirusinfectionandtransmission[56].Whiletheywouldreducespilloverfrompoultryinto wildbirdsandhumans[57],ifvirusescontinuetocirculate undetectedinasymptomaticvaccinatedpoultry,it couldspurtheemergenceofnewmore-virulentstrainsthatevadewildbirdimmunedefences:
Akeyconcernistheroleofpoultryvaccinationindrivingendemicityandtheevolutionofantigenically diverseHPAIH5lineages[57].
Poultryvaccinesmayhaveanimpactonwildbirdvirusesthrough thetransmissionofvirulent virusesthathaveevolvedinresponsetotheuseofpoultryvaccines[56].
Vaccinesthatkeephostsalivebutstillallowtransmissioncouldthusallowveryvirulentstrainsto circulateinapopulation[58].
[The]useofleakyvaccinescanfacilitatetheevolutionofpathogenstrainsthatputunvaccinatedhosts atgreaterriskofseveredisease[58].
Thesephenomenahaveprobablycontributedtoepizootics.TheoriginsofcurrentHPAIH5N8epizooticshave beentracedtomutationsofa2.3.4.4blineageinpoultryinEgypt,wherevaccinationisused[57].InChina,the widespreaduseofH9N2vaccinesinchickens‘exertedcontinuousmutationpressure’,whichresultedin increasedvirusinfectivityandledtowidespreadoutbreaks inchickensin2010–13[59].
4.2PlanningforHPAIinfectionsofwildlife
ThereisnonationalHPAIstrategyspecificforrespondingtoinfectionsinwildbirdsandmammals.The AUSVETPLANcontainsanappendixwithactionstoconsider,includingthefollowingforwidespread infection:
● identifyandproclaimrestrictedareas(forexceptionalcircumstances)
● applyappropriatesurveillanceandbiosecuritymeasures;applyenhancedbiosecurityand controlmeasuresatlocalpoultryholdings
● implementenhancedcommunicationsstrategy
● consideruseofvaccinationindomesticpoultryandforcaptivebirds
● consultwithhealthofficialsandenvironmentalofficials.
Thisverylimitedapproachprovideslittleimpetusorguidanceforwildlife managerstoprepareforHPAI infectionsinwildlifeandrespondtoconservationemergencies.
WildlifeHealthAustraliahasprepared GuidelinesforManagementofanEmergencyWildlifeDisease Response,whichprovidesonlygeneral(althoughuseful)guidanceonprocessesandisstillindraftform from2018[60].Theguidelinessaythatthemanagementofaresponsetoaparticularemergencywildlife diseaseneeds‘asimilarbasis’asadiseaseinproductionanimals(i.e.aplansimilartoanAUSVETPLAN). Likewise,aRamsarhandbookonavianinfluenzaadvisesgovernmentstoundertakeriskassessmentsand contingencyplanning,advisedbyanexpertornithologicalpanel,priortoincursionsofavianinfluenza [49].
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Becauseitwouldnotbefeasibletoeradicateavianinfluenzafrominfectedwildbirdpopulations,an outbreakwouldnottriggeraresponseundertheNationalEnvironmentalBiosecurityResponse Agreement.Unlessinfectioninwildlifeisconsideredarisktopoultryorpeopleandthereforetriggers someresponseundertheEmergencyAnimalDiseaseResponseAgreement,anyresponsewould normallybetheresponsibilityofeachstateandterritorygovernment
Thelackofnationalarrangementsforrespondingtowildlifediseasesthatcannotbeeradicatedisa majorgapinbiosecurity.Environmentgroupshaveproposedacategoryof‘emergingkeythreatening processes’undertheEnvironmentProtectionandBiodiversityConservation(EPBC)Act1999thatcould precipitatenationalplanning.Thereneedstobeanagreedprocesstoensurethecollaborationof environmentalandbiosecurityagenciestoprepareforandrespondtoemergingwildlifediseasethreats, whetherornottheycanbeeradicatedfromwildlife.
Thepotentiallyimminentseriousrisksofavianinfluenzawarrantanationalwildlifeplanpreparedand overseenbyanationalwildlifetaskforce.Wediscusspotentialmeasuresfortheproposedplaninsection 4.4.
Recommendations
❖ TheAustralianGovernmentestablishanationalwildlifetaskforce,withmembershipincluding environmentalandbiosecurityagenciesfromallgovernments,WildlifeHealthAustralia,other wildlifeanddiseaseexperts(includingveterinarians),zooorganisationsandenvironmental NGOs.
❖ Thenationalwildlifetaskforceprepareandoverseetheimplementationof anationalwildlife responseplanforavianinfluenza.
4.3Avianinfluenzasurveillance
Australia’sNationalAvianInfluenzaWildBirdSurveillanceProgram,managedbyWildlifeHealth Australia,hasbeenrunningfor18years.Itincludestargetedsurveillance(samplingofwaterbirdswhere theymixwithshorebirdsandwheretheyareincloseproximitytopoultryand humans)andgeneral surveillance(investigationofmassmortalityandmorbidityevents inwildbirdsinAustraliaandthe AustralianAntarcticTerritory)[61].
TheAUSVETPLANsays,‘Surveillanceofwildbirdpopulationswillbecommensuratewiththelevelof assessedriskposedtodomesticbirdpopulations’,whichimpliesthatsurveillanceisnotnecessarily focusedonthepriorityrisksforwildbirdpopulations.
Inlightoftheescalatingincursionrisks,researchershavecalled forenhancedsurveillanceofwildbirdsin thesecondhalfof2023[37].Werecommendthesurveillanceprogrambereviewedbytheproposed nationalwildlifetaskforcetoensurethatitincludessurveillanceprioritiesfortrackingriskstowildbirds, includingseabirds.
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BecauseAustraliaissovast,andmanyshorebird,waterbirdandseabirdpopulationsinhabitremote areas,thebestchancesofdetectingearlysignsofavianinfluenzamaycome fromobservationsby Indigenousrangers,birdwatchers,landmanagersorresearchers.Training shouldbeprovidedtoensure safetyprotocolsarefollowedbythoseparticipatinginsurveillance.
Recommendations
❖ Thenationalwildlifetaskforcereviewthe2023avianinfluenzasurveillanceprogramandprovide adviceaboutsupplementarysurveillanceprioritiesforwildbirdpopulations,includingseabirds. Thiscouldbesupplementedbysurveillance,incooperationwithinternationalpartners,along inwardmigrationpathwaysandintheSouthernOcean.
❖ Thewildlifetaskforcedevelopaprogramtoencouragesurveillancebyindigenousrangers, birdwatchers,landmanagersandresearchers,particularlyinremotelocations.
4.4Potentialmeasuresforpreventingandrespondingtoinfectionsin wildbirds
ThecurrentpolicyundertheAUSVETPLANistostampoutHPAIinpoultryandother captivebirdsby culling.Thisisnotregardedaseffectiveorfeasibleforwildbirdpopulations.Thereisnoeffective treatmentforavianinfluenzainwildbirds(orpoultry)[4].Itisalsonotfeasibletovaccinatewildbirds, althoughthereisapparentlypotentialforafuturevaccinetobedelivered bybait[55].
Themainpotentialstrategiesavailableforwildbirdpopulationsaretolimittheriskofvirusspreadby humanactivities(e.g.restrictingaccesstositesandinteractionswithbirds),removecarcases(toprevent scavengingbysusceptiblespecies),monitorimpacts(toinformunderstandingofthediseaseand recoverypriorities)andconductresearch(tobetterinformriskmitigation).Itisalsoimportanttokeep humanssafebyavoidinginteractionswithsickanimals.
Measuresappliedoverseasandexperienceswithoutbreaksshouldbereviewedtolearnwhatwas effectiveandwhatshouldbeavoided.Onlyafewcountriesororganisationshavepublishedwildbird responseplansorguidance.ThemostdetailedareadvicebyaUNScientificTaskForceonAvian InfluenzaandWildBirds[53],a2010Ramsarhandbook[49],a2022UnitedKingdomplan[62],areport ona2022Britishworkshopplanningfutureresponses[63],andapaperdescribingtheresponseinSouth Africa[29].InAustralia,themanagersofoneimportantbirdsite,thePhillipIslandNatureParks,have takentheinitiativetodevelopalocalresponseplan(seeBox5)[64].Apartfromthat,thereisnopublic evidenceinAustraliaofanysite-basedorjurisdictionalplanningfocused onavianinfluenzainwildlife.
Severalgroupsandresearchersoverseashavenotedalackofpreparednessformassoutbreaksinwild birds.TheUKRoyalSocietyfortheProtectionofBirds,whichmanages222naturereserves,said guidancefromthegovernmentduringoutbreakshad‘beenslowincoming,andoften contradictoryand confusing’[31].Grantedconsentbyoneagencytoburydeadterns,theorganisationwasinvestigatedby anotheragencyforunlawfuldisposal.SouthAfricanresearchersreportedon opportunitieslostduetoa lackofpreparationforoutbreaksincoastalbirds[29].Althoughtherewerebroadguidelinesfordisease
17
response,theyhadnotbeenimplementedatcolonies,which‘resultedinahighlevelofuncertaintyand lackofconfidence’whenmakingdecisions.Thelackofapre-preparedmonitoringplanmeant opportunitieswerelosttogatherinformationaboutthediseasesource,transmission,morbidityand mortality[29].AnanalysisofHPAIinAmericanotedalackofnational mortalitydataforCanada,Central AmericaandSouthAmerica,andthe‘needforeffectivedecisionframingtoprioritizemanagement needsandscientificinquiry’[65].
WedonotrecommendspecificmeasuresforAustralia(becausethatisnotourexpertise).Butbasedon otherplansandguidance,werecommendthatnationalresponseplanningconsiderthefollowingtypes ofmeasures.
Monitoring,reportingandresearch
Inadditiontothenationalsurveillanceprogram,monitoringoflocalsitesisimportantforearlydetection ofavianinfluenzaandthecollectionofdataonimpactsshouldavianinfluenzabedetected.
Documentingreal-timeprogressofthediseasecaninformongoingrisk management,increase understandingofdiseaseepidemiologyandshaperecoverypriorities.Itmayalsobeusefultocollect baselineinformationforsomepopulations.OnerecommendationfromBritainistocollectbaseline informationonraptorsbecausetheyarehighlysusceptiblebuttendtobefound singly,whichmakesit difficulttodeterminepopulation-levelimpacts[63].
Anationalsystemwithprotocolsfordocumentingandreportingavianinfluenzainfectionandmortality inwildbirdpopulationsshouldbeestablishedandpromotedtoenablestandardiseddatacollection. Australiaalreadyhasanemergencyanimaldiseasehotline.
Anationalresponseplancouldspecifystandardisedmethodsformonitoringanddatacollectionand protocolsfortestingforavianinfluenzaininfectedpopulations.Monitoringmethodscouldinclude environmentalDNAtechniques(forvirusdetection)anddronemonitoringofaffectedcoloniestoavoid humanentry(thiswasdoneinPeru[15]).
‘Management-drivenscientificinquiry’isurgentlyneededtodevelopdiseaseresponseprotocolsfor avianinfluenza(andotherwildlifediseases)[65].Itwillbeimportant tolearnasmuchaspossiblefrom diseaseeventstoapplytofutureriskmitigationeffortsandrecoveryefforts.Governmentsshould collaboratewithresearcherstoidentifypriorityresearchquestionsandfacilitatetheimplementationof pre-preparedresearchprojectsshouldHPAIH5reachAustralia.
Regulatinghumanaccessandactivities,biosecuritymeasures
Restrictinghumanaccesstobirdcoloniescanhelptoreducetherisksof virusintroductionandspread andminimiseimpactsonbirdwelfare.TheScientificTaskForceonAvianInfluenzaandWildBirdsadvises considerationofrestrictionssuchassuspendingrecreationalactivities inaffectedsites,with pre-determinedprocessesandstructures[53].
TheAUSVETPLANnotesthepotentialtodeclarearestrictedarea,butsays declaredareasisnota strategyforwildbirdoutbreaks.Whateverthemechanismofrestrictingaccess,decisionswouldhaveto bemadeaboutwhoshouldbepermittedaccess(e.g.researchersandveterinarians)andunderwhat circumstances.Itwouldbeparticularlyimportanttolimitaccessbypeoplewhocomeintocontactwith
18
poultry.Whereaccessispermitted,thereshouldbeprotocolstoreducethe riskofvirusspreadsuchas disinfectionofclothing,footwear,equipmentandvehiclesatkeyaccesspoints.
TheScientificTaskForceonAvianInfluenzaandWildBirdsrecommendsreducingformsofdisturbance thatmayencouragebirdstoflytootherareas[53].Riskassessments ofactivitiessuchasduckhunting, boatingandbirdfeedingwouldhelpinformrestrictions[31,66].
Removinganddisposingofdeadbirds
Thebodiesofbirdskilledbyavianinfluenzarepresentapotentialsourceofinfectionformanydaysor weeksafterdeath.Viralinfectivitycanpersistinfeathersfor15–30daysat20°C[67,68].Thereis emergingevidencefromEuropeanseabirdcoloniesthatcarcassremovalmayreducetheincidenceof avianinfluenzainsomespecies–byreducingscavengingandinteractions withbodies[32].Inthe NetherlandsandBelgium,theregular(every2days)removalofdeadsandwichternswhencase numberswerelowwasestimatedtoreducemortalityby80%[69].
Researchandcase-by-caseassessmentwouldbeneededtoweighupwhetherthepotentialbenefitsof removingasourceofinfectionexceedtherisksofspreadinginfection bycarcasscollectorsandbird disturbance[32].Protocolsforbodycollectionanddisposalwouldneedtobespecified.UndertheUK plan,bodycollectionispermittedinresidentialareasandwherecarcassesmaybescavengedby susceptiblespecies[62].ItisastrategyspecifiedinthePhillipIslandNatureParksplan[64].
Rescuingandeuthanasingwildlife
Considerationshouldbegiventowhethereuthanasiaofinfectedwildbirds bysuitablyqualified veterinarypractitionersonwelfaregroundswouldbepermittedandunderwhat circumstances.InSouth Africaswiftternswithclinicalsignsofavianinfluenzawereeuthanasedwhileendangeredpenguinswith mildormoderatesignswereassessedatawildliferehabilitationcentre[29].TheUKplanallowsfor euthanasia[62].
Therealsoneedtobeplansandprotocolsinplaceforwildliferescuegroups andwildlifehospitals–to limittherisksforinfectionofrescuersandotherwildlifeincareandcollectdata–includingthrough education,riskassessments,quarantine,disinfectionandpotentially vaccination.Thisisnotcoveredin theAUSVETPLAN.IntheNetherlands,alargebirdrescuecentresuffered anoutbreakafteran HPAI-infectedgoosewasadmitted,whichresultedintheinfectionofmorethanathirdofthebirdsin care[70].
Responseplanningforlocalcolonies
PhillipIslandNatureParks,whichhasimportantseabirdpopulationsandoverlapsaRasmarwetland,has developedalocalresponseplanspecifyingtheirintendedprecautionsandactionsfordifferentlevelsof risk(Box5)[64].PlanningandpreparationiswarrantedforotherimportantbirdsitesacrossAustralia. Communicationswithandbetweensitemanagersandotherstakeholderswillbeimportanttosupport preparationfor,responsestoandrecoveryfromoutbreaks,andtoexchangeideasandinformation[63].
Keepinghumanssafeandbuildingpublicawareness 19
Thereshouldbeastrongfocusonhowtolimittherisksofhumansbeinginfectedbyinteractionswith wildbirdsandviceversa.Peopleneedtoknowtonottouchsickordeadbirds andtocontrolpetswhen aroundwildbirds.Theyshouldknowwhatsignsinwildbirdscouldsignifyinfection.WildlifeHealth Australiaadvisesthefollowingcouldindicateinfection[44]:
● smallgroupsorclusters(>3)ofdeadorsickwildbirds.
● individualsickordeadwildbirds,includingforexamplebirdsofprey(eagles, hawks,etc.).
● clinicalsignsthatincludeincoordination,inabilitytostandorfly,diarrhoea,difficultybreathing, increasednasalsecretions,cloudinessoftheeyes.
Vaccinatingcaptive-bredcoloniesofthreatenedspecies
AlthoughtheAUSVETPLANnotesthepotentialforthistooccur,thereisnoguidanceaboutthespecies forwhichitshouldbeconsidered,thecircumstancesunderwhichitshouldoccurandwhetherthereare arrangementsinplacetoprogressthis.
Protectingbirdhabitats
Althoughnotashort-termstrategy,oneimportantmeasureistostrengthenprotectionforwetland habitats.AstudyinChinafoundthattheriskofHPAIoutbreaksforwildbirdswaslowerinproximityto highlyprotectedhabitatsthaninproximitytounprotectedhabitats[71].Theprotectiveeffectwaslikely duebothtotheseparationofwildbirdpopulationsfrompoultryandtheirdiversionfrom human-dominatedlandscapestowardprotectedareas.Risksmayalsobereducedbynotpermittingthe establishmentofnewpoultrybusinessesnearimportantwildbirdhabitats.
Recommendations
❖ Thenationaltaskforcereviewmeasuresappliedinandexperienceswithavianinfluenza outbreaksinoverseasbirdcoloniestolearnwhatwaseffective,whattoavoidandhowto optimiserecoveryafterwards.
❖ Indevelopinganationalresponseplanforwildlife,thenationaltaskforceconsidermeasuresof thefollowingtypes:
(a)monitoring,reportingandresearch
(b)regulatinghumanaccessandactivities
(c)removinganddisposingofdeadbirds
(d)rescuingandeuthanasingwildlife,
(e)responseplanningforlocalcolonies
(f)keepinghumanssafeandbuildingpublicawareness
(g)vaccinatingcaptive-bredcoloniesofthreatenedspecies.
20
Australiangovernmentsencourageandprovidedresourcesformanagersofsiteswithhigh concentrationsofshorebirds,waterbirdsorseabirdstopreparealocalresponseplanforavian influenzaoutbreaksinwildbirds.
Box5.PhillipIslandNatureParksdraftresponseplan
ThisistheonlyAustralianresponseplanforHPAIinwildbirdsthatweareawareof,preparedforPhillipIsland NatureParksin2022[64].Incollaborationwithresearchers,parkmanagershavealsobeenundertaking surveillance.Theyhavespecifiedmeasuresbasedondegreesofrisk.
Lowrisk:(nodetectionofHPAIinAustralia)-actionsfromlateSeptembertoApril
● Monitorfieldsitesforsicknessordeathsofwildlifeprior toundertakinghandling.
● WearappropriatePPEwhenhandlingwildlife,wearclean/disinfectedfootwearandclothingwhen enteringacolonyandusecleanequipment,washhandsbeforeandafter.
● Donotapproachcoloniesifadiseaseoutbreakissuspected(followspecifiedprotocols)
● Undertakestafftrainingonsignsofdiseaseandresponsemeasures
Mediumrisk:(detectionofHPAIinAustralia)
● Minimisemovementsbetweencolonies/areaswithinasingleday
● Wearcleanclothingthathasbeenwashedwithwarmwaterandsoapanddisinfectfootweareveryday andbetweencolonies
● Consideravianinfluenzawhenexamininganylivebirdsintherehabilitationcentre;quarantineanybird showingsymptomsofHPAI
● Keepalogofvisitstofieldsites
● Peoplenottotouchsickordeadwildlife
● Wildlifeprofessionalsshouldavoidcontactwithdomesticbirds,especiallypoultry,for48hourspriorto andafterhandlingwildbirdsormammals
Highrisk:(detectionofHPAIinVictoriaand/ornorthernTasmania)
● Increasefrequencyofmonitoringforunusualbirdmortality
● Recordallcasesofbirdmortality,investigateandreportanyunusualmortalityevents(withthe assistanceofaveterinarian)
● Restrictaccesstosuspectandsusceptiblepopulationsandareas(staffandvisitors)
● Restrictvisitoraccesstosites/areaswherebirdscongregate(boardwalkaccessonly)
● Evenwherecoloniesarenotshowingsignsofinfection,donotassumethatthevirusisnotcirculating. Adoptappropriatebiosecurityandhygieneprecautionswhen carryingoutanyactivitieswithinornear anybirdcolony.
● Establishasatelliterehabilitationfacilityforscreening suspectcases.
Immediaterisk:(spreadingdetectionandmortalitiesinVictoria)
● Undertakeonlyessentialactivitiesinseabirdandsealcoloniese.g.monitoringthatwilldirectly contributetounderstandingtheimpactsoftheoutbreak;allotheractivitiessuspended(research, maintenance,conservationprograms,etc)
● Ceaseallactivitieswhichrequirehandlingofwildlifeunlesstheydirectlyrelatetomitigationmeasures ordiseaseoutbreakmonitoring
● IncreasePPEtoincludeN95facemask,safetyglassesanddisposableoveralls
● Considerclosureofareas(includingpenguincolonies)withhighscalemortalities
● Undernocircumstancesshouldanyonewhoownsorworkswithdomesticpoultrycomeintocontact withanybirdsuspectedofcarryingavianinfluenza;nopersonwhohasworkedwithasuspectedbird shouldvisitanyareaswheredomesticpoultryarekeptforatleasttwoweeks.
● Undertakedailymonitoringforunusualbirdmortalityatkeylocations.
❖
21
● Removecarcassesandsickbirdsasdeemedappropriate
● Conductdailycountsofmortalityandroutinetestingofsuspiciouscases.
22
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