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1 ZoonosesinPetbirds:reviewand 2 perspectives 3 BOSERET,Geraldine(1),LOSSON,Bertrand(2),MAINIL,JacquesG(3),THIRY,Etienne 4 (4),SAEGERMAN,Claude.(1) 5 (1) Epidemiologyandriskanalysisappliedtoveterinarysciences(UREAR-ULg),department 6 ofinfectiousandparasiticdiseases,FacultyofVeterinaryMedicine,UniversityofLiège, 7 4000Liège,Belgium 8 (2) 9 Parasitology,departmentofinfectiousandparasiticdiseases,FacultyofVeterinary Medicine,UniversityofLiège,4000Liège,Belgium 10 (3) 11 Bacteriologyandpathologyofbacterialdiseases,departmentofinfectiousandparasitic diseases,FacultyofVeterinaryMedicine,UniversityofLiège,4000Liège,Belgium 12 (4) 13 Virology,departmentofinfectiousandparasiticdiseases,FacultyofVeterinaryMedicine, UniversityofLiège,4000Liège,Belgium 14 Authorsemailaddresses: 15 [email protected] 16 [email protected] 17 [email protected] 18 [email protected] 19 [email protected](correspondingauthor) 20 1 21 Table of contents 22 Abstract ................................................................................................................................................... 3 23 1. Introduction..................................................................................................................................... 3 24 2. Main transmission routes ................................................................................................................ 5 25 2.1 Direct contact : ........................................................................................................................ 5 26 2.1.1 Households ...................................................................................................................... 5 27 2.1.2 Petshops, bird fairs and markets ..................................................................................... 7 28 2.1.3 International trade .......................................................................................................... 7 29 2.2 Vector borne transmission ...................................................................................................... 8 30 2.2.1 Mites ................................................................................................................................ 8 31 2.2.2 Mosquitoes .................................................................................................................... 10 32 2.2.3 Ticks ............................................................................................................................... 11 33 3. 34 Most important diseases ............................................................................................................... 12 3.1 Bacterial diseases .................................................................................................................. 12 35 3.1.1 Chlamydophilosis........................................................................................................... 12 36 3.1.2 Salmonellosis ................................................................................................................. 14 37 3.1.3 Tuberculosis................................................................................................................... 15 38 3.1.4 Campylobacter jejuni..................................................................................................... 17 39 3.1.5 Lyme disease ................................................................................................................. 17 40 3.1.6 Others ............................................................................................................................ 18 41 3.2 Viral diseases ......................................................................................................................... 18 42 3.2.1 Avian influenza .............................................................................................................. 18 43 3.2.2 Arboviruses .................................................................................................................... 19 44 3.2.3 Others ............................................................................................................................ 20 45 3.3 Parasitic/fungal diseases ....................................................................................................... 21 46 3.3.1 Toxoplasmosis ............................................................................................................... 21 47 3.3.2 Cryptococcosis ............................................................................................................... 21 48 3.3.3 Others ............................................................................................................................ 22 49 4. Guidelines to prevent transmission from birds to humans .......................................................... 23 50 4.1 Household hygiene ................................................................................................................ 23 51 4.2 Birds’origin traceability : ....................................................................................................... 24 52 4.3 Awareness of sickness signs .................................................................................................. 25 53 4.4 Biosecurity and hygiene precautions in big facilities ............................................................ 26 54 5. Conclusion ..................................................................................................................................... 30 2 55 56 Abstract 57 Petbirdsareanot-so-wellknownveterinarian’sclientshipfraction.Bought 58 individuallyorincouples,asfamiliesoftendo(whichisalucrativebusinessforpet 59 shopsorlocalbreeders)ortraded(sometimesillegaly)fortheirveryhighgeneticor 60 exoticvalue,thesebirds,commonlycanaries,parakeetsorparrots,areregularly 61 soldathighprices.Theseanimalshoweverarepotentialcarriersand/or 62 transmittersofzoonoticdiseases.Someofthemcouldhaveanimportantimpacton 63 humanhealth,likechlamydophilosis,salmonellosisorevenhighlypathogenicavian 64 influenzaAH5N1.Thisreviewpaperalthoughnonexhausiveaimsatenlightening, 65 bythedescriptionofseveralcasesofbirds-humanstransmission,therisks 66 encounteredbybirdsowners,includingchildren.Publichealthconsequenceswillbe 67 discussedandemphasiswillbemadeonsomevector-bornediseases,knowntobe 68 emergentorwhichareunderestimated,likethosetransmittedbytheredmite 69 Dermanyssus gallinae.Finally,biosecurityandhygiene,aswellasprevention 70 guidelineswillbedevelopedandperspectivesproposed. 71 Keywords: zoonoses, petbirds, public health, trade, biosecurity, infectious diseases, 72 veterinary medicine, canaries, psittacines, passeriforms. 73 1. Introduction 74 Theterm«Petbird»designatesbirdshousedandbreededforanexclusively 75 ornamentaluse.Thiscategoryincludesandwillreferlaterinthispapertomainly 76 Passeriformes(e.g.canaries,finches,sparrows:seetable1),alsocalledsongbirds, 77 andPsittaciformes(parrots,parakeets,budgerigars,lovebirds:seetable1)[1-3], 3 78 andisaratherunknownvet’sclientshipfraction.Astatisticalstudymadebythe 79 AmericanVeterinaryMedicineAssociation(AVMA)repertoried11to16millions 80 companionandexoticbirdsintheUnitedStatesin2007[4].In2010,followinga 81 studymadebytheFACCO(chambresyndicaledesFabricantsd'Alimentspréparés 82 pourChiens,Chats,Oiseauxetautresanimauxfamiliers),6millionsofpetbirdsare 83 ownedbyFrenchpeople[5].InBelgium,everybredbirdhastobeidentifiedbya 84 ringsharinganumberdirectlyconnectedtothebreeding’sowner(Arrêtédu 85 Gouvernementwallonfixantdesdérogationsauxmesuresdeprotectiondes 86 oiseaux,AM2003-11-27).In2011,theAssociationOrnithologiquedeBelgique 87 (AOB)recensed249ornithologicsocietiesauthorizedtoidentifytheirbirdsbyan 88 officialring. 89 Manyfamiliesowntheir«kitchenpetbird»,whichrepresentalucrativebusiness 90 forpetshopsorlocalbreeders,asasinglecanarymaleissoldaround30eurosin 91 Belgiumandafemalearound20euros.Pricesareaboutthesameforzebrafinches 92 orbudgerigars,and50%to100%higherfor«special»fincheslikeGoulddiamonds. 93 Birdfairsandlivebirdsmarketsalsogatheredalotofpeople.Besides,somespecies 94 arebredfortheirveryhighvalue;forexample,inthecaseofcanaries,maleand 95 femalebreedingstockreproductorswithrecognizedgeneticpotentialarepresented 96 innationalandinternationalcontestsfortheirposture(theBossuBelge),their 97 colour(redmosaic)orfortheirsong(Harzer).Asaconsequence,theiroffsprings 98 couldbesoldathighforrisingprices.Finally,exoticbirdslikegreaterpsittaciforms 99 (parrots,e.g.ara,cockatoo),legallyorillegalytradedfromforexampleAsiaorSouth 100 America,remainhighintheclassementofpopularpetsandarealsoprofusely 101 representedinzoosandparks. 4 102 Notwithstandingthesesocio-economicfacts,theseanimalsarepotentialcarriers 103 and/ortransmittersofzoonoticdiseases.Someofthesepathologiescouldhavean 104 importantimpactonhumanhealth,likechlamydophilosis,salmonellosisoreven 105 highlypathogenicavianinfluenzaAH5N1,butalsohaveaneconomicimpactifsome 106 ofthesepathogensarespreadviacarriersorvectorslikewildbirds,humanbeings, 107 insectsormitestopoultrybreedingunitsorcattlefacilities[6],enteringthenthe 108 foodchain.Theaimofthisreviewistoenlightenanddiscusstherisksencountered 109 bybirdshandlers(includingchildren),professionalworkers(e.g.veterinarians, 110 traders,shopowners)inparticularandhumanpopulationingeneral,andtoassess 111 theeventualhealthandeconomicconsequences,andproposesomeguidelinesto 112 preventtransmissionfromsuchbirdstohumans. 113 2. Main transmission routes 114 2.1 115 Direct contact : 2.1.1 Households 116 Passeriformsandpsittacinesarehousedunderdifferentconditions,duetotheir 117 respectivebehavior.Indeed,psittacines,especiallyparrots,aremoreaggressive 118 thanpasserinesandwouldthenratherbekeptinpairsthangroups[2,3].However, 119 relativelyhighnumbersofbudgerigarscanbegatheredtemporarilyinthesame 120 cageforexampleinpetshopsfacilitiesormarkets. 121 Besidesthe“kitchen-housing”,usuallyasinglecagecontainingtypicallyacoupleof 122 canariesorbudgerigarsforexample,passeriformspeciesarepreferentlykeptin 123 captivityintwodifferenttypesofaviaries[2]:mixedornamentalaviariesand 124 breedingfacilities.Thefirsttypeisusuallyabigwire-nettingspace(upto10m³) 5 125 locatedoutsideandsometimeswithdifferentspecieskepttogether,mostlyfor 126 ornamentalpurposes[2].Inthesecondtype,relativelylargenumbersofthesame 127 species,dependingonthebreedingsizeandthebreedingpurpose(petshopsversus 128 competitions)aremaintainedinpairs,mostlyindoors(butsometimeswithapartial 129 accesstotheoutside).Inbothtypes,newindividualsareregularlyintroduced,inthe 130 firstcaseinapurposeofornamentaldiversificationandinthesecond,tobringnew 131 bloodinthegeneticdiversityofbirds.Thesemovementsaresupposedtobe 132 precededbyaquarantineofthenewincomers. 133 Severaltimesayear,performantbirdsarebroughttoshowsandcompetitions, 134 whereexchangeorsellingcouldoccur,andbythesameway,transmissionof 135 pathogens,asthiswaswellillustratedbyseveralauthors([7,8]).Inthecaseofthe 136 “kitchen-canary”,thiscouldbeinterestingtomentionthatinthesummer,thecages 137 couldbemovedoutside,inordertoallowthebirdtosunbath.Thiscouldbea 138 favorisatingconditionforcontactsbetweenwildandcaptivepasserines(Boseret, 139 pers.obs.).Thisisalsonotarareeventtohavecanariesescapedfromtheircage, 140 withapotentialrisktodisseminatepathogensintoawildavianpopulation, 141 pathogenswhichtheycouldhavecontractedintheiroriginalbreedingfacilityor 142 fromhumans(forexample,chlamydophilosis[8]).Predators,likecats,couldalsobe 143 infected.Thequestionwhetherbirds’predatorscouldbecomeeventuallysentinels 144 hastoberaisedandneedstobefurtherinvestigated.Finally,oneshouldnotforget 145 otherpotentialzoonoticpathogensshedders,likearthropodsorrodentswhich 146 couldalsofindaneasilyreachablesourceoffoodincages(Boseret,pers.obs.)or 147 directlyonbirdsthemselves,asthiscouldbethecaseforhaematophagousinsects. 148 [9,10]. 6 149 2.1.2 Petshops, bird fairs and markets 150 Indirectrelationshipwithlocalbreeders,housingofbirdsinpetshopfacilities 151 enhancestheriskoftransferofseveralzoonoses,likeforexamplechlamydophilosis 152 [8].Cagesareindeedoftenovercrowded,filledwithbirdsfrommixedorigin[8].The 153 overcrowdingalsoinducesintensestresstothebirdsduetothefightforfemales, 154 territory(whichisextremelylimitedinthiscase)orfood.Thiswillcausequick 155 debilitationofweakestindividuesandhighersensitivitytoinfections[11].This 156 situationisparticularlytrueinliveanimalsmarketsasrepresentedinnumerous 157 studiesperformedinAsiancountries[12,13].Unfortunately,nodataareavailable 158 forEuropeancountries. Butthisisaquitefrequentobservationthatpetbirdsare 159 sharingthesamespacethanpoultry,makingeasiertransmissionofpathogensand 160 parasites(e.g.Dermanyssus gallinae). 161 Finally,birdfairsconstitutealastexampleofcontaminationpossibility.Inthese 162 regional,nationalorinternationalgatherings,breedersmeeteachotherandpresent 163 theirproduction,inacontextofchampionships.Casesoftransmissionof 164 Chlamydophila psittacifrombirds-to-humaninsuchconditionshavebeenrecently 165 relatedinFranceandtheNetherlandsbyrespectivelyBelchior,andBerkand 166 collaborators[7,14].Inbothcases,clinicalsymptomsweredevelopedbypatients 167 andledinseveralcasestohospitalization. 168 2.1.3 International trade 169 Asillustratedbyseveralauthors,controlledaswellasnon-controlledmovementsof 170 birdscouldenhancetheintroductionofzoonoticpathogens(likechlamydophilosis 171 orhighlypathogenicavianinfluenzaA)andtheirvectors(likeD. gallinae)innon- 172 endemiccountries[15-18].Indeedthisremainsstillproblematictoobtainaccurate 173 estimationofwildlifetradeasmostofthetimeitisconductedthroughnon-official 7 174 andnon-legalroutes([19-21]).Itmustbepointedoutthatillegalwildlifetradefor 175 e.a.companionorornamentalpetsranksintermsofeconomicactivitiessecondto 176 theillegalnarcotictrade([22]).Inadditiontothishugefinancialimpact,this 177 situationreflectsalsoanon-negligeablethreatforhumanhealthsinceitfacilitates 178 multiplicationandcirculationofzoonoticpathogensandshouldfacilitateadaptation 179 ofthesepathogenstonewhosts([16][22]).Onanotherhand,controlling 180 movementsisnottheabsolutewaytopreventpathogenstransmission.Royand 181 Burnonfossehaveillustratedthisfactthroughtheirstudyonnuclearandsequence 182 dataanalysisofpestspecies[18]whereinauthorsshowedthatcommercial 183 exchangescouldhaveanimpactoninternationalgeneflowsinpopulationsofD. 184 gallinae,eveninahighlycontrolledcontext(forexample,quarantinemeasuresin 185 industriallayerfarms). 186 2.2 187 Vector borne transmission 2.2.1 Mites 188 Vector-bornediseasesrepresentamajorproblemforpublichealth.Bird 189 ectoparasites,especiallymesostigmaticmitesbelongingtoDermanyssidaeand 190 Macronyssidae,arewellknownfortheirheavypotentialtotransmitdiseasesto 191 poultry.Dermanyssus gallinaeinparticular,evenifexhaustivelydescribedinpoultry 192 breedings,isalsoapetbirdpathogenratherunderestimated.Thismiteisoftenfound 193 inbothpetbirdsfamilyhouseholdandintensivebreedings.D. gallinae isanocturnal 194 haematophagousectoparasiteandhasbeendescribedtocauseanimportant 195 debilitationbyexsanguination,involvinghighmortalityrateinnewborns,and 196 sometimesinhens,D. gallinaehasbeenalsoprovedtotransmitzoonotic 197 pathogens[23-25],suchasC. psittaci[26],Coxiella burnetii[24,25],Salmonella spp. 8 198 [27-29],Erysipelothrix rhusiopathiae[30,31],Listeria monocytogenes[24,25]and 199 viruseslikeFowlpoxvirus[24].Moreover,evidenceoftransmissiontohumanshas 200 beendescribed,withsubsequentapparitionofskinlesionsandadermatological 201 pruriticsyndrome.[32-38] D. gallinaeischaracterizedbyaspecificthigmotactic 202 behaviorandspendsmostofitslifeinthebird’senvironmentratherthanonthehost 203 itself,especiallyinnarrowintersticeslikeperches,feedingbowlsandsandtrays 204 anfractuosities;itactsmorelikeamosquitoorabedbugthanlikeotherparasites,as 205 itonlyoccasionallybitesitshoststotakeabloodmeal[39].Inadditiontocomplicate 206 earlydetectionofthemite(contrarytootherparasitesspendingmostoftheirlifeon 207 thebird,likee.g.theblood-suckingmiteOrnithonyssus silviarum-seealsobelow),this 208 particularlifetraitmakestheparasitehardtoeliminatebyantiparasiticspray 209 treatment(e.g.organo-phosphorus,pyrethrinoids)[40].Atopictreatment,with 210 applicationofalong-termremanentantiparasiticspot-onproduct(e.g.0,1% 211 ivermectine)directlyonthebirds’skin,hasbeensuggestedbyDorrestein[41];this 212 alternativehowevermightnotbeeasilyapplicableinlargebreedingsandbig 213 facilities. 214 D. gallinaecouldbeconsideredasaninvasivespeciespresentingahostspectrum 215 especiallywide,ofmorethan40birdsfamilies(includingPasseriforms[39,40]). 216 Hypothesishasbeenformulatedthattheseparasitescouldbeeasilytransmitted 217 horizontally,fromoneinfestedbirdnesttoanothercloseone[42]orinthecaseof 218 mixtcolonies[43])orfromwildbirds(e.g.passerines)feedinginopenairtogether 219 withdomesticspecies[40].Thiscouldalsorepresentawayoftransmissionto 220 humans.Indeedithasbeenwelldescribedthatpigeonsdonestinthevicinityof 221 humans(suchascitybuildings,includinghospitals[44])andseveralcasestudies 222 havepresentedtheevidenceofD. gallinaepopulationsclosetoabandonedpigeons 9 223 perchesornests,nearwindowsoraerationcircuitry[2,35].Suchinfestationhas 224 beenputtedindirectrelationshipwithdermatologicclinicalsyndromesinhumans 225 (“pseudo-scabies”),associatedwithpruriticsyndrome[32-38].AsD. gallinaehas 226 beenprovedtobesheddingzoonoticpathogens[28,37]andasbirdslikepigeonsare 227 foundtobeperchingalongsidehospitalwalls[35],onecouldpointouttheeventual 228 risksencounteredbyimmunocompromisedhumans,ashospitalizedpeople,ifthey 229 experiencedsuchsituation. 230 Ornithonyssus sylviarum(Macronissidae),alsonamedNorthernFowlmiteorwhite 231 poultrymiteisanotherblood-suckingarthropodidentifiedinpetbirds.Clinical 232 symptomsaresimilartothosedevelopedbyaD. gallinaeinfestation:depression, 233 anemia,newbornsmortality[41].However,O. sylviarumbehaviorisnotably 234 differentfromD. gallinae’s,asitspentitsentirelifeonthehost’sbody,makingpest 235 detectioninsomewayeasier[41,45].O. sylviarumhasbeenisolatedinwildavifauna 236 andpetbirds;itshowedtheabilitytoquititshostandreachbirdsevenhousedin 237 othercages.However,itscapacitytoresistfromstarvation(i.e.livinginabsenceof 238 anyhost)intheenvironmentissignificantlyshorterthantheredmite’s(resp.3 239 weeksand24weeks[45]).Onlyafewcaseofzoonotictransmissiontohumanshave 240 beenreported,withclinicalsignsrestrictedtodermatologicsymptomsassociated 241 withprurit[46].Nonetheless,O. sylviarumisconsideredtobeemergentinEurope 242 andtopresentanincreasinglyprobleminaviaries[41]andshouldthenbenot 243 neglected. 244 2.2.2 Mosquitoes 245 Differentspeciesofmosquitoes(Diptera,especiallyCulexspecies)areresponsiblefor 246 horizontalandreciprocidtransmissionofarboviruseslikeWestNilefeverVirus 10 247 (WNV;[47,48])orUsutuvirus([49]).Thesediseaseswillbediscussedfurtherinthe 248 nextsection. 249 Dipteraeactasbridgingvectorsbetweentwohostscategories:amplificators(e.g. 250 birds)andincidental/dead-end(e.a.humans).FollowingTurell,Sardeliset 251 collaborators([50][51],citedin[47]),aninfectedvertebratemustpresentaviremia 252 of105pfu/ml(pfu:plateformingunit)tobeefficientasanamplificationhost. 253 StudieshaveshownthathousesparrowsdevelopWNVviremiasuperiorto1010 254 pfu/mlafterexperimentalinfection,andmaintainitabove105pfu/mlforfivedays 255 [47,52,53]andareindeedgoodamplificatorshostsand,moreoveroverwintering 256 hosts[48]foratleastonearbovirus,theWNV.Besidetheseeffectsofamplification 257 andseasonalresistance,internationalexchanges,tradeandmigrationarefactors 258 enhancingtheseviraldiseasesemergence,asshownbytheincreasingnumberof 259 diagnosedinfectionsacquiredduringstaysintropicalcountries.Interestingly,Pfeffer 260 andDobler[53]pointedoutthefactthatnoattentionisactuallypaidon 261 accompanyingpetanimalsandparasitesthatthesepetscouldbecarrying.Petbirds 262 arealsoconcernedasalargeamountofcompanionbirdsareobtainedbysellersfrom 263 tradewithexoticcountries[15,53]. 264 2.2.3 Ticks 265 TicksfromthegenusIxodes(e.g.I. ricinus,I.scapularis),arecarriedbybirdsandthen 266 havetheabilitytotransmitpathogenslikeBorrelia burgdoferi,causativeagentofthe 267 Lymedisease,andtheflavivirusloupingillvirus.Migratingbirdsalsocouldbe 268 carriersofinfectedticksandthencontributetolongdistancedispersalofboth 269 vectorsandspirochetes[54].Mathersetcollaboratorshaverecentlypublisheda 270 interestingstudyonthepotentialroleofwildbirdsandtheticks thatfeedonthemin 11 271 theintroductionoftheagentofLymediseasetoemergentareas[55].Noevidence 272 howeverhasbeenreportedoftransmissionfromwildtodomesticpetbirdseven 273 housedinopenairaviaries. 274 3. Most important diseases 275 Note:table5summarizesthemaindiseasesdescribedbelowintermofclinicalsigns 276 andnecropticlesionspresentedbybirds,recommendeddiagnostictoolsandtreatment, 277 andsymptomatologyreportedinhumans. 278 279 3.1 Bacterial diseases 3.1.1 Chlamydophilosis 280 Oneofthemostthreateningzoonoticdiseasestransmittedbybirdstohumansis 281 chlamydophilosis(alsoknownaschlamydiosis,ornithosis,psittacosisorparrot 282 fever),causedbytheintracellularbacteriumChlamydophila psittaci.Psittacine 283 speciesarehighlysensitivetothispathogen,butpasserinesarenotexcluded[26,41, 284 56].Humansymptomscomefrommildrespiratorysignstoseverepneumonia,with 285 localizationinseveralorgansleadingtodiarrhoea,cunjunctivitis,arthritisand 286 genitalorgansinfection.Thefirstpeoplesusceptibletobeinfectedappeartobe,as 287 expected,veterinariansandbirdsbreeders;thishasbeene.g.enlightenedbythetwo 288 followingstudies.Thefirstreportedanaccidentalcontaminationofavetbyinfected 289 turkeys[57];thesecond,anepidemiologicalstudymadebyGhentuniversity, 290 pointedoutahighpercentageofhumaninfectioninownersandvetsworkingin 291 breedingpsittacinefacilities[8].On39breedingsfacilities,whichrepresent308 292 birds(mostofthempsittacineslikecockatoos,parrots,parakeetsandlories)and46 293 humans,19.2%ofbirdsweretestedpositiveforC. psittacibynestedPCR/EIA,13% 12 294 ofpetowners(andthevetstudentinchargeofthestudy)werealsopositiveafter 295 swappharyngealsampling.Atotalof66%ofthepositivepeoplepresentedmild 296 respiratorysymptoms,inassociationwithviableC. psittaciisolation.VanRompay 297 andcollaboratorsconcludedtheirinvestigationwithanimportantobservation:on 298 18breedingsfacilities,despiteabroadspectrum-antibiotherapy,60.6%werestill 299 positivefor C. psittaci throughculture andPCR(16.6%and44%respectively)[8]. 300 Thisraisesthepointofantibioticresistanceanddevelopmentofdrug-resistant 301 strainsinsomefacilities. 302 AnotherinterestingcasewasdescribedinaLiègehospital(Belgium),wherea10- 303 yearoldchildwasadmittedforpersistantfever,acuteabdomen,pneumoniaand 304 neurologicsymptoms[58].Thepathogen,furtheridentifiedasC. psittaci,was 305 cefotaxime-resistant.Twobudgerigars(thesecondmostpopularpetbird)were 306 housedinthechild’slivingplace;theelderbrotherofthischildpresentedahigh 307 levelofanti-C. psittaciIgA,whichsuggestedanon-symptomaticchlamydophilosis. 308 DirecttransmissionofC. psittacifrombirdstohumanshasbeenputtedinevidence 309 inacompendiumofsecuritymeasuresaboutavianchlamydophilosiseditedbythe 310 CentreofDiseasesControlandPreventionin1998,andwarnedbirdsowners(43% 311 ofinfectedpeopleinUSAbetween1987and1996)butalsoprofessionalsworking 312 withbirdslikee.g.veterinarians,breeders,zooworkerstobeawareofarealriskof 313 zoonotictransmission[59].Birdfairsareagoodillustrationoftheoccupationalrisk 314 presentedbyahighconcentrationofpeopleandbirdsinthethesamespacefora 315 relativelylongperiodoftime.BelchiorandBerkreportedrecentlytwosimilarevents 316 inrespectivelyFranceandtheNetherlands,wherechlamydophilosisoutbreaks 317 occurredduringbirdfairs.InBelchiorstudy,68%ofexhibitorsweretestedpositive 318 forC. psittaci infection[7,14]. 13 319 Finally,onehastomentionacaseofillegalyimportedchlamydophila psittaci-positive 320 psittacineoccurredintheAntwerpcustom,whichledtocustomofficer 321 hospitalizationafterhandlinginfectedparakeets[15,17]. 322 Thispointouttherealthreatpetbirdscouldrepresentwhenlittleinformationon 323 biosecurityisprovidedtothepeoplebreedingand/orhandlingthem.D. gallinae 324 couldmoreovertransferthispathogen[24-26].Thisreinforcestheurgentneedto 325 applyhygienicmeasuresonplaceatrisk,e.a.birdsfairs,petshopsfacilitiesandsmall 326 familialbreedingunits.TheCDCcompendiumofmeasurestocontrolChlamydophila 327 328 3.1.2 psittaci infection would be in this sight of a great help [59].Salmonellosis 329 Salmonellaspecieswereisolatedfromseveralcaptivepasserineorpsittacinebirds, 330 inrelationornot(asymptomaticcarriage)withclinicalsymptoms:diarrhea, 331 multisystemdisease,septicaemia,osteomyelitis,depression,cropstasis, 332 dehydration,anorexia[60,61],[62,63][56].TheserovarTyphimurium,awell- 333 knownzoonoticagent,wasdescribedinpasserinebirdsinsuchclinical 334 manifestationsasgranulomas(liver,ceca,spleen),multisystemicsymptoms,ocular 335 lesionsandosteomyelitis[61],[64].Transmissiontohumanswasreportedin 336 differentcases[63][65,66].Smithetcollaboratorsalsoreportedtwocasesof 337 Salmonella typhimuriumoutbreaksinelementaryschoolsrelatedtoowlpellets 338 dissection[67].Evenifthesecasesaremoreanecdoticalthanquitefrequent,men 339 shouldbecareful(andatleastrespectelementaryhygienicrules)when 340 manipulatingbirds’productssuchaswildbirdpellets,whichcouldbeinasomehow 341 comprehensivewayundertakenasadidactivemannertoteachnaturetokids. 342 Anotherpointofviewistheproblematicofwildreservoirs.Indeed,wildsongbirds 343 havebeenrepeatedlydocumentedasSalmonella spp. carriers[68,69]andimplicated 14 344 inthetransmissionofthesepathogenstohumansandmammals.Inparticular, 345 starlingswereshowntobepotentialspreadagentsofsalmonellosisincattlefeeding 346 operations[6].Linkedtothatfact,bovineherdshavebeendemonstratedtobe 347 reservoirsofmanygastro-intestinalpathogensbeingofconcerntohumans, 348 especiallyprofessionalslikelivestockproducersorveterinarians[70],aswellas 349 consumers[71]. 350 Finally,asdiscussedinchaptersabove,D. gallinaeseemstoplayasignificantrolein 351 Salmonella spp.Transmissioninlayerfarms,asdevelopedbyMoroandcollaborators 352 [23,27-29]. 353 3.1.3 Tuberculosis 354 IsolationofzoonoticagentsfromtheMycobacterium species isnotsorareinpet 355 birds,especiallyinpsittacines.Themostcommonlyisolatedspeciesarerespectively 356 Mycobacterium genavenseandMycobacterium avium[72][56].Themainspecies 357 causingtuberculosisinhumans,i.e.M. tuberculosis,hasbeenrarelyreportedinbirds, 358 andessentiallyinparrots.Inthisparticularbirds’family,ainterestingobservation 359 shouldtobepointedout,asitseemsthatthemainrouteofinfectionwasofhuman 360 origin.Welldocumentedexamplesarethesegreen-wingedmacaws(Ara chloroptera) 361 diagnosedpositiveforMycobacterium tuberculosis, thefirst inNewYorkCity[73]and 362 thesecondinSwitzerland[74].Bothbirdsdevelopedapanelofclinicalssigns 363 associatedwithtuberculosis:lethargy,osteomyelitis,multifocalgranulomatous 364 panniculitisandgranulomatoushepatitis.Birdownersinbothcaseshadahistoryof 365 culture-confirmedpulmonarytuberculosisandconfessedarealclosecontactwith 366 theirbirds(mouth-to-beakfeeding).Moreover,intheswisscase,twoveterinarians 367 inchargeofthecaseshowedapositivereactiontotuberculinskintestafterhandling 368 thesickbird[74].Oneobservationmadebytheauthorsisthattheseparrotshave 15 369 livedasufficientlylongtimeincubatingthediseasestobecomethemselvesapotential 370 sourceofinfectionforothershumans.Datalackaboutsusceptibilityofnonpsittacine 371 petbirdstoM. tuberculosis,asauthorsfoundonlyonestudyreportingsuchinfection 372 inacanary,wasdiagnosedwithalungknotpositiveforM. tuberculosis[75]. 373 ThisishoweverafactthatinfectionwithzoonoticMycobacterium sppinpetbirdsare 374 rare. Regarding the susceptibility of birds to Mycobacterium bovis, to date, only 375 experimentalinfectionshavebeenreportedasresponsibleforclinicalsigns.Arecent 376 study focusing on the experimental infection of budgerigars by several species of 377 Mycobacterium reported that the only clinical signs were seen 70 days after 378 inoculation with M. bovis, while no clinical signs were observed following the 379 challengewiththeotherspecies[76].M. bovisisalsoazoonoticagent,consideredto 380 beresponsiblefor1to2%ofhumancasesoftuberculosisinindustrializedcountries, 381 while this proportion is susceptible to be much more important in developing 382 countries(until8%ofhumancases,dependingontheregion)[77,78]. 383 Nevertheless,infected/carrying/untreatedbirdscouldbecomeapotentialreservoir 384 forhumans,andthenhaveconsequencesonpublichealth.Inanidealsituation, 385 surveillanceandearlydiagnosisofzoonoticmycobacteriashouldbeperformedin 386 everyimportedbirds’bunch[79,80]includinganimalscapturedfromthewild[81]. 387 MycobacterialcultureorPCRanalyseswouldbethemostsensitiveandspecific 388 laboratorytestsforadefinitivediagnosis[82].However,thelong-termonsetofthe 389 disease,thepathogen’sintracellularlocalisationandthedifficultytodisposeofnot 390 expensivehighlysensitivediagnostictestsmakessystematicand/orregularcheck- 391 upsdifficulttoperforminroutineconditions. 16 392 3.1.4 Campylobacter jejuni 393 Campylobacter spp.,andinparticularCampylobacter jejuniareresponsibleforfood- 394 bornediseasesinmanycountries,responsibleinhumansfordebilitatingsymptoms 395 suchasgastro-enteritidis(diarrhea,vomiting),headaches,anddepression,leading 396 sometimestodeath.Campylobacteriosiswasthemostfrequentzoonoticdisease 397 reportedin2009intheEuropeanUnion[71].ButCampylobacter spp.isnot 398 exclusivelyafood-bornedisease.Eveniflittleinformationisavailableontheroleof 399 otheravianspecies(likepetbirds)intheepidemiologyofthedisease,thispathogenis 400 shedbyanimportantbirdsvariety,amongwhichare«hobbybirds»including 401 estrildidae,canariesandpsittacines[41,83,84].Moreover,anItalianstudyshoweda 402 highoccurrenceofC. jejuni inmigratingpasseriforms[85],andconcludedthatthese 403 birdsconstituteareservoirandapossibletransmissionroutefrombirdstohumans 404 anddomesticatedanimals,includingcattle.Thisobservationwasalsomadeby 405 Adhikariandcollaboratorsin2004[86],inastudydealingwithdairycowsand 406 sparrowsfaecesinNewZealand.However,otherreportsandexperimentalprotocols 407 tendtodemonstratethatC. jejuniinfectionishighlyhost-specificandthatthe 408 transmissionfrombirdstohumans,a fortiorifrompetbirds,althoughnotimpossible, 409 islikelytoplayaminorrole[87][88].Nevertheless,onestillhastoconsiderthe 410 potentialroleofpetbirdsinC. jejuni sheddingandconsequentlyapplyelementary 411 hygienicprecautionswhilemanipulatingbirdsand/orfaeces. 412 3.1.5 Lyme disease 413 DifferentstrainsofBorrelia burgdorferisensu latowereisolatedfromtickscollected 414 onsongbirdsindifferentareasoftheworld,includingEurope[54].Olsenand 415 collaborators[89]showedthatcanariespresentedrelativelyquicklyamild 416 spirochaetemiaafterexperimentalinfectionwithB. burgdorferi,butwithoutorfew 17 417 clinicalsymptoms.Thissuggeststhatpasserinesmaybeoflittleimportanceaslong- 418 termamplifyingreservoirsforBorreliosis.Moreover,ticksareusuallyquickly 419 detectedinthefeathersofbredbirds,aswellasinkitchen-canaries,diminishingthen 420 theriskofwild-to-captivebirdstransmissionandafortioritohumans. 421 Concerningpsittacines,noevidenceofLymediseaseseemstohavebeenputtedin 422 evidence. 423 3.1.6 Others 424 Therearenumerousotherpotentialzoonoticbacteriaalsoidentifiedinpetbirds, 425 includingmultiplegram-negativebacteriasuchasPasteurellaspp,Klebsiellaspp, 426 Yersiniaspp,Pseudomonas spp.,andEscherichia coli[41,56,90,91].Indeed, 427 Escherichia coliO157:H7strainstransmittedfromwildpasserines(European 428 starlingsmostly)tocattleandthenintroducedintothefoodchainhasbeenreported 429 inseveralstudies[92-94].Lackofhygieneandtheabsenceofquarantine(especially 430 concerningimportedbirds),anddirtyfoodandwatersourcesseemtobethemost 431 probableoriginofinfectionwiththesezoonoticpathogens.Besides,thepotential 432 transmissionfromwildbirdstoopen-airaviarieshostedpetbirds(viafaecaldrops) 433 shouldbeconsidered(Boseret,pers.obs.).However,reportsoftransmissionofthese 434 bacteriafrompetbirdstohumansstilllackintheliterature. 435 436 3.2 Viral diseases 3.2.1 Avian influenza 437 HighlypathogenicavianinfluenzaAH5N1hasbeenintheworldhealthfocussince 438 theyears2000’soutbreaks.Perkinsetcollaborators[95],demonstratedin2003that 439 theavianinfluenzaAvirusH5N1afterintranasaladministrationwasabletoinduce 440 clinicalsymptomsleadingtodeathinpetbirdsspecieslikezebrafinchesandcommon 18 441 budgerigars,whichareverycommonhostsofdomesticornamentalaviaries,aswell 442 asinwildspecieslikehousesparrowsandeuropeanstarlings,usuallylivingcloseto 443 humanhabitations[95].Severalstudiesdemonstratedtheimportantroleof 444 migratingbirdsaspathogensvehiclesallovertheworld[21,96,97],beingputatively 445 abletoinfectwildindigenousbirds(housesparrows,europeanstarlings),theselatter 446 possiblycontaminatingpetbirdslivinginopenairaviaries[2].Thisviruscouldalso 447 spreadfromendemiccountries[12,16]tootherlocationsthroughinternationaltrade 448 ofexoticbirds[15,16,22].Inrelationwiththisfact,marketswherelivebirdsaresold 449 appeartorepresentagreatriskforzoonotictransmissionasdemonstratedbyseveral 450 authors[12,13].ThisisindeednoticeablethatAsianownersseemedtobe,evenat 451 thepeakoftheH5N1outbreak,unawareofthezoonoticrisksthiskindofbusiness 452 couldcause[12,13]andthiswasalsothecaseinWesterncountriesashybrids 453 betweencanariesanddifferentwildpasserineswereandarestillsoldonpublic 454 markets(Boseret,pers.inform.).Illegalbirdimportationcanalsoinduceariskas 455 suggestedbyVanBormandcollaborators[16]. 456 3.2.2 Arboviruses 457 WestNileFeverisanemergentvector-bornezoonosisinwhichbirds,e.a.house 458 sparrows,playakeyroleasmainandamplifyingreservoirhosts[48].Thevirus 459 responsibleforthisdiseaseisaflavivirus(Flaviviridae)knownunderthenameof 460 WestNileFeverVirus(WNV)whichwasisolatedfromnumerouspasseriform 461 species,includingcanaries[48],aswellaspsittacines[98].Birds,mostofthetime 462 aresubclinicallyaffected,butcanhoweverdevelopaclinicalformofthediseasewith 463 ocularandneurologicsymptoms[56].Usutuvirus(USUV)isanothermosquito-borne 464 flavivirusofAfricanorigin.Thisavianvirusistransmittedbyarthropodvectors 465 (mainlymosquitoesoftheCulex pipienscomplex).Since2001,deathofbirds 19 466 especiallypasserineshavebeenassociatedwithinfectionbyUSUV[99,100].Itis 467 wellknownthatfree-livingbirds,includingmigratoryspecies,havethepotentialto 468 dispersecertainpathogenicmicroorganisms[53].Usutuvirushasrecentlybeen 469 detectedinEuropeandisspreadingthroughAustria,Hungary,Italy,Spainand 470 Switzerland,causingdiseaseinbirdsandhumans[49].Followingthesamepattern 471 thantheWestNileFevervirus,USUVisacandidateasemergingpathogeninEurope 472 andtheconsequencesforhumanhealthsafetyhavetobeconsidered[49,53].Open 473 airaviariesarecommoninourcountriesandcouldbeanimportantfeedingsource 474 formosquitoes,whichcouldtheninoculatethevirustohumans 475 3.2.3 Others 476 Proventriculardilationdisease(PDD)isadiseaseinpetbirdsand,asitcouldbe 477 frequentlylethal,PDDisconsideredasamajorthreattoaviculture[101].This 478 syndromeisassociatedwithinflammationofthenervoussystemand 479 gastrointestinaldysfunctionaswellasneurologicchangeslikeseizures.Recently, 480 thecauseofthisdiseasehasbeenattributedtoanovelbornavirus,theAvian 481 BornaVirus(ABV)[102].However,thereisnoevidenceofABVcross-species 482 transmissionandthezoonoticpotentialofthisfamilyofvirusesremainsunclear 483 [103]. 484 Newcastledisease,causedbyavianparamyxovirus(APMV)wasalsodescribedin 485 petbirds[56,91,104].Transmissiontohumanscouldalsobepossible,with 486 conjunctivitis[56]butthemostimportantconsequencewouldbespreadingofthe 487 infectionamongpoultrybreedingbytheintermediaryofhuman,wildbirds 488 (especiallypigeons)ormaybeinsectsmechanicalvectorslikethehousefly(Musca 489 domestica)[105] 20 3.3 490 491 Parasitic/fungal diseases 3.3.1 Toxoplasmosis 492 Toxoplasmosisisawell-knownhumandisease,responsibleforabortionor 493 congenitalmalformationsinhuman.Althoughlessdocumentedthanthroughthe 494 cat-cycletransmission,Toxoplasma gondii hasalsobeendescribedasanimportant 495 pathogenforcanaries,finchesandbudgerigars[106,107],inducingblindness 496 amongothersymptoms.However,transmissiontohumansappearstobemostly 497 unlikely,asthebirdsdon’texcreteT. gondiiinfaeces(implyingnoriskof 498 contaminationbylackofhygieneorfecalmattermanipulation).Indeed,Toxoplasma 499 gondiishouldbefoundininternalorgansandmuscles,butasthesebirdsareusually 500 notbredinanalimentarypurpose,thiseliminatesthenthepossibilityofa 501 contaminationbyraworundercookedflesheating(Losson,pers.comm). 502 3.3.2 Cryptococcosis 503 Pigeonsareknowntobereservoirsofpathogenicyeasts,likeCryptococcus 504 neoformans,whichisdescribedtocauseopportunisticinfectionsinhumans[108]. 505 Howeverlessisknownontherolethatmightplaypetbirdsinsuchzoonotic 506 transmission.SeveralstudieshavedemonstratedthepresenceofC. neoformansin 507 parrots,littlepetbirdslikecanaries,budgerigarsorlovebirdsandcockatiels[109, 508 110].Asithasbeendiscussedabove,petbirds,moreoverhousedinoutdooraviaries 509 andthenincontactwithwildpigeons’droppings,couldbeapotentialhealthhazard 510 forhumansasCryptococcus neoformansreservoirs. 511 21 512 3.3.3 Others 513 Despitearelativelypoordocumentationonpetbirdsparasiticdiseases,giardiosis, 514 aspergillosisandcryptosporidiosishavebeenreportedintheseavianpopulations, 515 bothinchronicandinacuteinfections.Favorisatingconditionscouldbehigh- 516 densitypopulations,stress,adaptationtonewenvironmentorprolongedperiodsin 517 confinedhousings.[111]Transmissiontohumanoftenresultsfromfaeces 518 manipulationorlackofhygiene[41,56,90]. 519 AviangiardiasisiscausedbytwodifferentGiardiaspecies:G. ardeaeandG. psittaci. 520 G. psittacihasbeendemonstratedtoberesponsibleforfatalinfectionsin 521 budgerigars[112],butisnottransmissibletohumans.Thespeciesresponsiblefor 522 zoonoticinfectionsisGiardia duodenalis,causinggenerallyaself-limitedillness, 523 sometimesasymptomatic,characterizedbydiarrhoea,abdominalpainandweight 524 loss.[112]G. duodenalisisdividedintoeightgenotypesor“Assemblages”,among 525 whoseAssemblagesAandBappeartoberesponsibleforhumaninfections[113]. 526 Interestingly,thesegenotypeshavebeenisolatedinfaecesofdifferentavianspecies, 527 withoutleadingtothedevelopmentofclinicalsymptoms.Birdsseemthenmore 528 likelytoserveasmechanicalvectorsofcystsandoocysts.[111] 529 Inbirds,Cryptosporidiuminfectionleadstointestinal,respiratoryornephrotic 530 symptomsandcouldbecausedbythreedistinctspecies:C. galli,C. meleagridis and 531 C. baylei.Thetwolatterhavebeendescribedaspossiblezoonoticagents,thoughina 532 lowfrequencyincomparisonwithotherspeciessuchasC. hominis orC. parvum 533 [114].Themainhumanpopulationatriskareveryyoungchildren(firstexposure, 534 lackofhygiene)andimmunocompromisedindividuessuchasHIV-positivepatients, 535 whowilldevelopgastro-intestinallesionsbutalsoinfectionsofotherorganssuchas 22 536 pancreas,liverandsometimesrespiratorytract[115].Cryptosporidium parvumhas 537 beenisolatedinfaecesofvariousavianspecies,confortingthepossibilityofzoonotic 538 parasitessheddingandtransmissionbybirds.[116] 539 Aspergillosishasbeenfrequentlyisolatedfrompetbirds[56][117],inbothacute 540 (severerespiratoryconditionwithlethargyandchangesinvocalization)and 541 chronicforms(moreoftenfatalbecauseofitslong-termdevelopment).However, 542 humaninfectionwouldrathercomefromenvironmentalorigin,andthereforebe 543 consideredasaminorzoonoticthreat,aparteventuallyfromhuman 544 immunocompromisedpatients[117]. 545 546 4. Guidelines to prevent transmission from birds to humans 547 Oneinterestingdocumenttostartwithisthe“CompendiumofMeasuresToControl 548 ChlamydiapsittaciInfectionAmongHumans(Psittacosis)andPetBirds(Avian 549 Chlamydiosis),1998”editedbytheCentreforDiseasesControlin1998[59]. 4.1 550 Household hygiene 551 Thetransmissionofzoonoticpathogensfromanimalstohumanscouldbeeasily 552 decreasedbyapplyingsomeelementaryhygieneprinciples.Afewrecommandations 553 couldbedeliveredtotheownerbythebirdsellerlikethefollowingones: 554 • 555 Cleanclothingandshoesafteranycontactwithotherbirds(birdclubmeeting, birdfair,livepoultry). 556 • Washhandsbeforeandafterhandlingbirds(includingcagescleaning). 557 • Lookouteverydaytocages,foodandwater;tobesuretheyareclean(including 558 perches,feedingcups,etc.). 23 559 • Whengivingfruitsorvegetablestobirds,discardtherottenremainings. 560 • Changebathpotseverydayandletthemavailabletobirdsonlyonehour/day(to 561 avoidthebathingwastewatertobecomeareservoirforpathogens). 562 • Washcagesonceaweek. 563 • Preservefoodincleanandsealedcontainers. 564 • Cleananddisinfecteveryaviaryitemsbeforeuse. 565 Usually,birdsbreedersarecorrectlyawareoftheseprecautions;theriskishowever 566 higherinthecaseoffamilypetsboughtforthefirsttimeinadecorativepurposeor 567 aspresentforthechildren,especiallywheneitherparentsorkidshaven’tbeen 568 informedaboutthecitedaboveelementaryadvices. 569 4.2 Birds’origin traceability : 570 Inthecaseofbirdsbredinthecountrywhereintheyaresold(e.g.littlebirdslike 571 canaries,finches,budgerigars),theyareusuallyprovidedwithoutanycertificateor 572 identification(apartfromalegbandwiththebreedingidentificationnumber). 573 Sellersaresupposedtokeepanaccuratetraceabilityoftheirstocks,butthereisas 574 farasweknownolegalobligationofthesellertogiveanydocumentstothebuyer. 575 Aboutexoticpetbirdsissuedfromimportation,lawsdifferfromcountries,butina 576 generalview,avetcertificate,apassportandanimportationauthorizationhaveto 577 bedeliveredwiththebirds.Assaidbefore,smuggledbirdsrepresentahighriskof 578 zoonosesintroduction.InEurope,exoticbirdimportationfromnonEUcountriesis 579 forbiddenandanimalsimportedfromotherEU-memberscountriesshouldhavean 24 580 internationalpassport,acorrectidentificationandaveterinarycertificateofgood 581 health(Directive91/496/CE). 582 Howeverontheownerpointofview,therearesomerecommandationstobeaware 583 ofafterbuyinganewpetbird. 584 • Ifthebirdscomesfromanothercountry,requestcertificationfromthesellerthat 585 thesewerelegallyimported(eventuallyaskforofficialdocuments)andwere 586 healthypriortoshipment(certifiedbyanofficialveterinarian). 587 • Scheduleanappointmentwithaveterinarian. 588 • Isolatenewbirdsfromotherbirdsforaquarantinetimedeterminedbythe 589 veterinarian. 590 • Restrictaccesstobirdsfrompeopleowningbirdstoo. 591 • Keepbirdsawayfromotherbirds(e.g.inthegardens). 592 4.3 Awareness of sickness signs 593 Breedersusuallyknowthesicknesssignsofabird,eveniftheycouldbesomehow 594 difficulttodetect.Butfornoninitiatedpeople,likesellersinanimalshopsornew 595 owners,thiscouldbedifficulttoseewhethertheirbirdsarehealthyorill. 596 Preventiontoolsandinformationshouldthenbeprovidedbythebreederstopeople 597 theyareselling/givingtheiranimals.Veterinariansalsoshouldbetterinform 598 ownersforexamplebyprovidingdocumentationonwarningsignsofinfectiousbird 599 diseases.Ifunusualsignsofdiseaseorifunexpecteddeathsoccurinabreeding,the 600 ownersshouldthenwarntheiravianveterinarian. 25 4.4 601 Biosecurity and hygiene precautions in big facilities 602 Whenofsufficientsize,aHazardAnalysisandCriticalControlPoints(HACCP)plan 603 couldbeappliedinbreedingfacilitiesandinsellingfacilities.Toquarantinenewly 604 incomingbirdsisanabsolutelynecessaryprecaution.Theseanimalsshouldbekept 605 incleancagesforadurationestimatedbythesanitaryveterinarian,andpathogens 606 and/orpestsabsence(includingD. gallinae)shouldbecarefullychecked.CDC 607 recommendsatleastaquarantineof30-45dayswhenChlamydophila psittaci 608 infectionissuspected[59].Forexample,oneshouldcheckthesedifferentcontrol 609 points: 610 611 1. Directbirds’environment: - Presence/absenceofD. gallinaeinthequarantinecagesafteratleastoneweek, 612 whichisthetimeneededbytheparasitetoaccomplishacompletereproduction 613 cycle,fromeggtoegg[40].Forexample,theacaridscouldbeeasilyfoundon 614 feedballs,perchesorontheremovablebottomsandtray.Aneasytestistopush 615 stronglywiththethumbondirtyspotspastedonthereversefaceofthistrayand 616 scratchthemfromlefttoright(orviceversa).Ifabloodysmeardoesappear,this 617 wouldbeanefficientsignthatblood-fedparasitesdidbegintocolonizecages’ 618 anfractuosities(Boseret,pers.obs.). 619 - Color/consistency/quantityofdroppings:forexample,ayellowstainshould 620 suggestcampylobacteriosis,aliquidconsistencyshouldrefertosalmonellosisor 621 otherenterobacteriaceaeinfections[41]. 622 - 623 624 Transportcages:weretheysoiledorclean?Presenceofdeadbirds? 2. Birds:generalexamination 26 625 - Presence/absenceofotherpests’specieslivingmostoftheirtimeonthehost,e.g. 626 atthecalamusofthefeathers(likeOrnithonyssus sylviarum),attheedgeofthe 627 beakorintheleg’sscales(likeKnemidokoptes pilae, whichisanonzoonotic 628 mangeagent)orinanotherpartofthebody(e.g.ticks,lice).Brokenfeathersor 629 feather-losscouldindicatepruritusanddiscomfort,otherindicatorsof 630 ectoparasitesinfestation[41].Ectoparasitesareconsideredbymanybreedersto 631 beagoodindicatorofinadequatehygieneandmanagementandtheirdetection 632 thereforecouldawakeattentionoftheowneronthehealthstatusoftheir 633 infestedincomingbirds. 634 - Generalstateofthebirds(good/bad) 635 • Perching/lyingatthebottomofthecage 636 • Normalactivity/apathic,rolledinruffledfeathers 637 • Insocialgroups/isolated 638 • Brighteyes/enophthalmy 639 • Goodrespiratorystate/nasal-oculardischarge,openbeak 640 - 641 642 643 Plumageaspect:arethebirdsinmoltingperiod?Howisthemolting: homogenousandbilateral/heterogenousandasymmetric 3. Quarantinefacilitieshygienicstate: 644 - Frequenceandefficiencyofcages/walls/floor/shellsdisinfection 645 - Foodstorage(accesstomice,rats?) 646 - Environmentalconditions:temperature,humidity,durationoflighthours 647 Thislistisnotexhaustiveandacompletelistofadequatecontrolpointshastobe 648 determinedinfunctionofthekindandsizeofbreeding,facilitiesconformation, 27 649 season,frequenceofbirdsmovements,etc.Theaboverecommendationsshould 650 howeverconstituteabasisofelementaryexaminationstobeperformedinevery 651 cases. 652 Incaseofahighlevelofriskorwhenadoubtemergesrelativelytothebirds’health 653 state,thefollowinglaboratoryanalysescouldbeperformed: 654 655 656 657 658 1. Individulevel:necropsyofadeadorasacrificedsickindividu,performedalongwith bacterialanalysesofintestinalcontentorotherorganspresentinglesions. 2. Grouplevel:Bacterialanalysesofcloacalor/andoralswabsofabirdssamplebunch (one-to-ten,one-to-fifteen…). 3. Vectorlevel:molecularanalysesofvectorsfoundonbirdsand/orinthecages,to 659 detectspecificallyzoonoticagents:Chlamydophila psittaci,westnilefever,etc… 660 Thefirsttwotypesofanalysescouldbeaninterestinginvestmentandcouldn’tbe 661 toomuchexpensive(lessthan100euros/birds’bunch). 662 663 However,molecularanalysesareonanotherfinanciallevel.Oneshouldrecommend 664 theminparticularcases,firstwhenbirdsareabouttobehandledbyowners,like 665 parrots,parakeetsorcockatiels,secondwhenthepathogentargetedisofzoonotic 666 nonnegligeableimportance.Forexample,tuberculosisdetectionhastobecarried 667 outwithacriticalmind,asfalsenegativedooccur.Onanotherhand,assurveillance 668 ofzoonosesisaEuropeanlegalobligation(Directive2003/99/EC),testingbirds 669 couldbesystematicallyincludedinnationalsurveillanceprograms,afortioriwhen 670 humanhealthisestimatedtobeputatrisk,andthencouldthengrantthebreeders 671 withaofficialbudgetintervention. 28 672 Anothersuggestiontodiminishthecostsatalocallevelwouldbetoperformsuch 673 testsinmultiplexseries,allowingbreederstosharesomehowelevatedcosts.Butall 674 thesepossibilitiesinvolvesacompletechangeofmindandimpliesabroader 675 transparencyinthesekindofbreedings,whichstilllackseveninourhigh-controlled 676 countries(Boseret,pers.inform.). 677 Whenbirdsareprovedtobehealthy,thentheycouldbeintroducedintheir 678 definitivefacilities.Outcomingbirdsshouldbesubmittedtosimilarsanitary 679 systematicchecking. 680 Moreover,theprecautionofall-in/all-outreplacementsystem,alreadyappliedin 681 poultryexploitations,shouldbecarriedoutinpetbirdsbreedingstoo.Forexample, 682 onlybirdsofthesameageshouldbekeptinthesamelocation,andwhenmoved,the 683 facilityshouldbedisinfectedcarefullybeforewelcominganewflock. 684 Insellingfacilities,wherebirdsfromdifferentoriginscouldbemixedup,only 685 replacethemwhenthewholeflockhasbeensoldandthecagescleanedwithadhoc 686 disinfectants.Oneinterestinginitiativewouldbetocreateacertificateof«good 687 health»tomovingflocks,butasmanyanimalsaresoldinnon-officialways(e.g. 688 privatebreedings,markets),thiscouldn’tbenotsoeasytoputinplace. 689 Controlpointshouldbealsoimplementedonbird’sfairs.Sanitarycertificatescould 690 beanobligatorydocumenttoprovidetoauthoritiestoallowthebreedertoattend 691 anyfair. 29 692 5. Conclusion 693 Thisreviewaimedtopresentanon-exhaustivepanoramaofdatarelativeto 694 petbirds-humanpathogentransmission.Differentsituationshavebeenillustratedin 695 thisshortreview:familialhouseholds,breedingorsellingfacilities,birdfairs, 696 internationaltradeandthewildbirds’problematicofreservoirs.Althoughthis 697 representsaminorpartofthecompanionanimals’vetclientship,petbirds’diseases 698 withzoonoticpotentialshouldn’tbeneglectedorunderestimated,consideringthe 699 majorhealthimpactonthepopulation,includingchildren.ReferringtoPastoretand 700 Vallatzoonosesclassification,petbirdzoonosesowntothemostthreadfuldiseases 701 types:2and2+(seetable3;[118]).Vetscouldthenplayanimportantrolein 702 educatingpets(includingbirds)owners. 703 Onananotherpointofview,pathogens’sheddingbywildpasserinebirdscouldbe 704 responsibleofmaintaininginfectionindomesticbirdspools,suchasopenair 705 aviariesorpoultrybreedings,andcouldhaveimportanteconomicimpacts.The 706 presenceofSalmonellaspeciesinstarlingfaecesandincattlefeedingoperations 707 reportede.a.byCarlsonandcollaboratorsisagoodexampleofaunder-known 708 reservoirphenomenon.Anotherexampleistheroleofbirds,amongwhich 709 passerines,asamplifyinghostsforsomevector-bornezoonoticemergingviruses. 710 Openairaviariesarenotprotectedfrommosquitoes,andornamentalbirdshave 711 beenshowedtobeabletoactthesamewaythantheirwildcounterparts.Migrating 712 birdsarealsoasanitaryconcern,asthesebirdscouldspreadahighvarietyof 713 pathogensbysolelydefecatingaboveoutdooraviarieswhereinpetbirdsarehoused. 714 Thusthesebirdsconcentrationcouldbecomeanonnegligiblereservoirof 715 pathogens,contributingtomaintainandspreadinfectioninhumanpopulation. 30 716 Referringonvectors,D. gallinae followingauthor’sadviceisanunderestimated 717 concern–probablytoomanytimesmisdiagnosed-inpetbirdmedicineaswellasin 718 smallavianbreedings,astheparasitecouldbecarriedandtransferredfromone 719 speciestoanother,mostlybyinertmaterialssuchcages,perches,waterorfeed 720 bowls,etc.andeventuallybytheintermediaireofman.Threateningpathogenslike 721 C. psittaciorSalmonella ssp.werereportedtobecarriedbythemiteandtransmitted 722 topetbirds,whichcouldtheninfecteithertheirownersortheircagemates.In 723 addition,sanitarystateofpetbirdowningandtradeisratherunclearinmany 724 countries.HACCPorotherqualitycontrolplans(ISO,AFNOR…)areappliedbythe 725 FederalAgencyforFoodSafetyChain(FAFSC)inBelgianpoultrybreedings,butnot 726 in«backyardpoultryflocks»orinlocalpasserinebreedings.Legislationdoesexist 727 e.g.oninternationaltradebutdespitethis,illegalintroductionofbirdsinour 728 countriesstillremainsathreatforhumanhealthwhenconsideringthehighly 729 pathogenicagentsthatcouldbebroughtinourfrontiers(e.g.avianinfluenzaAvirus 730 H5N1orchlamydophilosis). 731 Therefore,investigatethehealthstatusofpetbirds,facilities,avianexploitations 732 andownersshouldbeaninterestingstartingpointtodefinehumanhealthrisks 733 encountered(fromfamilytobreedingscale),toproposeeconomicandsanitary 734 preventionmeasures(e.g.biosecurity,prophylaxy,hygiene)inaninterestofhealth 735 protectionandeconomicimprovement.Thisinvestigationcouldbeagoodpicture 736 illustratingtheconceptof«Animals+Humans=OneHealth». 737 738 Competinginterests 31 739 The author(s) declare that they have no competing interests. 740 Authors’contributions 741 GBandCSfixedthedesignofthestudy;GBhasrealizedtheliteratureresearchand 742 analysis;BL,ET,JMandCShavebeeninvolvedinrevisingthemanuscriptcritically 743 forimportantintellectualcontent;CShasgivenfinalapprovaloftheversiontobe 744 published. 745 746 Authors’information 747 GBisdoctorinveterinarymedicineanddefendedaPhDonsongbirds’behaviorand 748 healthstatus.Sheiscurrentlystudyingzoonosestransmittedbybirds,especially 749 petbirds,inCSresearchunit. 750 751 BL,ET,JGMandCSareprofessorsandheadsofrespectivelyparasitology,virology, 752 bacteriologyandepidemiologyandriskanalysissectionsofthedepartmentof 753 infectiousandparasiticdiseases,(FacultyofVeterinaryMedicine,Universityof 754 Liège,Belgium)andthereforeprovidedtheauthorwithexpertadvicesondiseases 755 discussedinthismanuscript. 756 757 Acknowledgments 758 WewouldliketoacknowledgetheteamoftheUREAR-ULgunitfortheirkind 759 supportinthisredactingprocess,DrsDalPozzo,HumbletandMartinelle. 760 761 762 763 References: 1. 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In: Proceedings of the OIE Global Conference on Evolving Veterinary Education for a Safer World OIE, 12-14 October 2009, Paris (France): 2009; 2009: 15-22. 38 1072 1073 TABLES 1074 Table1:mainpetbirdspeciesfollowingInternationalOrnithologicCongress(IOC) 1075 classification3.1(2012) Order Family Genus Species English name French name Passeriforms Fringillidae Serinus S. canaria Canary Canari/serindescanaries Carduelis C. carduelis Goldfinch Chardonneret C. chloris Greenfinch Verdier C. spinus siskin Tarin Pyrrhula P. pyrrhula Bullfinch Bouvreuil Fringilla F. coelebs Chaffinch Pinsondesarbres Estrildidae Taeniopygia T. guttata Zebrafinch Moineaumandarin Poephila P. acuticauda Long-tailedfinch Diamantàlonguequeue Erythrura E. gouldiae GouldianFinch DiamantdeGould Lonchura L. striata Bengalesefinch Bengali/moineaudujapon Sturnidae Gracula G. religiosa Mynah Mainate Sturnus S. vulgaris Starling Etourneau Psittaciforms Psittacidae Melopsittacus M. undulatus Budgerigar Perrucheondulée Agapornis A spp Lovebird Inséparable Psittacula P. eupatria Alexandrine parakeet Perruchealexandrine Lorius L. spp Lories Loris Psittacus P. erithacus AfricanorTimneh greyparrot GrisduGabon Poicephalus P.senegalus Senegalparrot PerroquetYouyou Ara A spp Macaw Ara Aratinga A spp Conure Conure Amazona A. aestiva Amazon Amazone Cacatuidae Cacatua C. alba Cockatoo Cacatoës Nymphicus N. hollandicus Cockatiel Calopsitte 1076 39 1077 Table2:maintransmissionroutesofdiseases 1078 Transmission route Contagious diseases Non contagious diseases Direct contact yes yes no no no no Indirect contact yes yes yes yes no no Vector-borne yes no yes no yes no Example in petbirds Chlamydiosis Tuberculosis West Nile Fever Cryptosporidiosis Lyme disease Genetic disorders 1079 1080 1081 1082 1083 Table3:classificationofemergingzoonoses[106] 1084 Transmission Wild to humans Humans to humans Wild to domestic Domestic to humans Example in petbirds 1 Yes No No No None 1+ Yes Yes No No None 2 Yes No Yes No WestNilefever Newcastledisease Yes 2+ Yes Yes Yes AvianInfluenza Salmonellosis Chlamydiosis Tuberculosis 1085 1086 1087 1088 40 1089 Table4:summaryofmainpetbirdzoonoticdiseases Disease Pathology Clinical issue Asymptomatic shedding Transmission route OIE listed disease Risk for human* Chlamydophilosis Systemic Fatal yes D/I/V Yes high Salmonellosis Digestiveto systemic Treatable yes D/I/V No Tuberculosis Respiratoryto systemic Fatal no D/I/V Yes high Campylobacteriosis Digestiveto systemic Treatable yes D/I/V No moderate Lyme disease None no V No low Avian Influenza Systemic Fatal no D/V? Yes high West Nile fever and other arboviruses Respiratoryto systemic Fatal yes V Yes (WNF) moderate Avian Bornavirus Digestive/nerv oustosystemic Fatal no D No null Newcastle disease Ocular Mildtofatal yes D/I/V Yes low ToSystemic Toxoplasmosis Digestive Digestive yes I No Nulltolow Giardiosis (G. duodenalis) Digestiveto systemic Treatable yes I No moderate Cryptosporidiosis Digestive Treatable yes I No moderate Cryptococcosis Digestive Treatable yes I No moderate 1090 *when handling a bird without hygienic precautions 1091 Legend: D =direct contact; I = Indirect contact ; V = vector-mediated contact 1092 1093 1094 1095 1096 41 1097 Table5:summaryofclinicaldataassociatedtomainpetbirdzoonoticdiseases[41] 1098 Disease Sensitive species Clinical signs Necroptic lesions Diagnostic Remarks and Pitfalls Treatment Human symptoms Dermanyssus gallinae:hide incages anfractuosities andcouldnot befoundon birds themselves Ivermectine, permethrinsin spray. Dermatitis,pruritus (sample/analysis) Blood-sucking mites All Nestlings: weakness, anemia, death None Directexamen Adults:AA, respiratory distress, depression Chlamydophilosis Psittacines –canaries -finches AA,SBS, diarrhoea, nasal discharge, dehydration, Total disinfectionof cagesand facilities(see alsochapter4) Air sacs lesions, hepatosplenomeg aly CSw,OSw,FE/BC, serology(paired serology2weeks apart),IMF,PCR Asymptomatic carriage(upto 40%),false negative Tetracyclins (1stof2d generation) Flu-likesyndrom, genital,articular,skin symptoms Congestive gastrointestinal tract, hepatosplenomeg aly CSw,FE Mostlyin winterandin outdoor aviaries; Not recommended (high probabilityof antibioresistance) Gastro-intestinal infection Progressive AA,WL, respiratory symptoms, longbones lesions Cachexia, osteolysis spotsin longbones, lung lesions (non caseous) RX(bonelesions), OSw/ Chronic development, sometimes duringmonths toyears; humanorigin infection Not recommended (high probabilityof antibioresistance) Chronicpulmonary symptoms(caseous lungknots), generalizedinfection Apathy, yellowfaeces (solidor liquid) Cachexia, congestive gastrointestinal tract, containing ayellow amylumor undigested seeds. FE/MO(curved rodsinstained smears), Canariesand psittacinesare asymptomatic carriers Not recommended (high probabilityof antibioresistance) Gastro-intestinal infection,GillainBarrésyndrome Dehydratio n, respiratory lesions OSw,CSw,BS/HP, PCR Mostlyin outdoor aviaries None Mildtosevere respiratoryand systemicinfection Ocularsigns Salmonellosis All(openair aviaries) AA,WL, diarrhoea, mild respiratory symptoms Tuberculosis Psittacines (canaries?) Campylobacteriosis Estrildidae mostly. Avian Influenza Passerines Sudden death,SBS, respiratory and neurological signs hardto differentiate frompseudotuberculosis MO(Ziehl-Nielsen), BC,HP BC 42 West Nile fever All Ocularand neurological signs OSw,CSw/PCR Mostly asymptomatic carriage None: prevention basedon limitationof exposureto mosquitoes (vectors) Mildtosevere respiratoryand systemicinfection, encephalitis, septicaemia,death Newcastle disease All SBS,AA, ocular, respiratory and neurological signs Dehydratio n, respiratory lesions OSw,CSw/serology None; preventionby vaccination Cunjunctivitis,mild flu-likesymptoms Toxoplasmosis Canary, finch, budgerigar minah SBS,AA, respiratory and neurological signs, blindness iridocycliti s, panophtha lmia, catarrhal pneumonia ,hepatosplenomeg aly CSw/MO,serology, HP,PCR Systemic symptoms sometimes unseen; detectionof thedisease3 monthslater (blindness) Trimetoprimsulfamids Mostly asymptomatic. None None Giardiosis Abortion,congenital malformation. Sometimes asymptomatic. (G. duodenalis) WL,diarrhoea, abdominalpain Cryptosporidiosis All Rare;acute diarrhoea Gastroenteric lesions CsW/MO Ronidazole Gastro-intestinal symptoms;liver, pancreas,respiratory tractlesions Cryptococcosis Parrots, little petbirds Rare None CSw/MO Possible aerosol-borne contamination Mostly asymptomatic. Respiratoryand nervoussymptoms. 1099 1100 1101 1102 1103 Legend : AA : Apathy-Anorexy ; WL : weight loss; FE: faeces examination; BC: bacterial culture; MO: microscopic observation; SBS: sick bird signs (ruffled feathers, standing at the bottom of the cage, depression); HP: histopathology (including immunocytochemistry); BS: blood sample; CSw: cloacal swab; OSw: oral swab; IMF: Immunofluorescence; PCR: polymerase chain reaction. 43
