Bat–man disease transmission: zoonotic pathogens from wildlife reservoirs to human populations

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Bat–man disease transmission: zoonotic pathogens from wildlife reservoirs to human populations

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Bat–man disease transmission: zoonotic pathogens from wildlife reservoirs to human populations
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Cell death discovery
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Bats ( lcsh )
Communicable diseases Ç‚x Transmission ( lcsh )
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Bats are natural reservoir hosts and sources of infection of several microorganisms, many of which cause severe human diseases. Because of contact between bats and other animals, including humans, the possibility exists for additional interspecies transmissions and resulting disease outbreaks. The purpose of this article is to supply an overview on the main pathogens isolated from bats that have the potential to cause disease in humans.

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OPEN REVIEWARTICLEBat – mandiseasetransmission:zoonoticpathogensfrom wildlifereservoirstohumanpopulationsNAllocati1,AGPetrucci1,PDiGiovanni2,MMasulli1,CDiIlio1,3andVDeLaurenzi1,3Batsarenaturalreservoirhostsandsourcesofinfectionofseveral microorganisms,manyofwhichcaus eseverehumandiseases.Because ofcontactbetweenbatsandotheranimals,includinghumans,thepossi bilityexistsforadditionalinters peciestransmissionsandresulting diseaseoutbreaks.Thepurposeofthisartic leistosupplyanoverviewonthemainpathogensisolatedfrombatsthathavethepotential tocausedisea seinhumans. CellDeathDiscovery (2016) 2, 16048;doi:10.1038/cddiscovery.2016.48;publishedonline27June2016 FACTSBatsareanimportantreservoirsofdifferentpathogenicagents, andmanyofthemhavealreadycauseddiseaseoutbreaks worldwide.Morethan200viruseshavebeenassociatedwithbats,and almostallareRNAvirusesprobablyowingtotheirgreatability toadapttochangingenvironmentalconditionsthrougha highergeneticvariability.Bacteriainbatsandtheirputativethreattohumansremain poorlystudied. OPENQUESTIONSTheunderstandingofthemechanismsofviralpersistencein batsremainsunclear.Extensivestudiesareneededtoimproveourunderstandingof bat – humaninteractionsinordertodesignnewcontrol measuresinthefuture.Strategiesonsurveillanceandmonitoringofdiseaseoutbreaks inbatpopulationsneedtobefurtherdeveloped,inparticular wherebatsandhumansareinclosecontact. Bats,mammalsoftheChiropteraorder,arepresentalloverthe worldwiththeexceptionoftheArctic,theAntarcticandafew oceanicislands.Batsaretheonlymammalswiththeabilityto y andarepresentin 4 1100differentspecies.1Batsareessential membersoftheglobalecosystemandhumansbene tfromtheir presenceinmanyways.Theyareinvolvedinseeddispersaland pollinationactivity:tropicalbatsarevital – asanexample – in rebuildingcutdownforestsandinthepollinationofwildplantsas bananas,avocadosanddates.Furthermore,the yingmammals arethemajorpredatorsofnightinsects,includingcropand humanpests.1Finally,theirguano,whichisrichinnitrogen,is usedasbiologicalfertilizer. Despitethemultiplebene tsattributedtotheseanimals,since theancienttimes – throughmythsandmisapprehensions – bats havegainedabadreputationinthegeneralpublic.Theclassical literatureisfullofexamplesinwhichbatsareassociatedwithevil anddarkness.TheromanpoetOvidnarratesintheMetamorphosesthatthegodBacchustransformsthedaughtersofMineus, kingofBoeotia,intobatsasapunishmentforprofanating hiscelebration(Figure1andBoxA).IntheDivineComedy(Inferno – CantoXXXIV),DanteAlighieri,thefatheroftheitalianlanguage, describesthedevilLuciferasbearinglargebatwings(Figure2and BoxB).Intheeighteenthcentury,scientistscalled ‘ vampire ’ abat thatfedonblood,givingrisetothemythofhumanvampiresthat suckedbloodfromothermenandcouldtransformintobats.The IrishnovelistBramStokerwithhisnovel,Dracula(1897)did nothingbutmakethisbelieffamousworldwide.Morerecently, BobKane,anAmericancomicbookartist,ideatedacharacter calledBatmanapositivecharacterthat,however,disguisesin abatcostumetoscarehisenemies: ‘ Criminalsareasuperstitious cowardlylot.Somydisguisemustbeabletostriketerrorintotheir hearts.Imustbeacreatureofthenight,black,terrible..... ‘ Justthena hugebat iesintheopenwindow ’ .Abat!That ’ sit!It ’ sanomen. Ishallbecomeabat!In:DetectiveComicsno33,1939. Bats,however,canbeinvoluntarilydangeroustohumans. Indeed,theyarenaturalreservoirhostsandsourcesofinfection forseveralmicroorganisms,includingpathogensthatcancause severehumandiseases,andaremorefrequentlyimplicatedin zoonoticvirusemergencies.1,2Batsarewidespreadinurbanareas andcomeinclosecontactwithbothdomesticanimalsand humans,contaminatinghouseswithguanoandurine,additionally,humansoccasionallyencroachintobathabitats.3Their characteristicecologyundoubtedlyin uencesthemaintenance andtransmissionofmicroorganismswithinthecolonyanddirectly orindirectlytohumans.1,3Microbialtransmissionwithinbatcoloniesispromotedbythe behaviorofseveralspeciesofthesemammalsaggregatingin crowdedroosts.Batscantransmitinfectiousagentstohumans throughintermediatehosts,whichareinclosecontactwith humans.4Theseintermediatehostscanbeinfectedinmanyways, includingingestionoffoodpartiallydigestedbybats.Frugivorous bats,infact,cannotingestwideamountsoffoodbecauseofthe aerodynamicsof ight,5therefore,theyextractnutrientsby chewingfruitsandspittingtheresidues.Thispartiallydigested 1DepartmentofMedical,OralandBiotechnologicalSciences,University ‘ G.d'Annunzio ’ ,Chieti,Italy;2DepartmentofPharmacy,University ‘ G.d'Annunzio ’ ,Chieti,Italyand3CESI-MET,University ‘ G.d'Annunzio ’ ,Chieti,Italy. Correspondence:NAllocati(allocati@unich.it) Received12May2016;accepted25May2016;EditedbyIHarris Citation:CellDeathDiscovery(2016) 2 ,16048;doi:10.1038/cddiscovery.2016.48Of cialjournaloftheCellDeathDifferentiationAssociation www.nature.com/cddiscovery

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fooddroppedonthegroundcanthenbeingestedbyother animalsandisapotentialinfectioussource.Asimilarmodalityof viraltransmissionhasalsobeendescribedforinsectivorousbats.5Batscanalsodirectlyinfecthumans.4Thiscanoccurthrough ingestionofinfectedbatmeat,asinsomeareasbatsareafood source,orthroughbat ’ sbiteasinthecaseofrabiesvirus. Otherfeaturesofbat ’ slifemakethemagoodhostforinfectious agents.Thefactthatseveralspeciesofbatshibernateduringthe winterisoneofthese.Althoughtheroleofthehibernationin infectiondynamicshasnotbeenwidelystudied,itislikelythatthis conditioncancontributetothemaintenanceofpathogensinthe coldweather(seebelow:white-nosesyndrome(WNS)).Moreover, unlikemanyothersmallmammals,batslive 4 30years.Their longlifemakesthemagreatreservoirforpathogensandgives themmanyoccasionstotransmitthemtootherspecies.In addition,somespeciesofbatsmigrate – alsofordistances 4 1000km – allowingthemtospreaddiseasesinbigareasand acquirenewmicroorganisms.6,7Finally,mostpathogensarenotdangerousforbatsandcan thereforesurviveforlongtimeinthehostwithoutkillingit. Indeed,despitethefactthatbatsareinfectedwithmoredifferent zoonoticvirusesperhost – withtheexceptionofrabiesvirusand other Lyssaviruses – theseareapparentlynotpathogenicforthem, suggestingthattheymaycontrolviralreplicationmoreef ciently thanothermammals.Ithasbeenhypothesizedthattheremaybe arelationshipbetween ightandlowvirulence.8During ight, batsshowanincreaseinthemetabolicrateandinbody temperature,comparabletothefeverresponserendering replicationofinfectiousagents,whicharetemperaturesensitive, lessfavorable. Inthisreview,wegiveacomprehensiveoverviewofthe microorganismsandvirusesisolatedfrombatsandtheirpossible roleinhumandisease. VIRUSES Batsarerecognizedasimportantreservoirsofdifferentfamilies ofviruses,mostofwhichareemergingashumanpathogens,such asEbolaandMarburgviruses,SevereAcuteRespiratorySyndrome (SARS)andMiddleEastRespiratorySyndrome(MERS)coronaviruses.Morethan200viruseshavebeenassociatedwithbats, andalmostallareRNAvirusesprobablyowingtotheirgreat abilitytoadapttochangingenvironmentalconditionsthrough ahighergeneticvariability.3,9Infact,RNAviruseshavehigher mutationratescomparedwithDNAvirusesastheviralRNA polymeraseslackproofreadingactivity.Furthermore,RNAviruses withsegmentedgenomeshavetheabilitytomodifytheirgenome throughgeneticre-assortment(i.e., Orthomyxoviruses ).Belowwe reportsomeexamplesofhumaninfectiousdiseasesassociated withbatviruses. Rhabdoviridae Rhabdoviridae containsixgenera,including Lyssavirus ,themost importantbat-associatedvirus.Atleast14speciesofthe Lyssavirus genuscanbedetectedinbats,whichareconsideredtheancestral hostsfortheseviruses. Lyssaviruses canbefoundworldwideand canbeclassi edusingdifferentcriteria,suchasgeneticdistance, antigenicpatterns,geographicaldistributionandhostrange.10,11Thecharacteristicbullet-shapedvirus,transmittedtohumans throughthebiteofinfectedanimals,causesanacute,and frequentlyfatal,encephaliticdisease. The rstreportofatransmissionofaviraldiseasefrombatsto humanswasin1911andrelatedtotherabiesvirus(RABV) belongingtothe Lyssavirus genus.12Carini12suggestedalink betweenrabiesinfectionandhematophagousbats,knownas vampires,inCentralandSouthAmerica.Severalyearslater,rabies wasalsodetectedinnon-hematophagousbatspecies.13Although RABVisfoundworldwideinseveralterrestrialhosts,itspresencein batsisobservedonlyintheAmericas.InEurope,fourdifferent Lyssaviruses havebeenisolatedfrombats:EuropeanBatLyssavirus type1(EBLV-1)andEuropeanBatLyssavirustype2(EBLV-2), BokelohBatLyssavirus(BBLV)andWestCaucasianBatVirus (WCBV).14Recently,anewputative Lyssavirus inbat,namedLleida Figure1. Bacchantes – LesMinides.IllustrationdeLesMtamorphosesd ’ Ovide.Modi edfromJeanMathieu,graveur;Ovide,auteur dutexte.Editeur:veuveLangelier(Paris) – 1619.Source:gallica.bnf.fr – BibliothquenationaledeFrance. BoxAThedaughtersofMineusarechangedintobatsIamquediesexactuserat,tempusquesubibat,quodtunec tenebrasnecpossisdicerelucem,sedcumlucetamendubiae con nianoctis:tectarepentequatipinguesquearderevidentur lampadesetrutilisconlucereignibusaedesfalsaquesaevarum simulacraululareferarum,fumidaiamdudumlatitantpertecta sororesdiversaequelocisignesacluminavitant,dumquepetunt tenebras,parvosmembranaperartusporrigiturtenuique includitbracchiapinna;necquaperdiderintveteremratione guram,sciresinunttenebrae:nonillasplumalevavit,sustinuere tamenseperlucentibusalisconataequeloquiminimametpro corporevocememittuntperaguntquelevistridorequerellas. tectaque,nonsilvascelebrantlucemqueperosaenoctevolant seroquetenentavesperenomen.(PubliusOvidiusNaso, Metamorphoses,bookIV,lines399 – 415)1.1Nowthedaywaspast,andthetimehadcomewhenyoucould notsaythatitwaslightordarkness,butaborderlandoflight anduncertainnight.Suddenlytheceilingshook,theoillamps seemedtobrighten,andthehousetoshinewithglowing res, and llwiththehowlingof ercecreatures ’ deceptive phantoms.Quicklythesistershideinthesmokelledhouse, and,invariousplaces,shunthe amesandlight.Whilethey seektheshadows,athinmembranestretchesovertheirslender limbs,anddelicatewingsenfoldtheirarms.Thedarkness preventsthemknowinghowtheyhavelosttheirformershape. Theydonotriseonsoftplumage,butliftthemselvesonsemitransparentwings,andtryingtospeakemitthetiniestsqueak, asbe tstheirbodies,andtelltheirgriefinfaintshrieks.They frequentrafters,ratherthanwoods,and,hatingthelight,they yatnight,andderivetheirname, ‘ vespertiliones ’ ,from ‘ vesper ’ theevening. (TranslatedbyASKline:www.poetryintranslation.com/). Batsandinfectiondiseases NAllocati etal2CellDeathDiscovery(2016)16048Of cialjournaloftheCellDeathDifferentiationAssociation

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BatLyssavirus(LLBV),wasfoundinSpain.15Todate,nohuman exposuretoLLBVhasbeenreported.EBLV-1,withthesub-types EBLV-1aandEBLV-1b,isthemostisolatedtypethroughout Europe.Inaddition,spilloverinfectionsbyEBLV-1inother mammalswerealsoobserved.13,14Thetype2ofEBLVisbelieved tobelessvirulentthantype113andisfoundlessfrequentlybeing presentonlyinfewcountriesandhumancontaminationhasbeen reportedonlyintwocases.14Twoothermembersofthisfamilyare foundinbatsbutsigni cantlylessfrequentlythantheprevious ones:BBLVisolatedinGermanyandFrance13,16,17;WCBVisolated onceintheCaucasusMountainsbutalsodetectedinKenyain seropositivebats,suggestingagreatergeographical distribution.14,18AustralianBatLyssavirus(ABLV)isthe rst endemiclyssavirusidenti edinAustraliaandisphylogenetically relatedtoRABVandEBLV1.10,19ABLVhasbeenidenti edinall yingfoxspeciesonAustralia ’ slandmass.Threefatalhuman infectionsbyABLVhavebeenreported.Additionally,otherviruses ofthisfamilydetectedinbatsaresummarizedinTable1. Paramyxoviridae Paramyxoviridae constituteawideviralfamilythatincludeshuman andanimalpathogens.Severalbat-borneparamyxoviruseshave beenrecognizedsuchasparain uenzatype2virus,Mapuera, MenangleandTiomanvirusesandtwoinfectiousagentsof emergingdiseases,suchas Nipah and Hendra viruses.20Nipah and Hendra viruses,classi edasthegenus Henipavirus ,arecapableof causingsevere,potentiallyfataldiseasesinhumans.20Fruitbatsof the Pteropus genusarethecommonreservoirhostsofthe Nipah and Hendra viruses.20Nipah virus(NiV) rstemergedin1998inMalaysia,causingan outbreakofrespiratoryillnessandencephalitisinpigs.21Pig-tohumantransmissionof Nipah virus – associatedwithseverefebrile encephalitis – wasdescribedanditwasthoughttooccurthrough closecontactwithinfectedanimals.Althoughuncommon, human-to-humantransmissionofviruswasalsodescribed.21In twootheroutbreaksinBangladeshandIndia,anintermediate animalhostwasnotidenti ed,suggestingbat-to-humanand human-to-humantransmissions. Hendra virus(HeV)causesafatalrespiratorydiseaseinboth humansandhorses.20,22SeveraloutbreaksofHeVhaveoccurred inAustralia.Horseistheintermediatehostandthevirusislikely transmittedviaingestionoffeed,pastureorwatercontaminated withurine,salivaandfecesofinfectedbats.Horse-to-human transmissionoccurswhenthereisclosecontactwithillanimals.20Todate,human-to-humantransmissionhasnotbeenobserved. Coronaviridae Coronaviruses (CoVs)priortotheSARSoutbreakwereonlyknown tobethesecondcauseofthecommoncoldafterrhinoviruses. Atleastfourdifferentspeciescancausemild,self-limitingupper respiratorytractinfectionsinhumans:alphacoronaviruses HCoV-229EandHCoV-NL63,andbetacoronavirusesHCoV-HKU1 andHCoV-OC43.Morerecently,twomoreadditionalpathogenic human-CoVwereidenti ed:SevereAcuteRespiratorySyndrome Coronavirus(SARS-CoV)andMiddleEastRespiratorySyndrome Coronavirus(MERS-CoV).23SARS-CoVwas rstidenti edinChina inFebruary2003,and4monthslater, 4 8000caseshadbeen reportedwithabout800deathsin27differentcountries worldwide.24SARS-CoVhasawidehostrangeanditisassociated withwildlifemeatindustry.Thenaturalhistoryofthevirus involvesbatsasprimaryhoststhatthentransmittedittothe intermediateamplifyinghosts – asmaskpalmcivetsandraccoon dogs – thatthencouldspreadittohumans.23,25Human-to-human transmissionfollowsandcanleadtolargenumbersofinfected patientsandisconsideredthemainrouteoftransmissioninlargescaleepidemics.9MERS-CoVisphylogeneticallyrelatedtoSARS-CoVandshare withSARS-CoVtheorigininbats.23,26,27SeveralCoVshavebeen identi edininsectivorousandfrugivorousbatspeciesinvarious countries,indicatingthatbatsmayrepresentanimportant reservoiroftheseviruses.23MERS-CoVwas rstidenti edinSaudi Arabiain2012andthenspreadtoothercountriescausing hundredsofdeaths.26,28ClinicalfeaturesofMERS-CoVaresimilar toSARS-CoV,althoughthisvirushasalsobeenassociatedwith severalextrapulmonarymanifestations,suchassevererenal complications.Recentstudieshaveindicatedthatdromedary camelsmaybetheintermediatehostsandpotentialsourceofthe virusforhumans.26,29Inaddition,the rstexperimentalinfection ofbatswithMERS-CoVhasbeendescribed.Thevirusmaintains theabilitytoreplicateinthehostwithoutclinicalsignsofdisease, supportingthegeneralhypothesisthatbatsaretheancestral reservoirforMERS-CoV.30Human-to-humantransmissionhasalso beenreported.Basedonepidemiologicaldata,bothanimal-tohumanandhuman-to-humantransmissionareconsideredtobe importantelementsinMERSoutbreak.26 BoxBLuciferatthecenterofCocytusLo'mperadordeldolorosoregnodamezzo'lpettouscafuordela ghiaccia ; epiconungiganteiomiconvegno,cheigigantinon fanconlesuebraccia: …… …… Sottociascunauscivanduegrand'ali,quantosiconveniaa tantouccello:veledimarnonvid'iomaicotali.Nonaveanpenne, madivispistrelloeralormodo;equellesvolazzava,schetreventi simoveandaello: … (DanteAlighieri:LaDivinaCommedia,Inferno,CantoXXXIV)2.2Theemperorofthesorrowfulkingdomstood,waistupwards, fromtheice;andIamnearertoagiantinsizethanthegiants aretooneofhisarms: … .. … ..Undereachfacesprangtwovastwings,ofasize tforsuch abird:Ineversawship ’ ssailsaswide.Theyhadnofeathers,but werelikeabat ’ sinformandtexture,andhewas appingthem, sothatthreewindsblewoutawayfromhim: … .. (TranslatedbyASKline:www.poetryintranslation.com/). Figure2. Satan.Modi edfromDanteAlighieri ’ sInfernofromthe OriginalbyDanteAlighieriandillustratedwiththedesignsof GustaveDor – 1861.Source:commons.wikimedia.org. Batsandinfectiondiseases NAllocati etal 3Of cialjournaloftheCellDeathDifferentiationAssociationCellDeathDiscovery(2016)16048

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Filoviridae Ebolavirus and Marburgvirus aretwogeneraofthefamily Filoviridae ,responsibleforsevere,oftenfatal,hemorrhagicfever diseasesinhumansandotherprimates.31The rstreportonthe Marburgvirus rstwasin196732inGermanlaboratoryworkersin MarburgwhocontacteditfromAfricanmonkeysimportedfrom Uganda.In1976,aviruswithsimilarcharacteristicsbut immunologicallydistinctwasisolatedintheNorthernDemocratic RepublicofCongoanditwasnamed Ebolavirus .32Bothviruses havegeneratedseveralepidemicsduringthepastyears.31Recently,in2014,thelargesteverregisteredEbolaepidemic startedinWestAfricaandhasaffectedseveralcountrieswith 4 10000con rmedcasesandthousandsofdeaths(SourceCDC Atlanta,USA:2014EbolaoutbreakinWestAfrica,updated 22September2015).Thenaturalreservoirsfor Marburgvirus and Ebolavirus arebothfruitandinsectivorousbatspecies,indicating thatthese lovirusesaremultihostparasites.31,33Thevirusis transmittedtohumansthroughcontactwithbody uids – mainly bloodandfeces – anddeadbodiesofinfectedbats.Otheranimals suchasmonkeysandapescanalsodevelopthediseaseandin turntransmitittohumans.Epidemicsusuallyareaconsequence ofhuman-to-humantransmissionofthevirus(Figure3). Athird lovirusspeciesofthenew Cuevavirus genus,named Lloviu virus,wasrecentlydetectedininsectivorousbatsinSpain.34Lloviu virus,geneticallydistinctfromtheothers,isthe rst lovirus detectedinEuropethatwasnotimportedfromAfrica.Unlikethe othertwospecies,thisvirusmaybevirulentinbats.34Asthisvirus hasnotbeenyetisolated,itscapacitytoinfectothermammalian cellsortocausediseaseinhumansremainstobedetermined. Orthomyxoviridae Orthomyxoviridae areenvelopedsegmentedRNAvirusesthat include vegeneraofwhichin uenzaAvirusisthemost preponderantpathogeninhumans.Itcausesrespiratorytract infections,resultinginmoderate-to-severediseaseandoccasionallydeath.In uenzaAvirusesaredividedintosubtypesonthe Table1.Overviewofbat-associatedinfectiousagentswithzoonoticpotential PathogenDiseasesinhumanBat-to-humantransmissionhasbeen observed Reference Viruses Rhabdoviridae RabiesvirusAcutefatalencephalitisYesJohnson etal.13EuropeanBatLyssavirustype1AcutefatalencephalitisYesMcElhinney etal.14EuropeanBatLyssavirustype2AcutefatalencephalitisYesMcElhinney etal.14BokelohBatLyssavirusNoFreuling etal.16WestCaucasianBatvirusNoKuzmin etal.18LleidaBatLyssavirusNoArchigaCeballos etal.15AustralianBatLyssavirusAcutefatalencephalitisYesWeir etal.19Aravanvirus NoBanyard etal.10Khujandvirus NoBanyard etal.10IrkutvirusAcutefatalencephalitisYesBanyard etal.10LagosBatVirus NoBanyard etal.10DuvenhagevirusAcutefatalencephalitisYesBanyard etal.10Shimonibatvirus NoBanyard etal.10Filoviridae Ebola virusEbolahaemorrhagicfeverYesOlivalandHayman31Marburg virusMarburghaemorrhagicfeverYesOlivalandHayman31Coronaviridae SARS-CoVSevereAcuteRespiratorySyndromeYes(palmcivets,raccoondogs)aDrexler etal.23MERS-CoVMiddleEasternRespiratorySyndromeYes(camels)aDrexler etal.23Paramyxoviridae Nipah virusNipahdisease(severeencephalitis)Yes(pigs)aClayton etal.20Hendra virusHendradisease(fatalrespiratory disease) Yes(horses)aClayton etal.20Orthomyxoviridae In uenzaA virusRespiratorytractinfectionsNoFreidl etal.37Bunyaviridae Hantaan virusFatalhemorrhagicfeverNoHolmesandZhang39Reoviridae MammalianorthoreovirusEntericandrespiratoryinfectionsUnclearWang etal.42Bacteria Bartonella spp.EndocarditisUnclearVeikkolainen etal.54Pasteurella spp.SystemicinfectionsNoMhldorfer51Leptospira sp.SystemicinfectionsUnclearVashi etal.64Salmonella spp.SalmonellosisNoMhldorfer51E.coli SeveralillnessesNoMhldorfer51Fungi H.capsulatum PulmonaryandsystemicinfectionsUnclearSantos etal.71aViaintermediatehostasindicated. Batsandinfectiondiseases NAllocati etal4CellDeathDiscovery(2016)16048Of cialjournaloftheCellDeathDifferentiationAssociation

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basisoftwosurfaceglycoproteins,namely,hemagglutinin(H)and neuraminidase(N).In uenzaAvirusisanuncommonpromiscuousviruswithawidehostrange,includinghumans,pigsand birds.Recently,twonewsubtypesevolutionarilydistinctfromall others – H17N10andH18N11 – weredetectedindifferentfruit batspeciesinCentralandSouthAmerica.35,36Ithasbeen observedthat,althoughH17N10subtypeisphylogenetically separatefromallothersubtypes,thevirusgenomeiscompatible withgeneticexchangewithhumanin uenzaAviruses,suggestingapotentialre-assortmentcapabilitybetweensubtypesandthe consequentabilitytogeneratehighlypathogenichybridforms.35Morerecently,serologicalevidenceofin uenzaAvirussubtypes otherthanH17N10andH18N11werereportedinAfrican frugivorousbats.37Inparticular,about30%antibodydetection ratewasfoundagainstavianH9subtypeknowntocause infectionsinhumansworldwide.38Thesedata,albeitpreliminary, suggestthatbatsmightrepresentasymptomaticmammalian carriersofin uenzaAviruses.37Thus,similartootherpathogens, batsmayrepresentaconsiderablereservoirfortheseviruses. Bunyaviridae Hantavirus genus(fromHantanriverinSouthKorea)isconstituted ofseveralemergingsegmentedRNAvirusesthatcancause humaninfections,includingsevereandlethaldiseasessuchas hemorrhagicfeverwithrenalsyndromeandhantaviruscardiopulmonarysyndrome.39,40Rodentshavelongbeenbelievedtobe theprimaryreservoirsofhantaviruses;however,awiderrangeof mammalianhosts,includinginsectivorousbats,hasbeen reported.39,40Theevolutionaryhistoryofthisgenusischaracterizedbyrelativelyfrequentcross-speciestransmissionthatisalso consideredamajorforceinitsevolution.The rsthantavirus isolatedfrombatswasthe Hantaan virus,theetiologicalagentof hemorrhagicfeverwithrenalsyndrome.41Successively,hantaviruseswereidenti edinotherbatspecies,buttodate,however, nobat-to-humantransmissionofhantaviruseshasbeen observed.39Reoviridae Mammalianorthoreovirus ofthegenus Orthoreovirus cancause mildrespiratoryorgastrointestinalillnesstoseverediseases, includingencephalitisanddiarrhea.Thevirusispresentin differentserotypesthroughouttheworldandhasbeenisolated fromseveralmammals,includinghumans.42Mammalianorthoreoviruses werealsoisolatedinseveralbatspecies,suggestingan extensivedistributionofthevirusintheseanimals.42,43,44Several evidencesuggestthatbatsmayactasthenaturalreservoirof theseviruses.42Althoughbat-originorthoreoviruseshavebeen isolatedfromhumanpatients,thezoonoticpotentialofthese virusesisstillunclear.43,44,45Otherviruses Severalothermammalianviruseshavebeendetectedinbats forwhichthezoonoticpotentialorhostrangeisunclear.9,46 – 48Anexampleare Poxviruses – importantinfectiousagentsofboth humansandanimalsandcapableofinfectingmultiplehost speciesandtoinducecross-speciesinfectionsthatwerealso recentlyidenti edinbats.49AnotherexampleistheDenguevirus, anarthropod-bornevirusbelongingtothe Flavivirus genus ( Flaviviridae )thatincludesseveralrelevanthumanpathogens associatedwithencephalitisandhemorrhagicfevers.Despitethe factthat Flaviviridae arethesecondmostfrequentvirusesfoundin Figure3. SchematicrepresentationofEbolavirustransmission.Batsarethepotentialsourceofthevirus.Infectedbatscandirectlyorthrough intermediatehostsspreadtheinfectiontohumans.Human-to-humantransmissioncanthenresultinepidemics. Batsandinfectiondiseases NAllocati etal 5Of cialjournaloftheCellDeathDifferentiationAssociationCellDeathDiscovery(2016)16048

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batsandDenguevirushasbeendescribedinseveralbatspecies worldwide,theroleoftheseanimalsinthedynamicsofviral spreadingremaininsuf cientlyunderstood.50BACTERIA Unlikeviruses,bacteriainbatsandtheirputativethreattohumans remainpoorlystudied.51Herewereportsomeexamplesof bacteriaresponsibleforcommonhumanandanimalinfections thathaveoccasionallybeendetectedinbats. Bartonellaspp. Bartonellosisisagloballyemergingzoonoticbacterialdisease.52Bartonella sp.isaGram-negativebacteriumtransmittedthrough thebiteofhematophagousarthropodvectors.Severalspecies havebeenidenti edindomesticandwildanimals,including bats.53 – 55Recently,twospeciesof Bartonella – B.mayotimonensis and B.naantaliensis – weredetectedfromboththeperipheral bloodofbatsandintheirectoparasites,suggestingthatbats mightbeasourceofthehumanbacterialpathogens.54More recently,ithasbeenreportedthepresenceofcloselyrelated Bartonella genotypesinfruitbatsandtheirassociatedbat iesin Madagascar,suggestingthetransmissionofapotentiallyzoonotic pathogenbybat yvectors.56Pasteurellaspp. Pasteurella iscommonlyspreadamonganimalsaspartofthe normalmicrobiotaoftheoral,nasopharyngealandupper respiratorytract.57Thisgenuscomprisesopportunisticpathogen speciesthatcancauseendemicdiseaseandareassociatedwith epizooticoutbreaks.57Animalbitesandnasalsecretionsarethe mostlikelysourcesoftransmissiontohumans.Inbats,various Pasteurella species – mainly P.multocida – havebeenidenti edas themainpathogensofseverallocalizedandsystemic infections.51,58Thepredominantsourceofinfectionsappearsto bewoundscausedbythebiteofdomesticpredators.However, arecentstudyfromWisconsininUSAreportedforthe rsttimean outbreakofacutepasteurellosisfrom P.multocida inwildbats withoutassociatedtraumaticinjures.59Leptospirasp. Leptospira hasworldwidedistributionanditstransmissionto humansisprimarilythroughexposuretowatercontaminatedwith theurineofinfectedanimals.60Bacteriumharborsinseveralwild anddomestichosts,colonizestheirkidneysanditiseliminatedin theirurine.Thepresenceof Leptospira inbatshasbeen demonstratedinseveralstudies.51,61,62However,thepotential roleofbatsinhumanleptospirosisisquestionable.63,64Inacase report,thepatient ’ shistoryofbatexposuresupportstheideathat batsareareservoirofthebacteriumandcanserveasavectorin diseasetransmissiontohumans.64Enterobacteriaceae Severalmembersofthe Enterobacteriaceae family – responsible foravarietyofhumanillnesses – wereisolatedfrombats.51,65 – 67Anumberofstudiesreportedthat Salmonella serotypesisolated frombatshavesimilarcharacteristicstothosefoundfrom livestockandhumans,indicatingthatbatscanbelocally importantintheepidemiologyofsalmonellosisinhumanand domesticlivestock.51,66Twooftheseserotypes, S.typhimurium and S.enteritidis ,areafrequentcauseofhumanandanimal diseases. Escherichiacoli strainhasalsobeenfrequentlyisolatedfrom bats.51,66 – 68Itistoemphasizethehighpercentageofmultiresistanceoftheseclassofpathogenstoseveralclassesof antimicrobials51,66,68thatisamajorandincreasingglobalhealthcareproblem.Antimicrobialresistancewasalsoobservedin domesticandwildanimals,withanincreasedincidenceof resistanceinbothpathogenicandendogenousbacteria.69Resistantpathogenscanthenbetransmittedtohumansandbats canthereforecontributetothespreadingofresistantbacteria. Severalothergenera – suchas Yersinia Campylobacter Vibrio – havebeenidenti edinbats,buttheirimpactontheseanimals remainsmostlyunknown.51FUNGI Histoplasmacapsulatum H.capsulatum isadimorphicpathogenicfungusofmammals, whichcausespulmonaryandsystemicinfectionsinhumansandit isacquiredviainhalationofthefungalspores.Thismicroorganism iscommonlyfoundinsoilassociatedwithgreatamountsofbirds ’ droppingsorbatsguano.Althoughbatsareconsideredthemain reservoiranddispersersofthisfungusintheenvironment,their roleinspreading H.capsulatum remainsunclear.70Ithas,however, beenobservedthatsubjectsoccupationallyexposedtobatsites, suchasminers,geologistsorfarmerswhousebatguanoas fertilizer,havehighriskofinfectionandcandevelopsevere clinicalformsofhistoplasmosis.70,71Pseudogymnoascusdestructans Althoughimplicationsinhumanhealthforthismicroorganism arenotknown,itisimportanttowriteafewwordsonan emergingfungaldisease,namedWNS,responsibleforthedeaths ofmillionsofbatsinNorthAmerica.Itiscausedbythe psychrophilic(cold-loving)fungus P.destructans thatinfects theskinofbats – especiallythewings – duringthewinter monthswhiletheyareinhibernation.72Unlikeotherdermatophytes,whichcolonizetheouterlayeroftheskin, P.destructans is abletoinvadethelivingtissueofthehostcausingthe characteristicsevereskinlesions.73Inaddition P.destructans increasesthefrequencyofperiodicarousalsinbats,resultingin prematureconsumptionofstoredfatessentialtosurvivethe winterleadingtodeathwithin4monthsofinfection.72Recently, ithasbeenobservedthatbacteriaofthe Pseudomonas genus – isolatedfromtheskinofbats – inhibitthegrowthofthefungus invitro .74Additional invivo studieswilltelluswhetherinthe futuretheycouldbeusedasbiologicalcontrolagentstoprotect batsexposedto P.destructans CONCLUSIONSANDFUTUREPERSPECTIVE Emergenceofnewinfectiousdiseasescorrelateswithsocioeconomic,environmentalandecologicalfactorsandareamajor publichealthproblemaswellasanimportantburdenon economiesworldwide.75Mostofthesearecausedbyzoonotic pathogensoriginatinginwildlifeandthenspreadingtohumans. Batsareanimportantreservoirofseveralpathogenicagents, mainlyviruses,andmanyofthemhavealreadycauseddisease outbreaksworldwide.Theincreasingrateofbat-associated infectionsisalsosupportedbyanexpandingoverlapbetween batandhumanhabitats.Recently,toincreasetheknowledge ofbat-associatedviruses,adatabasehasbeenconstructed (http://www.mgc.ac.cn/DBatVir).76DbatViranalyzesthevirome diversityofbatsaswellastheecologicalandepidemiologicaldata toexamineandtrackcurrentandfuturebat-relatedtransmissible diseases.Todate,DbatVirhascollectedinformationon5717 bat-associatedanimalvirusesdetectedfrom207batspeciesin 77differentcountries(updateon2march2016).Strategieson surveillanceandmonitoringofdiseaseoutbreaksinbatpopulationsneedtobefurtherdeveloped,inparticularwherebatsand humansareinclosecontact.Extensivestudiesarealsoneededto improveourunderstandingofbat – humaninteractionstodesign Batsandinfectiondiseases NAllocati etal6CellDeathDiscovery(2016)16048Of cialjournaloftheCellDeathDifferentiationAssociation

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