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Terms of Use: https://bioone.org/terms-of-useShortcommunicationWildl.Biol.18:333-336(2012)DOI:10.2981/11-094WildlifeBiology,NKVwww.wildlifebiology.comFirstreportofSpirocercalupiinfectioninredfoxVulpesvulpesinGreeceAnastasiaDiakou,ElisavetKaramanavi,MarkEberhard&EleniKaldrimidouDuringthenecropsyofaredfoxVulpesvulpesthathaddiedfrompoisoning,wefoundanoduleof2Histologicalexaminationindicatedthatathick-wallednodule,whichconsistedofparasiticgranulo-masandgranulationtissue,waslocatedintheoutermostconnectivetissue(adventitia)ofthestom-achwallandfocallyin“ltratingintothelayersofsmoothmuscles(muscularisexterna),resultinginextensionofthegranulomatoustissuetothesubmu-cosa.Granulomasconsistedofcentrallylocatedworms(Fig.1),surroundedbydegeneratedandviableeosinophilsandneutrophilsandnecroticcellulardebrisadmixedwithbacilli,rimmedbyawellvascularised,collagenousrichconnectivetissuein“ltratedpredominantlybymononuclearcells,speci“callyhistiocytes,plasmacellsandlympho-cytes.Wealsoobservedisolatedorfociofparasiteeggswhichweresurroundedbydegeneratedandviableeosinophils,neutrophilsandnecroticcellulardebris.Intothecollagenousconnectivetissue,pre-sumablyadjacenttothewormtract,diusein“ltratesorfocioftheabovementionedin”ammatorycellswerepresent.Wealsosawparticularlyactive“bro-blastswithoutmarkedcellularatypia.Thewormsinthegranulomasexhibitedcharac-teristicfeaturesofspiruridnematodes.Multiplesectionsofacoiled,large,gravidfemalewormwerepresent.Thecuticlewassmoothwithoutanyspecialornamentationandthehypodermiswasthinandinconspicuousexceptattheareasofthelateralchords,whichwereverylargeandprojectedfarintothebodycavity(seeFig.1).Themusclecellswereprominent,numerous(polymyariantype)andex-tendedintothebodycavity(coelomyariantype).Theintestinewaslargeanddistinctive;thecellswerecolumnarandslender,thenucleialltendedtolieatthesamelevelinthecells,andaveryprominentmicrov

illusorbrushborderwaspresent.Thepairedu
illusorbrushborderwaspresent.Thepaireduterinetubeswerelargeand“lledwithcharacteristicsmall,longandslenderspirurideggswithathickshellthatcontainedadevelopinglarva(Fig.2).First,westudiedthemorphologicalfeaturesoftheparasitesisolatedfromthenodulemacroscopically,andthenmicroscopicallyusingastereoscopeandamicroscope.Thewormswerebrightrednematodes,1mminmaximumdiameterand4cm(males)to7.5cm(females)long.Theirmouthwassurroundedbysixlobes.Thehindendofthemalewasspirallycoiled,hadlateralalaeandpapillaeandunequalspicules.Inthefemale,thevulvaopenedclosetothehindendoftheoesophagusandtheuteruscontainedcharacter-isticthickandsmoothshelledeggs,30-37311-15lminsize.Wedidnotperformapost-mortemfaecalexaminationfordetectionofparasiticova.Accord-ingtotheirmorphology,theparasiteswereidenti“edasS.lupi(Soulsby1968,Yamaguti1961).S.lupipredominantlyoccursinspeciesbelongingtoCanidaeandhasaworldwidedistribution,butitismoreprevalentinwarmclimates(i.e.tropicalandsubtropicalregions).InGreece,S.lupihasbeenre-portedin0.4-24.2%ofthedogs(Himonas1968,Haralabidisetal.1988,Mylonakisetal.2001)butnotinwildcarnivores.Theadultwormsarefoundcoiledwithingranu-lomatousnodulesformedmainlyintheoesophagus,wheretheydepositembryonated(L1)eggs,whichpassintothegastrointestinallumenthroughsmall“stuloustractswhichtheparasiteopensthroughtheFigure1.MorphologicfeaturesinsectionsofSpirocercalupiincludelargelateralchordsextendingintobodycavity(arrows),prom-inentgut(arrowheads)anduterinetubes“lledwithdevelopingeggs(asterisks).Gran-ulomatoustissue(openarrows)developedinthegastricwallissurroundingthecoilednematode.334WILDLIFEBIOLOGY18:3(2012)oesophagealwall.Theeggsarepassedinthefaecesormaybeshedinvomitus.Eggsareingestedbytheintermediatehost(avarietyofspeciesofarthropods,mainlycoprophagousbeetles)andthelarvaeencystwithinthetissuesanddeveloptoinfectivity(L3)withintwomonths.Thebeet

legetsingestedbythe“nalhost(acarnivore)
legetsingestedbythe“nalhost(acarnivore)oraparatenichost(e.g.reptiles,birdsandsmallmammals;Bailey1972,Soulsby1968,Foxetal.1988,Urquhartetal.1996).Spirocercosisisusuallysubclinical,butitmayalsobethecauseofoesophageal/stomachgranulomasandsarcomas,aorticscarringandaneurysms,tho-racicdiscospondylitis/spondylosis,hypertrophicos-teopathyandsalivaryglandnecrosis(Mylonakisetal.2008).Inthecasewedescribehere,weobservednootherlesionsrelevanttotheparasitespresence,apartfromthegastricnodule.Diagnosisofspirocercosiscanbemadebydemonstratingthecharacteristiceggsoftheparasiteinfaecesapplyinganappropriatemethod,byendoscopyorbyradiography(Mylona-kisetal.2008).Inthecaseoffoxesandotherwildanimals,diagnosisisusuallymadepostmortem,i.e.bynecropsy.GastriclesionsinfoxesduetoS.lupihavebeenreportedinSicily(Italy),where9.16%oftheanimalsharbouredthesenematodesexclusivelyingastricnodules(Ferrantellietal.2010).ThereisalsoareportofgastricnodulecausedbyS.lupiinadomesticcatinFlorida,USA(Menseetal.1992).Anotherparasiteofthesamefamily(Spirocercidae),Cylicospiruraspp.wasreportedtocausesimilarlesionsinwildFelidae(Fergusonetal.2011).Pence&Stone(1978),ontheotherhand,foundthataorticinvolvement(scarringandaneurisms)aremorefrequentinwildcarnivoresthanesophagealnodules.Inatotalof32helminthspeciesfoundinredfoxinsouthernBelarus,S.lupiwaspresentin2.1%ofthefaecalsamples(Shimalov&Shimalov2003).ThisparasitewasalsofoundinredfoxinBelgrade(Pav-lovicetal.1997)andtheIberianPeninsula(Segoviaetal.2004).Inalltheabove-mentionedcases,theanimalsexaminedweredead,sopossibleclinicalsignscouldnotbeobserved.DespitethegreatvarietyofhelminthspeciesfoundinpreviousstudiesofredfoxinGreece(Diakou1996,Papadopoulosetal.1997),ourobservationisthe“rstreportofS.lupiinthisanimalspecies.InfectionbyS.lupicaninsomecasesbefatal.Thisisanimportantfacttobeconsideredincountrieswherewildcarnivores(

e.g.thegreywolfCanislupusandthegoldenj
e.g.thegreywolfCanislupusandthegoldenjackalC.aureusinGreece)arevul-nerableorthreatenedbyextinction.Moreover,parasitessuchasS.lupiwhichcanbefoundbothindomesticatedandwildanimalsareofparticularepidemiologicalsigni“canceascrossinfectionbe-tweenthetwoanimalgroupsispossible.ReferencesBailey,W.S.1972:Spirocercalupi:acontinuinginquiry.-JournalofParasitology58:3-22.Diakou,A.1996:Paqa´risasotpepsijot´jaisotamapmetrsijot´rtrsg´laso1sxmhgkarsijx´mjaisxmpsgmx´msotZxokocijot´Kg´potHerrakomi´jg1.(InGreekwithanEnglishsummary:ParasitesofthedigestiveFigure2.High-powermagni“cationofSpi-rocercalupisection,illustratingthenatureofthegut,includingtheprominentbrushbor-der(largearrow),andtheuteri“lledwithtypical,thick-shelledspirurideggs(smallarrows)containingadevelopinglarva.Whenviewedincrosssection,theeggsappearround.WILDLIFEBIOLOGY18:3(2012)335andtherespiratorysystemofmammalsandbirdsinThessalonikiZoo).-Anima4:40-50.Ferguson,J.A.,Woodberry,K.,Gillin,C.M.,Jackson,D.H.,Sanders,J.L.,Madigan,W.,Bildfell,R.J.&Kent,M.L.2011:Cylicospiruraspecies(nematoda:spirocerci-dae)andstomachnodulesincougars(Pumaconcolor)andbobcats(Lynxrufus)inOregon.-JournalofWildlifeDis-eases47:140-153.Ferrantelli,V.,Riili,S.,Vicari,D.,Percipalle,M.,Chetta,M.,Monteverde,V.,Gaglio,G.,Giardina,G.,Usai,F.&Poglayen,G.2010:Spirocercalupiisolatedfromgastriclesionsinfoxes(Vulpesvulpes)inSicily(Italy).-PolishJournalofVeterinarySciences13:465-471.Fox,M.S.,Bums,J.&Hawkins,J.1988:Spirocercosisindogs.-CompendiumonContinuingEducation10:807-822.Haralabidis,S.T.,Papazachariadou,M.G.,Koutinas,A.F.&Rallis,T.S.1988:Asurveyontheprevalenceofgas-trointestinalparasitesofdogsintheareaofThessaloniki,Greece.-JournalofHelminthology62:45-9.Himonas,C.A.1968:Aklimhe1stjtmdijaigrglariaatsxmei1sgmdgl.(InGreekwithanEnglishsummary:TheparasitichelminthsofdoginGreeceandtheir

publichealthim-portance).-Scienti“cYearb
publichealthim-portance).-Scienti“cYearbookoftheVeterinaryFacultyofThessaloniki9,Greece,pp.163-390.Mense,M.G.,Gardiner,C.H.,Moeller,R.B.,Partridge,H.L.&Wilson,S.1992:Chronicemesiscausedbyanematode-inducedgastricnoduleinacat.-JournaloftheAmericanVeterinaryMedicalAssociation201:597-598.Mylonakis,M.E.,Koutinas,A.F.,Liapi,M.V.,Saridomi-chelakis,M.N.&Rallis,T.S.2001:AcomparisonoftheprevalenceofSpirocercalupiinthreegroupsofdogswithdierentlifeandhuntingstyles.-JournalofHelminthol-ogy75:359-61.Mylonakis,M.E.,Rallis,T.&Koutinas,A.F.2008:Caninespirocercosis.-CompendiumofContinuingEducationforthePracticingVeterinarian30:111-116.Papadopoulos,H.,Himonas,C.,Papazahariadou,M.&Antoniadou-Sotiriadou,K.1997:HelminthsoffoxesandotherwildcarnivoresfromruralareasinGreece.-JournalofHelminthology71:227-31.Pavlovi,I.,Kulisi,Z.&Milutinovi,M.1997:Theroleoffoxes(VulpesvulpesL.)intheepizootiologyandepidemi-ologyofnematodeparasiticzoonoses.-ActaVeterinaria47:177-182.Pence,D.B.&Stone,J.E.1978:ViscerallesionsinwildcarnivoresnaturallyinfectedwithSpirocercalupi.-Vet-erinaryPathology15:322-331.Segovia,J.M.,Torres,J.&Miquel,J.2004:Helminthparasitesoftheredfox(VulpesvulpesL.,1758)intheIberianPeninsula:Anecologicalstudy.-ActaParasi-tologica49:67-79.Shimalov,V.V.&Shimalov,V.T.2003:Helminthfaunaoftheredfox(VulpesvulpesLinnaeus,1758)insouthernBelarus.-ParasitologyResearch89:77-78.Soulsby,E.J.L.1968:Helminths,ArthropodsandProtozoaofDomesticatedAnimals.6thedition.-Baillieres,TindallandCassell,London,UK,277pp.Urquhart,G.M.,Armour,J.,Duncan,J.L.,Dunn,A.M.&Jennings,F.W.1987:VeterinaryParasitology.-LongmanScienti“candTechnical,Essex,UK,77pp.vanderMerwe,L.L.,Kirberger,R.M.,Clift,S.,Williams,M.,Keller,N.&Naidoo,V.2007:Spirocercalupiinfectioninthedog:areview.-TheVeterinaryJournal176:294-309.Yamaguti,S.1961:SystemaHelminthum.VolumeIII.Thenematodesofvertebrates.-NewYork&London:Pub-lishersInc.,600pp.336WILDLIFEBIOLOGY18:3(20