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See discussions, stats, and author profiles for this publication at:https://www.researchgate.net/publication/51671935 Gurltia paralysans (Wolffhugel, 1933):Description of adults and additional casereports of neurological diseases in... Article in Veterinary Parasitology · September 2011 DOI: 10.1016/j.vetpar.2011.08.035 · Source: PubMed CITATIONS 3 READS 161 10 authors , including:Manuel MoroniUniversidad Austral de Chile 11 PUBLICATIONS 12 CITATIONS SEE PROFILE Marcelo GómezUniversidad Austral de Chile 37 PUBLICATIONS 36 CITATIONS SEE PROFILE Gerardo Acosta-JamettUniversidad Austral de Chile 49 PUBLICATIONS 319 CITATIONS SEE PROFILE David S LindsayVirginia Polytechnic Institute and State… 452 PUBLICATIONS 14,086 CITATIONS SEE PROFILE All content following this page was uploaded by Gerardo Acosta-Jamett on 01 December 2016.The user has requested enhancement of the downloaded file. All in-text references underlined in blueare linked to publications on ResearchGate, letting you access and read them immediately. VeterinaryParasitology 184 (2012) 377–380 ContentslistsavailableatSciVerseScienceDirect Veterinary Parasitology journalhomepage:www.elsevier.com/locate/vetpar Short Communication Gurltia paralysans (Wolffhügel, 1933):Description of adults andadditional case reports of neurological diseases in three domestic catsfrom southern Chile M. Moroni a , P.Mu˜noz a , M. Gómez b , ∗ , M. Mieres c , M. Rojas b , C. Lillo b , F. Aguirre a ,G. Acosta-Jamett d , M. Kaiser b , D.S. Lindsay e a InstitutodePatologíaAnimal,UniversidadAustraldeChile,Valdivia,Chile b InstitutodeFarmacologíayMorfofisiología,UniversidadAustraldeChile,Valdivia,Chile c InstitutodeCienciasClínicasVeterinarias,UniversidadAustraldeChile,Valdivia,Chile d InstitutodeMedicinaPreventivaVeterinaria,UniversidadAustraldeChile,Valdivia,Chile e DepartmentofBiomedicalSciencesandPathobiology,Virginia-MarylandRegionalCollegeofVeterinaryMedicine,VirginiaTech,Blacksburg,VA,USA a r t i c l e i n f o Articlehistory: Received25January2011Receivedinrevisedform28August2011Accepted29August2011 Keywords:Gurltiaparalysans NematodeSpinalcordChile a b s t r a c t Adults of Gurltia paralysans were obtained from veins of the spinal cord subarachnoidspace from three domestic cats presenting with chronic paraparesis/paraplegia from ruralareas of southern Chile. Four adult nematodes were collected (2males and 2 females)were recovered from cat 1, 14adult nematodes (12 females and 2 males) from cat 2,and12 nematodes (10females and2 males) were collected from cat 3.Parasite inducedlesions that compromised subarachnoid vein microvasculature at the thoracic, lumbar,sacralspinal cord segments extending to conus medularis. Female nematodes measured25mm long (range =25–30 mm) and 0.1 mm wide. Male measured amean of 16 mm length(range =13–18 mm) with abodydiameter of 0.1 mm (range =0.08–0.15 mm). The presentstudy described structural features of G. paralysans , a rare parasite first reported in the1930s,and provides additional reports on associated clinical and pathological findings innaturallyinfected domestic cats. © 2011 Elsevier B.V. All rights reserved. 1.Introduction Gurltiaparalysans isanematode(OrderStrongylida,FamilyAngiostrongylidae)ofdomesticcatsfirstreportedanddescribedbyWolffhügelinChileintheearly1930s(1933,1934)(Bowmanetal.,2002).Sincethefirstdescrip- tion,fewadditionalreportsof G.paralysans infectionhavebeenpublished(Bowmanetal.,2002;Gómezetal.,2010). TheparasiteisfoundindomesticandwildcatsofsouthernChile,adjacentareasofArgentina,Colombiaandpossi-blyNewYork,USA(Bowmanetal.,2002;Guerreroetal.,2011).Theadultwormsinhabitmainlytheveinsofthe ∗ Correspondingauthor.Tel.:+5663221072;fax:+5663221473. E-mailaddress:
[email protected](M. Gómez). spinalcordsubarachnoidspaceandparenchyma,produc-ingmeningomyelitis,thrombophlebitis,varicousveinsandcongestion(Gómezetal.,2010).Clinicalsignsinaffected catsincludepelviclimbataxia,paraparesis,paraplegia,tailandanalatonia,urinaryincontinency,fecalimpactionandpelviclimbmuscleatrophy(Wolffhügel,1934;Gómezetal.,2010).Neurologicalsignsareprobablyduetochronic myelopathyorpolineuropathycompressionlesionsduetovaricousveins,andaccumulationofadultworms,eggs,inflammatorycellsandthrombithatdevelopintheassoci-atedvasculature.Wolffhügel(1933,1934)providedtheoriginaldescrip- tionandnamedtheparasitefromdomesticcats.Heindicatedthattheparasitehadafiliformbody,lackedlips,oralpapillaeandbuccalcapsule.Maleswereabout12mmlongand50–102 mwidewithspiculesofsimilarlength 0304-4017/$–seefrontmatter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.vetpar.2011.08.035 378 M.Moronietal./VeterinaryParasitology 184 (2012) 377–380 andanindistinctgubernaculum.Wolffhügel(1934)indi- catedthatfemaleswere20–23mmlongand144–155 mwide,haveavulvapositionedneartheposteriorendofthebody,andwereoviparous.Theobjectivesofthepresentreportaretodetermineandreviewmorphologicalfeaturesoffemalesandmalesof G.paralysans , depositparatypesofmaleandfemalespecimensininternationalmuseums,andtodescribeclinicalsignsandmicroscopiclesionsduetothenematodesinthreenaturallyinfecteddomesticcats. 2.Materialsandmethods 2.1.Animals Threeadultdomesticshorthairedcatswereexaminedinthepresentstudy.Allwereindoor/outdoorcatsthatlivedinruralareasofsouthernofChileandhadsignsofchronic(>2months)paraplegia/paraparesis.Catsweredonatedbytheirownersbecauseofchronicparaparesisandpoorprog-nosisfortreatmentandrecovery.Thestudywas approvedfromtheUniversidadAustraldeChileInstitutionalAni-mal CareandUseCommittee,UniversidadAustraldeChile(UACh)Valdivia,Chile.Thefirstcatwas1yearold,3.9kg,malefromCoique,Futrono(40 ◦ 05 S;72 ◦ 22 W, RegióndelosRíos,Chile).Thesecondcatwasa3yearold,2.6kg,femalefromYuco,Ancud(41 ◦ 52 11S;73 ◦ 49 13W,RegióndelosLagos,Chile).Thethirdcatwasa2yearold,3,6kg,femalefromLastarrias(39 ◦ 22 0 S;72 ◦ 38 0 W, RegióndelaAraucania,Chile). 2.2.Neurologicalandnecropsyexaminations CatsweretransportedtotheVeterinaryClinicalHospitalatUAChforneurologicevaluation.Followingneu-rologicexaminations,catswereanesthetizedwithxylazine(10mg/kg)andketamine(1mg/kg)solutionandlatereuth-anizedbyintravenousinjectionof0.3ml/kgofeuthanasiasolution(T61 ® euthanasiasolution,Intervet/Schering-PloughAnimalHealth).NecropsyexaminationswereconductedattheAnimalPathologyInstitute,UACh.Sam-plesfromheart,lungs,spleen,liver,kidney,brainandspinalcordwerefixedin10%bufferedformalin.Paraffin-embeddedtissuesweresectionedat5 mandstainedwithhematoxylin–eosin.Thecompletespinalcordwasremovedfromthevertebralcanalandthenincisionsmadeinthespinalduramaterexposingthesubarachnoidatthecervical,thoracic,lumbarandsacralregions.Grosslyaffectedspinalcordareas,containingcongestedand/ordilatedvesselswerefurtherdissectedandthemicrovascu-laturewasinspectedusingastereomicroscope.Nematodeswereextractedmanuallyusingafineneedle.Recoveredparasiteswerefixedin70%ethanol,clearedinAman’slac-tophenol(Galeanoetal.,1990)andindividuallymounted onamicroscopeslideformorphologicexaminationlightmicroscopy.Measurementswereperformedusingacal-ibratedocularmicrometer.Morphologicidentificationof adultnematodeswasbasedonthedescriptionsmadebyWolffhügel(1933,1934). 3. Results 3.1.Neurologicalandnecropsyexaminations Neurologicexaminationofthecat1revealedparapare-sis,asymmetricpelviclimbataxia,decreasedflexorreflexintherightpelviclimb,proprioceptivedeficitsinbothpelviclimbs,reducedperianalreflexandtailatony.Addi-tionally,hyperaesthesiaoftheskinatthelumbosacralandperianalarea,hipoalgesiaofthetailandoccasionalrightpelviclimbandtailtremblingwas alsoobserved.Neuro-logicexaminationofcat2showedparaplejia,severemuscleatrophyofthepelviclimbs,augmentedpatellarreflexinbothpelviclimbs,extensorreflexinrightpelviclimb,blad-deratony,urinaryandfecalincontinence,tailatonyandskinulcersandabscessesattheperinealregion.Neuro-logicexaminationofcat3showedmoderateambulatoryparaparesisandpelviclimbataxia,andreducedtailtone.Neuroanatomicaldiagnosisonallcatssuggestedamultifo-calordiffusespinalcordlesionfromT3-L3and/orL4-Cd5segments.Two malesandtwofemaleswererecoveredfromthesubarachnoidveinsfromthelumbarandsacralregionsofcat1.Twelvefemalesnematodesandtwo maleswereremovedfromthethoracic,lumbar,sacralandcaudalspinalcordsegmentsfromcat2.Twelvefemalesandonemalewerecollectedfromthethoracic,lumbar,sacralandcaudalspinalcordsegmentsofcat3. 3.2.DescriptionofadultG.paralysans Freshlyremovednematodeswerelongandlightgrayincolor.Femalenematodeswere25mmlong(range=23–30mm) and0.1mmwide.Theanteriorendwas roundedwithoutlips,oralpapillaeorabucalcapsule(Fig.1).A0.6mmrhabditoidesophaguswithanisthmus andbasalbulbwas present.Theposteriorendwas short,curvedandrounded.Theanalporewaslocated0.03mmfromthecaudalend,whilethevulvawas 0.15mmfromthecaudalend.Theano-vulvardistancewas 0.13mm. Thevaginalporeopenedinavalvularmuscularprotuberance.The4malesweresmallerandmoreslenderthanthefemales.Theyhadathinsmoothcuticleandmeasured16mminlength(range=13–18mm) withabodydiameterof0.1mm. Theesophaguswas0.4mmlong.Theposteriorendofmaleshadacopulatroybursawithtwo equalbrownspiculesmeasuring0.8mmlongand0.003mm wide(Fig.1)thatwereuniformlycurvedtaperedsmoothlytotheend.Anindistinctgubernaculumwaspresent.Thecopulatorybursahadthreepoorlydigitatebursalrays.Thebursamea-sured0.13mmofwidthand0.066mmlength.Inallcases,thoracic,lumbosacralandcaudalspinalcordsegmentsandthecaudaequinashowedmarkeddila-tionandtortuouscongestedsubarachnoidvessels.Somenematodeswereobservedunderthedissectingmicro-scopelyingintodilatedvesselsinacoiledfashionandoccasionallymovinginthevessellumen.Histopatholog-icalfindingsintheaffectedareasofallcatsincludedseveredilationandcongestionofsubarachnoidveinsandthrombosisofveinsatthelumbarandsacralspinalcordsegments(Fig.2).Organizedthrombiwerepresentinsome M.Moronietal./VeterinaryParasitology 184 (2012) 377–380 379 Fig.1. Specimensof Gurltiaparalysans .Femalecranialend(A).Femalecaudalend(B).Malecranialend(C).Malecaudalend(D).an:anus,cb:copulatorybursa, es:esophagus,in:intestine,sp:spicules,va:vulvaraperture(scalebar:100 m). Fig.2. Transversesectionofthelumbarspinalcordfromacatinfectedwith Gurltiaparalysans .Sectionsoftheparasitesareinsidetheparenchymaattherightdorsalhornofthespinalgraymatter(arrow).Severemeningitisandanorganizedthrombuscontainingeggs(arrow-head).Submeningealandintraparenchymatousveincongestion(asterix).Deformitytheleftdorsalfuniculusofthespinalcordduetochroniccom-pression(doubleasterix). subarachnoidvesselsandcontainedabundantnematodeeggsand/oradultparasiteswhichweresurroundedbymononuclearinflammatorycells(Fig.2).Additionally,mild inflammatoryinfiltrateandassociatedcuffingcellswereobservedinsomesectionsofthelumbosacralspinalcordparenchyma.Histologicalsectionsofthelumbarspinalcordsegmentcontaining G.paralysans andassociatedlesionsfromanatu-rallyinfectedcat(cat2)weredepositedintheUnitedStatesNationalParasiteCollection(USNPC092920.00),UnitedStatesDepartmentofAgriculture,ARS,ANRI,Bldg.1180,BARC-East,10300BaltimoreAvenue,Beltsville,Maryland20705,USA.Fouradultspecimens(2malesand2females)weredepositedintheRoyalVeterinaryCollegeHelminthCollection(Collectionno.8064)HertfordshireAL97TA,UK. 4.Discussion Littleisknownaboutthegeographicdistributionorotheraspectsoftheepidemiologyandlifecycleof G. paralysans .ThecatsinthepresentstudywerefromLas-tarria(RegióndeLaAraucania),FutronoLake(RegióndeLosLagos)andAncud(IsladeChiloé,RegióndeLosLagos)insouthernChile.Theoriginaldescriptionof G.paralysans wasfromdomesticcatsfromChileandincludedgeograph-icalareasnearTodosLosSantoslake(Peullá,Puntiagudo,Chilcón,Cayutué),nearLlanquihuelake(Ensenada,LosRiscos)andnearOsornocity(Wolffhügel,1933,1934).In ourpreviousreportweidentified G.paralysans inhistolog-icalsectionsofspinalcordfromcatsfromruralareasof PuertoMontt,ValdiviaandNieblainChile(Gómezetal.,2010).AllthesegeographicalregionsareimmersedintheValdiviantemperaterainforest(“BosqueValdiviano”)aparticularecoregionofsouthernChile(around37–48southlatitude).Wolffhügel(1934)alsomentionedsuspectcases of G.paralysans fromcatsinruralareasofNahuelHuapilakeandChubutprovinceinArgentina.Recently,alsoinArgentina,onecaseof G.paralysans infectionwas reportedintheareaofBaradero,BuenosAiresprovince(Guerreroetal.,2011).Bowmanetal.(2002)describedacaseofwhat wasprobably G.paralysans fromadomesticcatpresentedtotheCollegeofVeterinaryMedicineatCornellUniversity,Ithaca,NewYork,USA.Nomaleswerepresentinsamplescollectedatnecropsysoadefinitiveidentificationcouldnotbemade.Theoriginandtravelhistoryofthiscatisnot 380 M.Moronietal./VeterinaryParasitology 184 (2012) 377–380 known(DwightD.Bowman,personalcommunication,Jan-uary6,2011).ItislikelythatthiscattraveledtoanendemicareaandwasinfectedorwasbroughtintotheUSAfromanendemicarea.Thelifecycleof G.paralysans andstructureoflarvalstagesispresentlyunknown.Basedontheknownlifecyclesofothermetastrongylenematodes,varioustrueinterme-diateorparatenichostshavebeenpostulatedincludinglizards( Liolaemus spp),frogs,blowflies( Calliphoridae spp),someinsects( Coleoptera spp),mollusks,slugs,snails,andavarietyofrodents(Wolffhügel,1934;Gómezetal.,2010). Itisprobablethatthelackofappropriateintermediateorparatenichostsinotherregionsoftheworldlimitthedis-tributionof G.paralysans totheregionsofSouthAmericawhereithasbeenreported.Thislimitedgeographicdistri-butionalsosuggeststhatthecasereportedfromNewYork,USAdidnotoriginateinNorthAmerica.Additionallifecyclestudiestodeterminethestructureoflarvalsagesof G. paralysans areneededbeforeanattempttoidentifyinter-mediateorparatenichostscanbeinvestigated.MoleculartoolssuchasPCRalsoneedtobedevelopedtohelpanswerthesequestionsabouttheepidemiologyof G.paralysans . Itisalsopossiblethat G.paralysans isametastrongylepara-siteofsomeotherhostandthatinfectionsindomesticcatsareduetoaccidentalexposureofcatstoinfectivestagesof theparasite.ThemorphologicaldimensionsofmaleandfemalenematodesandthelocationwithinthehostinthepresentstudyaresimilartothosereportedbyWolffhügel(1933)inhisoriginaldescription.Presently, G.paralysans istheonlymemberofthegenus Gurltia inthefam-ilyAngiostrongylidae.OthervascularandneurotropicnematodesofthefamilyAngiostrongylidaeareincludedinthegenus Angiostrongilus ( Angiostrongyluscantonen-sis , Angiostrongylusvasorum )(Andersonetal.,1978).Wolffhügel(1934)foundedsimilaritiesbetweenthe G. paralysans and A.vasorum .However,hepointedoutthat G.paralysans had3pairsofbursalrayswhile A.vaso-rum possessedfourpairsofbursalrays.Ourstudysupporthisobservationthat3pairsofbursaraysarepresentin G.paralysans males.Additionally,hementionedthat G. paralysans didnothavelipsandoralpapillaewhilethesestructuresarepresentin A.vasorum .We alsosupporthisobservationsonthisparasiteincats.Bothliveinsidethebloodvessels; G.paralysans insidetheveinsoflep-tomeningesand A.vasorum insidetherightventricleandpulmonaryarteries.Henamedthegenus Gurltia inordertohonorErnstFrederichGurlt(1794–1882)aGermanveteri-naryanatomistandteratologist.Clinicalfindingsinalltheaffectedcatsinthepresentstudywereconsistentwithchronicandmultifocalordif-fusespinalcordlesionsbetweenT3andCd4segments(Dewey,2003).PelvicLimbtremorortremblingobserved inonecatmay resultfrommuscleweaknesssecondarytospinalcordorperipheralspinalnervealterationorpossiblyoccursasreflectionofneuropathicpain(Bagley,1992).Itis interestingtonotethatthecatreportedbyBowmanetal.(2002)f romCornellUniversity,USAhadlesionsbetweenL3andL6.Theprogressivecourseanddurationoftheneu-rologicsignsaresimilartothosepreviouslyreportedforinfectionsofcatswiththisnematode(Gómezetal.,2010).Suggestedmechanismsfordevelopmentofspinalcordvaricesincludesincreasedvenouspressureandveinenlargement(Moonisetal.,2003;Paldoretal.,2010). Mechanicalobstructionduetonematodesandvenousthrombosismay inhibitvenousreturnandresultinginvari-cosity.Myelopathyandradicolopathycanbeexplainedbyacombinationofvenousestasis,thrombosisanddilationthatcreateprogressivespinalcordandnerverootcompres-sionsimilartoneoplasia,othermass-likelesionsorspinalepiduralvarices(Moonisetal.,2003).Additionally,migra- tionoftheparasiteintothespinalcordparenchymacanproducedirectdamageandassociatedlocalinflammatoryresponsetothenematode.Theretrogradevenousrouteof parasiteinfectionisfoundin Schistosoma sppandmaybeusedalsoby G.paralysans who onlylieinveinsofthespinalcordandprobablybrain(KatchanovandNawa,2010).This isthefirstreportfeaturingandupdatingmorphologicalaspectof G.paralysans sincetheoriginalisolationanddescriptionmadefromWolffhügel(1933,1934)inChile. Acknowledgements Thestudywas supportbyanintramuralgrantfromDireccióndeInvestigaciónyDesarrollo,UniversidadAus-traldeChile(GrantNo.S-2011-49). 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