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Gurltia Paralysans ( Wolffhügel, 1933): Description Of Adults And Additional Case Reports Of Neurological Diseases In Three Domestic Cats From Southern Chile

Adults of Gurltia paralysans were obtained from veins of the spinal cord subarachnoid space from three domestic cats presenting with chronic paraparesis/paraplegia from rural areas of southern Chile. Four adult nematodes were collected (2 males and 2

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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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