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Rev Colomb Cienc Pecu 2018; 31(3):188-195 188 Revista Colombiana de Ciencias Pecuarias Ultrasound diagnosis of lateral digital extensor muscle, tendon, and synovial sheath alterations in Colombian creole horses with clinical signs of tarsus hyperflexion ¤ Diagnóstico ecográfico de las alteraciones del músculo extensor digital lateral, tendón y vaina sinovial en caballos criollos colombianos con signos clínicos de hiperflexión del tarso Diagnóstico ultrassonográfico das alterações do musculo digital lateral, tendão e bainha sinovial em cavalos crioulos colombianos com sinais clínicos de hiperflexão do tarso Fernando E Vega 1* MVZ, MS, cPhD; José R Martínez 2 MVZ, MS, PhD. 1 Facultad Medicina Veterinaria y Zootecnia, Universidad del Tolima. Barrio Santa Helena Parte Alta, Cód. Postal No. 730006299, Ibagué, Tolima, Colombia. 2 Línea de Investigación en Medicina y Cirugía Equina (LIMCE), Grupo de Investigación CENTAURO, Escuela de Medicina Veterinaria, Facultad de Ciencias Agrarias, Universidad de Antioquia UdeA, Calle 70 No. 52-21, AA 1226, Medellín - Colombia. (Received: March 01, 2017; accepted: November 24, 2017) doi: 10.17533/udea.rccp.v31n3a03 ¤ To cite this article: Vega FE, Martínez JR. Ultrasound diagnosis of lateral digital extensor muscle, tendon, and synovial sheath alterations in Colombian creole horses with clinical signs of tarsus hyperflexion. Rev Colomb Cienc Pecu 2018; 31(3):188-195. * Corresponding author: Fernando Emilio Vega Diaz. Facultad de Medicina Veterinaria y Zootecnia, Universidad del Tolima. Barrio Santa Helena ParteAlta. Código Postal No. 730006299, Ibagué, Tolima, Colombia. E-mail: [email protected] Abstract Background: Tarsus hyperflexion alters locomotion biomechanics in horses. This alteration is of frequent presentation in the Colombian creole horse (CCH). Objective: To determine the echographic alterations of lateral digital extensor (LDE) muscle, tendon, and synovial sheath in CCH with clinical signs of tarsus hyperflexion. Methods: Thirty horses were divided into two groups: 15 healthy horses with no history of locomotion defects (Group 1; control), and 15 horses with clinical signs of tarsus hyperflexion (Group 2). A cross-sectional and a longitudinal echocardiographic examination of the LDE muscle and tendon was performed in all horses, and a histopathological study was performed only to Group 2. Results: 86.7% of the horses showed echographic alterations, with 53.4% showing signs of adhesions in the LDE muscle and tendon in the lateral surface of the hock, where it crosses the tarsus. 33.3% presented increased tendon synovial sheath fluid. 13.3% showed no echographic alterations and 53.3% presented histopathological alterations. Conclusion: These findings may be related to the presentation of tarsus hyperflexion that could characterize the classic stringhalt in CCH. Keywords: Equine, hock hyperflexion, locomotion, mechanical claudication, stenosing tenosynovitis.

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Page 1: 188 riginal articles - bibliotecadigital.udea.edu.cobibliotecadigital.udea.edu.co/bitstream/10495/10720/1/VegaFernand… · Esta alteración es de presentación frecuente en el caballo

Rev Colomb Cienc Pecu 2018; 31(3):188-195

188

Revista Colombiana de Ciencias Pecuarias

Original articles

Ultrasound diagnosis of lateral digital extensor muscle, tendon, and synovial sheath alterations in Colombian creole horses with

clinical signs of tarsus hyperflexion¤

Diagnóstico ecográfico de las alteraciones del músculo extensor digital lateral, tendón y vaina sinovial en caballos criollos colombianos con signos clínicos de hiperflexión del tarso

Diagnóstico ultrassonográfico das alterações do musculo digital lateral, tendão e bainha sinovial em cavalos crioulos colombianos com sinais clínicos de hiperflexão do tarso

Fernando E Vega1* MVZ, MS, cPhD; José R Martínez2 MVZ, MS, PhD.

1Facultad Medicina Veterinaria y Zootecnia, Universidad del Tolima. Barrio Santa Helena Parte Alta, Cód. Postal No. 730006299, Ibagué, Tolima, Colombia.

2Línea de Investigación en Medicina y Cirugía Equina (LIMCE), Grupo de Investigación CENTAURO, Escuela de Medicina Veterinaria, Facultad de Ciencias Agrarias, Universidad de Antioquia UdeA, Calle 70 No. 52-21, AA 1226, Medellín - Colombia.

(Received: March 01, 2017; accepted: November 24, 2017)

doi: 10.17533/udea.rccp.v31n3a03

¤ Tocitethisarticle:VegaFE,MartínezJR.Ultrasounddiagnosisoflateraldigitalextensormuscle,tendon,andsynovialsheathalterationsinColombiancreolehorseswithclinicalsignsoftarsushyperflexion.RevColombCiencPecu2018;31(3):188-195.

* Correspondingauthor:FernandoEmilioVegaDiaz.FacultaddeMedicinaVeterinariayZootecnia,UniversidaddelTolima.BarrioSantaHelenaParteAlta.CódigoPostalNo.730006299,Ibagué,Tolima,Colombia.E-mail:[email protected]

Abstract

Background:Tarsushyperflexionalterslocomotionbiomechanicsinhorses.Thisalterationisoffrequentpresentation in theColombian creole horse (CCH).Objective:Todetermine the echographic alterationsoflateraldigitalextensor(LDE)muscle,tendon,andsynovialsheathinCCHwithclinicalsignsoftarsushyperflexion.Methods:Thirtyhorsesweredividedintotwogroups:15healthyhorseswithnohistoryoflocomotiondefects(Group1;control),and15horseswithclinicalsignsoftarsushyperflexion(Group2).A cross-sectional and a longitudinal echocardiographic examinationof theLDEmuscle and tendonwasperformedinallhorses,andahistopathologicalstudywasperformedonlytoGroup2.Results:86.7%ofthehorsesshowedechographicalterations,with53.4%showingsignsofadhesionsintheLDEmuscleandtendoninthelateralsurfaceofthehock,whereitcrossesthetarsus.33.3%presentedincreasedtendonsynovialsheathfluid.13.3%showednoechographicalterationsand53.3%presentedhistopathologicalalterations.Conclusion:ThesefindingsmayberelatedtothepresentationoftarsushyperflexionthatcouldcharacterizetheclassicstringhaltinCCH.

Keywords: Equine, hock hyperflexion, locomotion, mechanical claudication, stenosing tenosynovitis.

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Resumen

Antecedentes:lahiperflexióndeltarso(corvejon)alteralabiomecánicadeldesplazamientoenloscaballos.Estaalteraciónesdepresentaciónfrecuenteenelcaballocriollocolombiano(CCC).Objetivo:determinarlasalteracionesecográficasdelmúsculoextensordigitallateral(EDL),tendónyvainasinovialenCCCconsignosclínicosdehiperflexióndelcorvejón.Métodos:treintacaballosfuerondivididosendosgrupos:15equinosclínicamentesanos,sinhistoriadedefectosdelocomoción(Grupo1;consideradocomocontrol),y15equinosconsignosclínicosdehiperflexióndelcorvejón(Grupo2).SerealizóunexamenecográficotransversalylongitudinaldelmúsculoytendóndelEDLentodoslosanimales,yunestudiohistopatológicosoloalGrupo2.Resultados:el86,7%deloscaballosmostraronalteracionesecográficas.El53,4%mostrósignosdeadherenciasenelmúsculoytendóndelEDL,endondelasuperficielateraldelcorvejónsecruzaconeltarso.El33,3%presentóunaumentoenellíquidodelavainasinovialdeltendón.El13,3%nopresentóningunaalteraciónecográfica,yel53,3%mostróalteracioneshistopatológicas.Conclusión:estoshallazgospodríanestarrelacionadosconlapresentacióndehiperflexióndeltarsoquepuedecaracterizarelarpeoclásicoenelCCC.

Palabras clave: claudicación mecánica, equino, hiperflexión del corvejón, locomoción, tenosinovitis estenosante.

Resumo

Antecedentes: a hiperflexãodo tarso altera a biomecânicada locomoçãodos cavalos.Esta alteraçãoéde frequenteapresentaçãonocavalocrioulocolombiano (CCC).Objetivo:determinarasalteraçõesnoultrassomdomúsculoextensordigitallateral(EDL),otendãoeabainhasinovialemCCCcomsinaisclínicosdehiperflexãodojarrete.Métodos:trintacavalosforamdivididosemdoisgrupos:15cavalosclinicamentesaudáveissemhistóricodealteraçõesemlocomoção(Grupo1;consideradacomocontrolo),e15cavaloscomsinaisclínicosdehiperflexãodojarrete(Grupo2).SerealizaramavaliaçõesultrassonográficastransversaiselongitudinaisdomúsculoedotendãodoEDLnatotalidadedosanimaiseestudohistopatológicosóaoGrupo2.Resultados:o86.7%dosequinosmostraramalteraçõesnoultrassom,o53.4%mostrouaderênciasnotendãodoEDLnaproximidadeondecruzaasuperfícielateraldojarrete,o33.3%apresentouaumentodolíquidodabainhasinovialdotendão,o13.3%nãoapresentounenhumaalteraçãoultrassonográficaeo53.3%mostroualteraçõeshistopatológicas.Conclusão:essesachadospodemestarrelacionadosàapresentaçãodahiperflexãodotarsoquepoderiamcaracterizaroarpejamentoclássiconoCCC.

Palavras-chave: claudicação mecânica, equino, hiperflexão do jarrete, locomoção, tenossinovite estenosante.

Introduction

Tarsus hyperflexion is a sign of biomechanicalalterationinseveralclinicalconditionsaffectingthepelviclimbsofhorses(e.g.bonespavin,suspensorydesmitis,alterationsinthefemorotibiopatellarjoint,andclassicalAustralian stringhalt).Therefore, specificdiagnosticapproaches such as clinical evaluation, anestheticblocks, radiology,ultrasound,andelectromyographyarerequiredtodeterminetheoriginofthisalteration,although insomecases it isconsideredof idiopathicorigin(Duqueet al.,2014).However,mostcliniciansinitiallyrelatecasesoftarsushyperflexiontoclassicalstringhaltintheColombiancreolehorse(CCH).

Classic stringhalt-related tarsus hyperflexion isoneoftheexclusivepathologiesinCCH,affectingthe

sportsperformanceoftheanimals.Theappearanceof the pelvic limb affected by tarsus hyperflexionhas been traditionally considered an inheritedcondition, although it has not been demonstrated.Stringhalt causes economic losses due to rejectionfrom competition and reproduction.The almostunmistakableclinicalsignofclassicstringhaltisaninvoluntaryhyperflexionofthetarsus.

Theetiologyofclassicstringhalt isstillunclearand,inmanycases,itremainsunknown.Neuropathicmuscleatrophyofthelateraldigitalextensor(LDE)musclehasbeenreportedasapossiblecause(Valentine,2003;Araujoet al.,2008).Otherresearchersconsiderpathologiesaffecting tarsusorhock joints, suchasosteoarthritis,mayinducethiscondition(Crabillet al., 1994).Tarsusinjuries,specificallythoseaffectingits

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lateralaspect(femorotibiopatellarjoint),nervelesions(degenerationofthesciaticnerveandperoneusnerves)andfootlesionscancausespasmodiccontractionofthemuscles,flexingthepelvicextremityand,therefore,inducethecondition(Cahillet al.,1985;Crabillet al., 1994;Arayaet al.,1998).

Ultrasonography is awidely used diagnosticimagingtechniquetoevaluateinjuriestosofttissuesand synovial structures (Whitcomb, 2006;Garret,2014).However, its usehasnotbeen standardizedfor the studyanddiagnosisof stringhalt inhorses.The tarsus is a complex anatomical regionwith alarge number of tendons, ligaments, and synovialstructures (Dik, 1993).Therefore, comprehensiveknowledgeof theregionalanatomyandultrasoundtechniquearerequiredtosuccessfullyperformtarsusultrasonography(Whitcomb,2006).

TheLDEmuscle, its tendon, and the associatedsynovial sheathcanbeaccessedbyultrasonographyfrom the lateral sideof thepelvic limb (tarsus) andthe proximal third ofmetatarsus III, respectively,through transverse and longitudinal sections (Reef,1998;Whitcomb,2006;Garret,2014).Undernormalconditions,LEDmuscleandtendonareobservedusingacross-sectioninanovalsegment,withwell-definedbordersandhomogenousechogenicity.Inalongitudinalsection,thetendonshowsaparallelfibrillarpatternandwell-definededgesthroughoutitslength(Dik,1993).

The cause of classic stringhalt in theCCHhasbeendiagnosedwithultrasonographyonalterationstotheLDEmuscleandtendon,andsynovialsheathadhesions. The treatment described for classicstringhalt is tenectomy of the LDE and partialmyectomy (Sullins, 2002).Adherences can bepreventedwithmedicalproceduresthatimprovethecondition.Althoughresultsarenotalwaysimmediate,prognosisisfavorable(Stashak,2004;Torre,2010).

To the best of our knowledge, no studies haverelatedstringhalttoalterationsofeitherLDEmuscle,itstendon,oradhesionsofthesynovialsheath.TheobjectiveofthisstudywastoestablishthepresenceofLDEmuscle,tendon,andsynovialsheathalterationsusinganultrasonographictechniqueintheCCHwithclinicalsignsoftarsushyperflexion,comparingtheaffected structureswith those observed in healthy

horses.Additionaly,adhesionsbetweenthetendonanditssynovialsheathwerestudiedandhistopathologyoftheLDEmuscleandtendonwasconducted.

Materials and Methods

Horses

Thirty adultCCHs fromcommercial stallsweremonitored, regardless ofweight, age, or sex.Twoexperimentalgroupswereanalyzedbyultrasound.Thefirstgroup(control)consistedof15clinicallyhealthyhorses,with no history of locomotion alterations.This statuswasconfirmedbyageneralandspecificphysical examination of the locomotor system (instatic anddynamic), as referredbyStashak (2004).Thesespecimenswereevaluatedbyacross-sectionaland longitudinalultrasoundexaminationof theLDEmuscle and tendon (Garret, 2014).Thisgroupwasconsideredas reference for thenormalfindings.Thesecondgroupconsistedof15horseswithclinicalsignsofhockhyperflexion,confirmedbyphysicalexaminationasproposedbyStashak (1987).TarsalhyperflexionwascategorizedaccordingtothegradingdescribedbyHuntingtonet al. (1989).Thesespecimenswerealsosubjected toultrasoundexamination, evaluating thestructuresofLDEmuscle,tendon,andsynovialsheath,inordertocomparetheirresultswiththoseofGroup1.Radiographicevaluationwasalsoperformedtothisgroup.Noanestheticdiagnosticblockswereused todismissothercausesofhyperflexion.

Ultrasound, radiographic, and histopathological evaluations

Horsesfrombothgroupsweresubjectedtophysicalrestriction.Beforescanning,trichotomyoftheareawasperformediftheownerauthorizedtheprocedure;otherwise,thecoatwasremovedusingscissors.AnAquilaVETultrasoundscanner,manufacturedbyPieMedical,fromMaastricht,TheNetherlands,equippedwithalinear8.0MHZultrasonictransducer,attachedtoastandofpad,wasused.TheexaminationoftheLDEmuscleandtendonwascarriedoutwhenthesestructureswereintensionorsupportingtheirweight,becauserelaxationofthetendonscausesareductioninthegrayscaleoftheimage,producinghypoechoicartefactsthatcouldbeconfusedwithlesions(Woodet al.,1991;BoswellandSchramme,2000).

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Ultrasound evaluationswere performed in twoplanesoftherightangle.Transverseplanesectionswereperformedtoevaluatethesizeandechogenicityofthesection.Byslightlyrotatingthebackofthetransducer,theoptimalangleofpresentationoftheultrasoundwasdefined.Whentheimagewasbrighterthanthepreviousones,therecommendedangleforthestudyofthemuscleand tendon in the examined areawas established.Subsequently, longitudinal plane sections wereperformedtoestablishthelengthandmorphologyofthemuscularandtendinousfibrils.Imageenhancementwasachievedbyslowlymovingthetransducertothelateralandmedialsides,comparingtherelativeechogenicityand internal alignment of themuscle and tendonfibersunder study.Once the transducerwas located,measurementsoftheLDEtendonthicknessweretaken,aswellasof the spacebetween the tendonsynovialsheathwhereitcrossesthelateralborderofthetarsus.

Specimens fromGroup 2were also subjectedto radiographic andhistopathological examination.Radiographicstudiesfromthekneetothethirdphalanxwere takenwith aDonmun-100P,manufacturedbyDongmun, fromGoyang City, SouthKorea,considering four projections:Medial-lateral (ML),plantar-dorsum(PD),lateral-lateralormedial-oblique(LLMO),andmedialdorsal-planeoroblique-lateral(MDOL). The examination was carried out todetermineiftherewerepathologiesotherthanthoseofsofttissuethatwouldalterthepossibleresultsofthestudy.Insuchcase,anewpatientwasadmittedtothegroupfulfillingtheinclusioncriteria.

Samples of theLDEmuscle and tendonwereobtainedbymyotenectomyandtransportedina10%formalin solution. Sampleswere fixed in paraffinandstainedwithhematoxylinandeosintodeterminemixed polyneuropathywith axonal degenerationanddemyelinationofnervefibers(Armengouet al., 2010).Histopathologicalstudieswerecarriedoutonmuscleandtendonsamplestocorrelatethesewiththeultrasoundfindings.

Statistical analysis

The data obtained from echographic andhistopathological examinationswere processed bydescriptive statistics and presented in percentages

withrespecttoallthehorsesinGroup2withsignsof evident tarsus hyperflexion.These resultswerecomparedwithGroup1,considerednormal(nosignsofhyperflexion).At-testwasusedtocomparetendonthicknessandthespacebetweenthetendonsynovialsheathwhereitcrossesthelateralborderofthetarsus.Bothmeasurementswere done for each limb andcontralateral,bygroup,andbetweengroups(1and2).Ap<0.05wasconsidersignificant.

Results

Group1(control)didnotshowanypathologicalfindingsonphysicalandclinicalexaminations.Thetransverseplaneechographicevaluationofthisgroupshowedanovalsectionwithwell-definedbordersandahomogenousechogenicity.Awell-definedparallelfibrillar pattern in the longitudinal planewas alsoobserved(Figure1A).

FivehorsesinGroup2showedsignsofbilateralhyperflexion(with4/5to5/5degrees),and10horsesshowed unilateral hyperflexion (with 1/5 to 3/5degrees),accordingtoHuntingtonet al.(1989).An86%ofthehorsesinGroup2showedechographicalterations.A 53.3% (8/15) showed compatiblefindingsofLDEtendonadhesions(Figure1B)anda33.3%(5/15)showedanincreaseinLDEtendonsynovialsheathfluid(Figure1C).Twohorseswithincreasedsheathfluidpresentedbilateralhyperflexionand4/5degreesofflexion.Thethreehorsesremainingshowedunilateral hyperflexion and3/5 degrees offlexion.Finally,noechographicalterationswerefoundin13.3%(2/15)ofthehorsesthatpresentedunilateralhyperflexionwith1/5degreesofflexion.Theequineswiththegreatestalterationswerethoseshowingthehighestdegreeofflexion.Noradiographicalterationswerefoundinthisgroup.

Measurements,byanimalandgroup,oftheLDEtendon thickness aswell as space between tendonsynovial sheathwhere it crosses the tarsus lateralborder are shown inTable 1.The comparison ofmeans(SD±)ofthevariablesineachgroupdidnotshowsignificantdifferences.However,asignificantdifference(p<0.05)wasfoundwhencomparingthetwovariablesbetweengroups.

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Figure 1.Ultrasoundimages(linear8.0MHZultrasonictransducerwithcoupling)ofLDEtendonandsynovialsheathwhereitcrossesthelateralborderofthetarsusinaCCH.A)TransverseultrasonographicimageofanormalLDEtendon(blackarrow)anditssynovialsheath(whitearrows).B)TransverseultrasonographicimageofanabnormalLDEtendonoftarsushyperflexion,showingadhesionsbetweenthetendonandthesynovialsheath(whitearrow).C)Transverseultrasonographicimageofanabnormaltarsus(hyperflexion)showingliquidsbetweenthesynovialsheathandtheLDEtendon(whitearrow).

Table 1. Ultrasound measurements of the LDE tendon thickness as well as space between tendon and synovial sheath where it crosses the lateral border of the tarsus, of both pelvic limbs of healthy horses (Group 1) and of horses affected by tarsus hyperflexion (Group 2).

Limb evaluated Mean Standard error SD± Variance Minimum MaximumHealthy horses (Group 1)

Thickness of the LDE† tendon (mm)

RPL* 4.89Aa 0.16 0.63 0.40 3.9 5.9

LPL** 4.84Ac 0.16 0.62 0.38 4.1 5.9

Space between the LDE† tendon and the synovial sheath (mm)

RPL 1.23Ba 0.04 0.15 0.02 1 1.5

LPL 1.21Bc 0.04 0.16 0.03 1 1.4

Horses affected by hock hyperflexion (Group 2)Thickness of the LDE† tendon (mm)

RPL 4.17Ab 0.27 1.06 1.12 2.7 5.4

LPL 4.12Ad 0.20 0.78 0.61 2.7 5.4

Space between the LDE† tendon and the synovial sheath (mm)

RPL 0.63Bb 0.05 0.20 0.04 0.3 1.1

LPL 0.54Bd 0.03 0.13 0.02 0.4 0.8

SD±: Standard deviation. Same capital letters show no difference between limbs of the same group for each variable. Different lowercase letters show significant difference (p<0.05) between limbs of different groups for each variable. †Lateral digital extensor tendon. *Right pelvic limb. **Left pelvic limb.

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Regarding the histopathological study, onlysamples from eight horses fromGroup 2 (53.3%)showed shape and sizemultifocal irregularities offascicularmusclefibers.

Discussion

Tarsus hyperflexion has been linked to otherpathologiesthatalterthebiomechanicsoftherelatedjoint (bonespavin,suspensorydesmitis,stifle jointpathologies),beingsomeof thestructuresreportedelsewhere (described as secondary or incidentalfindings in some cases) the ones evaluated in thisstudy. Consequently, tarsus hyperflexion cannotbe only limited to the stringhalt types describedin the literature. Therefore, specific diagnosticaids are needed to differentiate and dismiss otheretiologies. In the present study, anesthetic blocksand electromyographywere not performed, sowedescribedclinicalcasesastarsushyperflexioninsteadofclassicstringhalt.

Control statuswas assigned toGroup1 due toabsenceoflamenessorclinicalsignsofhyperflexionat initial examination. In addition, those animalshadnohistoryof treatments for recent locomotionconditions.Likewise, normality of structureswasverifiedbyechographicevaluation,asdescribedbyGarret(2014),soresultsobtainedinthegroupwithtarsushyperflexionwerecomparable.

ClinicalevaluationofGroup2verifiedvariabilitybetween hyperflexion degrees, and unilateralor bilateral presence of hyperflexion.Absenceof abnormalities (as determined by radiologicalevaluation) dismissed other pathologies that,accordingtostateofevolutionandseverity,couldleadtogaitdisorderssimilartohyperflexionasreportedinclassicstringhalt.However,noanestheticdiagnosticblocks (to tibial or peroneal nerves)were used todismiss other causes of tarsal pain.This could beconsideredalimitationofthepresentstudy.

Abnormal ultrasoundfindings inGroup2werein agreementwith those reported byReef (1998),Stashak(2004),andGarret(2014).Undefinedborderscharacterize thesefindings, aswell as non-parallelfibrillarpatternsinmosttendons,andnoechogenic

homogeneity,contrastingwiththefindingsdescribedinGroup1,whichdidnotpresentthecharacteristicsignofhyperflexionandotherlocomotionalterations,asdescribedabove.Nevertheless,itisunknownwhytheLDEmuscleendsupinvolvedinahyperflexionthatshowscertaindegreesofimprovementwiththetenectomy(Stashak,2004;Torre,2010),afactthatencouragesfurtherinvestigationintothecauseofthisclinicalcondition.

DuringthemyotenectomyprocedureinpatientsinGroup2,agreatertensileforce(uptotwopeople)was required to remove the ruptured tendon in itsdistalpart.Thisobservationwaspossiblyduetotherupture of the adhesions thatwere formed aroundthetendonwhencrossingthetarsus,asitwasfoundechographicallyinourstudy(53.3%),andpreviouslydescribedbyStashak (2004).Although there is noelucidated cause of classic stringhalt in theCCH,it has been described as idiopathic (Duqueet al., 2014).However, there is a lackof research aimedat considering the inflammatory process in theLDEmuscularpackagederivedfrominjurydue torepetitiveexercise(Martínezet al.,2007).

Fivehorses(33.3%)presentedalterationsinthesynovial fluid volume according to the ultrasoundexamination.Thesefindingsarepossiblyrelatedtobiomechanical stress, generating inflammation andadhesions,aspreviouslydescribed(Stashak,2004).Althoughtheoriginofthefluidwasnotdetermined,the effusionwas present, in contrast towhatwasobserved inGroup 1 horses.On the other hand,onlytwohorses(13.3%)withtarsushyperflexionoflowerdegreedidnotshowanyultrasoundfindings.Therefore,itcouldbeinferredthatflexionseverityisrelatedtothepresenceofultrasonographicalterations(Whitcomb,2006;Garret,2014).

The LDE tendon thickness andwidth of thespacebetweensynovialsheathandthesametendonwereequalbetweenlimbsofthesamehorse,ineachof the two groups.These findings contrastwhencomparingbetweenthetwogroups.Group2showedsignificantlysmallermeasurementsbybothvariableswhencrossing the lateralaspectof the tarsus.Thisnarrownesscouldbeclinicallyrelatedtohorse`shockstenosingtenosynovitis,leadingtothepresentationofstringhalt-likemanifestations,followedbyadhesions

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reportedinourstudyandbyotherauthors(Stashak,2004),possiblyduetoinflammatoryprocessesasaresultofrepetitiveexercise(Martínezet al.,2007).

Histopathologicalfindingswerepossiblyassociatedwithaxonaldegenerationandvacuolizationofnervefibers,aspreviously reported inclassicstringhalt inCCH(Duqueet al.,2014).Similarly, thesefindingscanbeassociatedwithaxonopathyandneuromusculardeficit(Domangeet al.,2010;Penningtonet al.,2011;OliverandSuarez,2016).Therefore,alocalizednervedysfunctionmaybe involved in thepresentationofhyperflexion,whichcharacterizesbothstringhalttypes.

Electromyographicevaluationwasnotperformedinourstudy.Weconsiderthatthisdiagnosticapproachcouldhaverevealedsimilarfindingstothosereportedby other authors (Duque et al., 2014;Oliver andSuárez, 2016). Similar histopathological findingsobservedinthisstudywouldreaffirmthemyoelectricdeficits reported for tensionandflexionduring theLDEevaluation.Ontheotherhand, it is importanttoemphasizethatnoneofthepreviouslydescribedstudiesusedultrasoundasadiagnosticaid.

In this study, the association observedbetweenclinical,echographic,andhistopathologicalfindingsreveal a relationship between the presence ofalterations and the degree of severity. Horsespresenting obvious alterations in themyofibrillarpattern showed the highest degree of flexion,independentlyofwhetheritwasunilateralorbilateraltarsushyperflexion.

Finally, 86.6% of horses with signs of hockhyperflexionshowedechographicalterationsoftheLDEtendonandsynovialsheath.Whenconfrontingthese findings with 53.3% of horses showinghistopathologicalchanges, inferencecouldbedoneonthepossiblecauseofstringhalt.However,thewayinwhichhistopathologicalchangesaregeneratedinthetwotypesofstringhaltisstillnotclear.Australianstringhaltfocusesondamagescausedbyaneurotoxinthatcompromisesseverallongandperipheralnerves,incontrasttotheclassicstringhalt,whereachronicinflammatoryprocessintheLDEtendonalterstarsusbiomechanics(Huntingtonet al.,1989;Penningtonet al., 2011). Nevertheless, the histopathologicresults show similar neuromuscular alteration.We

hypothesize that neuromuscular damage in classicstringhaltcouldbesecondarytochronicinflammatoryprocesses(adhesions)derivedfromrepetitiveinjury(trauma),particularlyintheCCH.

Inconclusion,theultrasoundandhistopathologicalresultsinthisstudyareindicativeofalterationsoftheLDEtendonandsynovialsheathcausedbytarsushyperflexion,possiblyrelatedtoclassicstringhaltintheCCH.

Acknowledgments

The authors acknowledge funding from theResearch and ScientificDevelopmentBureau ofUniversidad del Tolima (Colombia), and thankthe fellowsat thepathology laboratoryatFacultaddeMedicinaVeterinaria yZootecnia for samplesprocessing.

Conflict of interest

The authors declare they have no conflicts ofinterestwith regard to thework presented in thisreport.

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