real-time ultrasound elastographic imaging of ocular and ... · ophthalmic surgery, lasers &...

Ophthalmic Surgery, laSerS & imaging · VOl 41, nO 1, 2010 135

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Real-TimeUltrasoundElastographicImagingofOcularandPeriocularTissues:AFeasibilityStudy

Efstathios T. Detorakis, MD, PhD; Eleni E. Drakonaki, MD; Miltiadis K. Tsilimbaris, MD, PhD; Ioannis G. Pallikaris, MD, PhD; Spiridon Giarmenitis, MD, PhD

n BACKGROUND AND OBJECTIVE:Thisstudyexaminesthevalueofultrasoundelastographyfortheexaminationofocularandperiocularstructures.

n SUBJECTS AND METHODS:Fivepatients,aged22 to75 years,who eachhadoneblind eyewere in-cluded.Patientsunderwentultrasoundelastographyoftheirblindeyeandperioculartissuesusinga7-13MHzprobe. Strain grayscale and color-coded elastographicmapswererecorded.Intheformer,aquantitativeassess-mentofsignalintensity(correspondingtoelasticprop-erties)forspecificanatomicalstructureswasperformed.

n RESULTS:Anteriorvitreousdisplayedintermediateelasticity,whereasposteriorvitreousdisplayedlowelastic-ity.Medialandlateralrectusmuscleelasticitywashigherinprimarypositionthaninadductionorabduction.

n CONCLUSION:Thepatternofelasticimaginginthevitreouscavitycouldbeattributedtoposteriorvit-reousdetachment,whereas thatofmedialand lateralrectus muscles may be related to the level of musclefiberstrain.

[Ophthalmic Surg Lasers Imaging 2010;41:135-141.]

From the Departments of Ophthalmology (ETD, MKT, IGP) and Medical Imaging (EED, SG), University Hospital of Heraklion, Crete, Greece.

Accepted for publication March 30, 2009.The authors have no financial or proprietary interest in the materials presented herein.Address correspondence to Efstathios T. Detorakis, MD, Department of Ophthalmology, University Hospital of Heraklion, Crete, Greece.doi: 10.3928/15428877-20091230-24

INTRODUCTION

Thedeterminationof theelasticityof living tissueshasbeenusedasanimportantindicatorofdiseasebecausethemechanicalpropertiesofdiseasedtissuearetypicallydifferent from those of the normal tissue surroundingthem.1 Elastography is a method of imaging and mea-suring the elastic properties of tissues based on staticcompression and cross-correlation methods.2The mainelastographic techniques include magnetic resonanceelastographyandultrasoundelastography.3Intheformermethod,constrainedmodulusreconstructiontechniqueshavebeenemployed,assumingthatthegeometryofnor-

malandsuspicioustissuesisavailablefrommagneticreso-nanceimagingsegmentation.3Inthelattermethod,thefootprintoftheultrasoundprobeisusedtocompressthetissuesaxiallyandtissueaxialdisplacementsareestimatedwithcross-correlationanalysisappliedtopre-decompres-sionandpost-decompressionechoes.3

Byemployingultrasoundelastography,avarietyofnormal and diseased living human tissues and organshavebeenevaluated,includinglymphnodes,4prostate,5articularcartilage,6pancreas,7kidney,8skin,9andbreast.10Through thedevelopmentofultra-fast algorithms tai-loredtosuitablehardware,ultrasoundelastographycancurrentlybeperformed ina typicalclinicalultrasound

136 cOpyright ©SlacK incOrpOrated

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settingatquasireal-time(approximatelyataframerateof8frames/sec)andwiththeuseofahandheldtransduc-er(asopposedtothepreviouslyusedframe-suspendedset-up),duringandsimultaneouslywithanultrasoundexamination.1Inthisstudy,wepresentfindingsfromul-trasoundelastographyinlivinghumanocularandperi-oculartissues.Itisapreliminaryfeasibilitystudyinblindeyes,whichcouldhelpindeterminingthepotentialroleofultrasoundelastographyintheevaluationofnormalanddiseasedocularandperioculartissues.

SUBJECTS AND METHODS

Patients were recruited from the Department ofOphthalmology of the University Hospital of Her-aklion,Crete,Greece.Elastography imagingwasper-formedattheDepartmentofMedicalImagingoftheUniversityHospitalofHeraklion,Crete,Greece.Fiveadult patients, three men and two women, who hadsufferedpermanentandcomplete(nolightperception)vision loss inoneeyewere studied.Theexaminationofblindeyeswasbasedonsafetyissuesbecausetheuseof acoustic radiation force as the stressingagentmayrequireintensitiesexceedingthoseallowedbytheU.S.Food and Drug Administration.11 Participants gavewritten informed consent to a protocol approved bytheInstitutionalReviewBoardinconformitywiththetenetsoftheDeclarationofHelsinki.

Meansubjectage(±standarddeviation)was52±7years,witharangeof22to75years.Demographicandclinicalcharacteristicsofsubjectsstudied,includ-ingage,gender,andcauseofunilateralblindness,arepresented inTable1.Amedical andophthalmichis-torywasrecordedfromeachpatient.Acomprehensiveophthalmicexaminationwasalsoperformed,includingapplanationtonometry,cornealpachymetry,andaxiallengthmeasurementoftheexaminedeye.

Each subject underwent combined ultrasound B-modeandelastographyimagingoftheblindeyeandip-silateralorbit.Allelastographicstudieswereperformedbythesameexperiencedexaminer(EED).Acommer-ciallyavailableultrasoundsystem(SiemensAntares,Pre-mium Edition; Siemens Medical Solutions, Erlangen,Germany),equippedwithspecificsoftwaretoperformelastography (eSie-touch elasticity; Siemens MedicalSolutions), was used. The ultrasound examination ofallvolunteersincludedB-modescanning(usinga7-13MHzprobe)andreal-timefreehandelastography.

Subjectswereexamined in the supineposition.Anadequate amount of coupling gel was applied over thegentlyclosedeyelids.Real-timefreehandelastographywasperformedbyapplyingsubtlemanualcompressionwiththetransducerovertheregionofinterest(ROI).TheROIwassettoincludetheeyeballandadjacentorbitalstruc-tures.Measurementswererecordedinatransversesectionthroughtheequatoroftheeyeball.TheB-modeandelas-tographicimages(colorandgrayscale)weredisplayedside-by-sideonasplit-screendisplay.Inthecaseofgrayscaleelastographicimages,thelowerluminositysignal(darker)represented areas of lower elasticity, whereas the higherluminosity signal (brighter) represented areas of higherelasticity.Inthecaseofcolor-coded(pseudo-chromatic)real-timeimages(superimposedontheB-modeimage),thecolorcodeindicatedtherelativestiffnessofthetissueswithintheROIandrangedfromred(moststiff)toblue(leaststiff).Greenandyellowcolorsindicatedintermedi-atestiffnesses.Color-codedimageswereconstructedau-tomaticallywiththesamesettingsthroughoutallstudies.To ensure reproducibility, three compression-relaxationcycleswereappliedtotheorbitandtheimageswerestoredascine-loopsinthememoryoftheultrasoundsystem.Toensurecorrectapplicationofthetechnique,onlytheim-ages where the elastogram consistently overlapped withtheB-modeimagewereusedforevaluation.

Table1

Demographic and Clinical Characteristics of Patients StudiedPatient Gender Age (Y) Eye Studied Cause of Visual Loss

1 Male 75 left Opticneuropathy

2 Male 62 Right absoluteglaucoma

3 Female 28 left absoluteglaucoma

4 Male 22 left Opticneuropathy

5 Female 58 Right Retinaldetachment

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Subjectswereimagedwiththeeyesinprimarypo-sition, adduction, and abduction. Transverse sections(throughtheequatoroftheglobe)wereexamined.Theopticnervedarkzonewasidentifiedinallcasesandusedasalandmarkfortheimagingoftheocularandorbitalstructures,includingtheanteriorandposteriorvitreouscavity,medialandlateralintraconalorbitalfatpads,andmedial and lateral rectus muscles. In one case (case 5inTable1,sufferingfromchronicretinaldetachment),theelasticpropertiesofdetachedretinaandsubretinalfluidwerealsoexamined.DigitalgrayscaleelastographicimageswerequantifiedandanalyzedusingeFilmwork-station(eFilmMedicalInc.,Toronto,Ontario,Canada)andthe imageprocessingtoolboxoftheEvoRadRIS/PACSsystem(EvoRad,Athens,Greece).

Thecross-sectionalareaofimagedstructures,includ-ingtheanteriorandposteriorvitreouscavity(anteriorandposteriortotheglobeequator),posteriorsclera(betweenthemedialandlateralrectusinsertions),andopticnerveandintraconalfatpads(betweentheopticnerveandme-dialorlateralrectusmuscle)weredelineatedattransversesectionsnearesttotheequatoroftheeyeball.Themeanlu-minositysignalofthedelineatedstructureswasmeasured(histogram,luminositychannel)usingAdobePhotoshop,version7.0(Adobe,SanJose,CA).Likewise,themedialandlateralrectusmusclesweredelineatedinprimarygaze,

adduction,andabduction.Themeanluminositysignalofdelineatedmusclesinadductionandabductionwasalsorecordedandrespectivevaluesbetweendifferentgazepo-sitionswerecompared(paired-samples t test).StatisticalanalyseswereperformedusingSPSS8.0software(SPSS,Inc.,Chicago,IL).

RESULTS

Elastographic imaging of ocular and periocularstructures resulted in reproducible findings in all sub-jectsexaminedinthisstudy.Ingrayscaleimages,thein-traconalorbitalfatpadsappearedwithahigherluminos-itysignal(moreelastic)thantheopticnerveandmedialandlateralrectusmuscles(Fig.1B).Attheposteriorpoleoftheglobe,arimoflowerluminositysignal(lesselastictissue)appearedinterlacedbetweentworimsofhigherluminosity signal (more elastic tissue), as presented inFigure 1B. These possibly corresponded to the sclera(lesselasticrim),retinaandchoroid(moreelasticrimattheinnersurfaceoftheglobe),andintraconalfatpads(moreelasticrimattheinnersurfaceoftheglobelater-allyandmediallytotheopticnerve).Theiridolenticulararea and anterior vitreous cavity appeared of interme-diateluminosity(intermediateelasticity)inallsubjects,whereastheposteriorvitreouscavityappearedoflower

Figure 1.Grayscaleultrasoundtransverseelastographicimageof(a)aneyeandorbitand(b)correspondingb-scanimage.Theretinaandchoroid(RC)arepresentedwithhigherluminosity(moreelastic)thanthesclera(*).Theintraconalfatpads(+)lateralandmedialtotheopticnervearealsoshownwithahigherluminosity(moreelastic).Themedialandlateralrectusmuscle(MRandlR,respectively)andtheopticnerve(ON)areshownwithintermediateluminosity.Theanteriorvitreouscavity(aV)isshownwithintermediateluminosity(intermediateelasticity)comparedwiththeposteriorvitreouscavity(lowerluminosityand,therefore,lowerelasticity).Thegrayscalefromwhite(moreelastic)toblack(lesselastic)isshownbetweenaandb.



luminosity(lesselastic).Acolor-codedimageandcor-respondingB-scanimageofaneyeandperioculartissuesarepresentedinFigure2(sameeyeasinFig.1).Meanluminosityvaluesofopticnerve,intraconalfatpads,lat-eralandmedialrectusmuscles(primarygazeposition),anteriorandposteriorvitreouscavity,andposteriorscleraarepresentedinTable2.

Detachedretinainaneyewithchronicretinaldetach-mentappearedasabandofhighelasticityembeddedwiththeposteriorvitreouscavity.Inthesameeye,subretinalfluidappearedwithlowerluminositysignal(lesselastic),retinalpigmentepitheliumandchoroidallayersappearedwithintermediateluminosity(intermediateelasticity),andscleraappearedwithlowluminosity(lowerelasticity).AneyewithchronicretinaldetachmentispresentedinFigure3(B-scanandgrayscaleelastographicmap)andFigure4(B-scanandcolor-codedelastographicmap).

Theopticaldensitiesofthemedialandlateralrectus

musclesweresignificantlydecreasedinbothadductionandabductioncomparedwiththeprimarygazeposition(Table3).Grayscaleultrasoundelastographicimagesofthelateralrectusmuscleinprimarypositionandabduc-tionarepresentedinFigure5.Color-codedelastographicimagesofthemedialrectusmuscleinprimarypositionandadductionarepresentedinFigure6.

DISCUSSION

Thisstudyevaluatedthefeasibilityofperformingul-trasoundelastographyinocularandperioculartissuesbyemployingacommerciallyavailablesystem.Resultsimplythatthetechniqueisfeasibleandcanprovideinformationoftheelasticityofocularandperioculartissuesthatmayhaveclinicalimplicationsinvariousconditions.

Resultsfromseveralpreviousstudiesemployingul-trasoundelastographyintheinvivoexaminationofvari-

Table2

Mean Area Delineated and Mean Luminosity Values (Mean ± SD) of Optic Nerve, Medial and Lateral Intraconal Fat Pads, Anterior and Posterior Vitreous Cavity, and Posterior Sclera

Delineated Structure Area (mm2, Mean ± SD) Luminosity (Mean ± SD)

Opticnerve 92.1±16.9 69.4±22.8

Medialandlateralintraconalfatpads 141.2±24.2 100.6±32.4

anteriorvitreouscavity 130.1±19.1 96.3±27.5

Posteriorvitreouscavity 113.0±40.3 25.1±10.6

Posteriorsclera 104.2±18.1 34.2±12.9

SD = standard deviation.

Figure 2.Color-codedultrasoundtransverseelastographicimageofthesameeyepresentedinFigure1(b)andcorrespondingb-scanimage(a).Thecolorscalefromblue(moreelastic)tored(lesselastic)isshownbetweenaandb.

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Figure 3.Grayscaleultrasoundtransverseelastographicimageofaneyewithchronicretinaldetachment(b).Thedetachedretina(RD)appearsmoreelastic(withhigherluminosity),comparedwiththeposteriorvitreouscavity(PV)andlong-standing(viscous)subretinalfluid(SRF).Thecomplexofretinalpigmentepithelium(RPe)andchoroid(C)alsoappearswithahighluminosity(elastic),whereastheanteriorvitreouscavity(aV)appearswithintermediateluminosity.Onthecontrary,thesclera(S)isshownwithalowluminosity(inelastic).acorrespondingb-scanimageisalsopresented(a),whereasthegrayscalefromwhite(moreelastic)toblack(lesselastic)isshownbetweenaandb.

Figure 4.Color-codedultrasoundtransverseelastographicimageofthesameeyepresentedinFigure3(b)andcorrespondingb-scanimage(a).Thecolorscalefromblue(moreelastic)tored(lesselastic)isshownbetweenaandb.

Table3

Mean Luminosity Signal of the Medial and Lateral Rectus Muscles in Primary Position, Adduction, and Abduction, and Statistical Significance of Respective Differences

Muscle Adduction Pa Primary Pa Abduction

Medialrectus 21.1±13.4 .11 25.8±12.1 .15 22.3±14.0

lateralrectus 23.1±17.8 .23 25.7±14.3 .16 22.9±16.7aPaired samples t test.



oustissues,otherthanocularandperiocularstructures,implythatthetechniquecanaccuratelyassesstheme-chanicalpropertiesoftissues,differentiatenormalfromabnormal tissues, and provide indications for the na-tureoftumors.4-10Theeyediffersfromotherorgansinwhichelastographyhasbeenappliedsofarbecauseitisnotsolidandhasaheterogeneousinternalstructure.Thecalculationoftheelasticmodulusofatissuedependsonassumptionsonitsproperties(ideallythetissueshouldbe incompressible, isotropic, and solid).2Thecyst-likeinternalconfigurationandheterogeneousarchitectureoftheeyeimplythatitmaydeviatefromthepreviouslyde-scribedidealelastictissuemodelandinsteaddisplay,atleastinpart,poroelasticproperties(inporoelasticmod-els,asolidskeletonincorporatesamountsoffluidwithinitspores).2Nevertheless, the fact that imagesobtainedfromallsubjectswerereproducibleandcompatiblewiththehistologiccharacteristicsoftissuesexaminedimplythat ultrasound electrography may be applied for thestudyofocularandperiocularstructures.ThetechniqueisnotcurrentlyapprovedbytheU.S.FoodandDrugAdministration for routine ophthalmic applications.11However,becausethestressingpulseisbrief(onlyafew

millisecondsinduration),thepotentialfordamagefromtemperature increase is minimized and probably doesnotintroduceaserioussafetyissue.12

Inthecaseoftheeyeball,thevitreouscavitydisplayedaheterogeneousappearanceinbothgrayscaleandcolor-codedelastographic images.Thesignal fromtheanteri-orvitreouscavitycorrespondedto intermediateorhighelasticity,whereas the signal fromtheposteriorvitreouscavity corresponded to low elasticity.This finding maybeexplainedbythefactthatalleyesexaminedhadpos-teriorvitreousdetachment (evident in indirectophthal-moscopy)andthustheposteriorvitreouscavitywasfilledwithaqueousfluid.The latterdisplayeda lowelasticitysignalduetoitsincompressiblenature.Onthecontrary,the degenerated vitreous scaffold (partly compressible)wasdisplacedintheanteriorvitreouscavity,whichthusdisplayedanintermediateelasticitysignal.However,thisfindingmayalsobeartefactual,resultingfromexcessiveincoherentfluidmotioninsidethevitreouscavityunderexternalcompression,ashaspreviouslybeendescribedforthyroidcysticlesionswithcolloidcontent.13

The fact that themedial and lateral rectusmuscles

Figure 6. Transverse b-scan images (a and C) and respectivecolor-codedultrasoundelastographicimages(bandD)ofaneyeinprimaryposition(aandb)andadduction(CandD).Thecentralportionofthemedialrectusmuscle(MR)displaysadifferentcolorpattern in adduction (red-yellow) than in primary position (blue-green),implyingdecreasedelasticityinthelattercondition.Thecol-orscalefromblue(moreelastic)tored(lesselastic)isalsoshown.

Figure 5.Transverse b-scan images (a and C) and respectivegrayscaleultrasoundelastographicimages(bandD)ofaneyeinprimaryposition(aandb)andabduction(CandD).Thelateralrectusmuscle(lR)isshownwithdecreasedluminosity(lesselas-tic) inabductioncomparedwithprimaryposition.Thegrayscalefromwhite(moreelastic)toblack(lesselastic)isalsoshown.

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displayed a signal of lower elasticity with the globe inprimarygazepositionandasignalofhigherelasticityinadduction or abduction (although not at a statisticallysignificantlevel)mayreflectthetensionstatusofmusclefibers in thesemuscles indifferent gazedirections.Thepossibilityofevaluatingtheelasticpropertiesofextraocu-lar muscles by ultrasound elastography may be appliedinconditionsinwhichmusclerigidityisaltered,suchasGraves’orbitopathy,inwhichrestrictivefibroticchangesrendertheaffectedtissuesinelastic.14Therefore,ifnorma-tivedataarecollectedontheelasticityofextraocularmus-cles,ultrasoundelastographycouldhavediagnosticvalueinthediagnosisofGraves’orbitopathyandpossiblyinthedifferentialdiagnosisbetweenGraves’orbitopathyandor-bitalmyositis,whichisacommonclinicalquestion.

Thequantitativeevaluationoftheelasticityoftheocularwallsmaybeusedintheassessmentoftheocularrigidity.Thelatteriscurrentlyindirectlycalculatedbymeasuringchangesintheintraocularpressurefollowinggradedvolumedisplacementandemployingnormativedatafromcadavericeyes(Friedenwalddiagram).15Thismethodhasreceivedcriticismbecausetheelasticprop-ertiesofcadavericeyesdifferfromthoseinlivingeyes.15Althoughmethodsofdirectmeasurementofocularri-gidityinlivinghumaneyeshavebeendescribed,theyare interventional and include the intraoperative in-traocularinsertionofmanometricprobes.16Theeasiernoninvasiveelastographicexaminationofocularrigid-itycouldthusleadtotheevaluationoftheroleofthisparameterinvariousconditions,includingglaucoma17andage-relatedmaculardegeneration,18inwhichrigid-itymayplayasignificantpathogeneticrole.

Although the current report did not include pa-tientswithintraocularorintraorbitaltumors,duetoitsdesignasafeasibilitystudyitwouldbereasonabletoas-sumethatoncethevalueofultrasoundelastographyforocularandperioculartissuesisestablisheditsusemaybeexpandedtotheevaluationofocularorperiocularneo-plasticconditions.Themethodisalreadyinwidespreaduseforthesystematicstudyofvariousnon-ophthalmictumors.4,5,7,8,10Thefactthatdetachedretinawasimagedin both grayscale and color-coded elastographic mapsimpliesthatthetechniquecanbeusedforthediagnosisand study of retinal detachment and possibly the dif-ferentiationbetweenretinaltissuehemorrhagicormem-branousformationsinthevitreouscavity.

Thesmallnumberofpatientsstudiedandnon-ran-domizedselectionmaybeconsideredweakpointsofthis

study.Furthermore,luminositysignalmeasurementcor-respondingtoelasticityvalueswasindirectlyobtainedus-ingAdobePhotoshop7.0becausetheelastographysystemuseddidnotprovidedirectluminositymeasurementsofthestructuresexamined.Ontheotherhand,thefactthatallpatientswereexaminedbythesameexaminerusingthesametechniquepossiblyenhancesthevalidityofresults.Futureresearchinthisareamaysetspecificnormativedataofelasticityforocularandperioculartissuesandexplorethepotentialroleofultrasoundelastographyintheevalu-ationofvariousophthalmicpathologicalconditions.

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