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Imaging of the spine and spinal cord: An overview of magnetic resonance imaging (MRI) techniques
VARGAS GOMEZ, Maria Isabel, BOTO, Jose Manuel, MELING, Torstein
Abstract
This review will discuss conventional and advanced magnetic resonance (MRI) imaging techniques used to study the spine and spinal cord according to the anatomical structures and clinical indications. Clinical challenges that neuroradiologists may face are also discussed, such as the "when" and "where" concerning the use of each technique, and in which pathology or clinical scenario each technique is useful. Finally, some "tips and tricks" to overcome the challenges are provided with clinical examples.
VARGAS GOMEZ, Maria Isabel, BOTO, Jose Manuel, MELING, Torstein. Imaging of the spine and spinal cord: An overview of magnetic resonance imaging (MRI) techniques. Revue
neurologique , 2020
DOI : 10.1016/j.neurol.2020.07.005 PMID : 32800350
Available at:
http://archive-ouverte.unige.ch/unige:143615
Disclaimer: layout of this document may differ from the published version.
International meeting of the French society of neurology 2020
Imaging of the spine and spinal cord: An overview of magnetic resonance imaging (MRI) techniques
M.I. Vargas
a,b,* , J. Boto
a, T.R. Meling
b,caUnitofDiagnosticNeuroradiology,DivisionofNeuroradiology,UniversityHospitals,GabriellePerretGentil4,1205 Geneva,Switzerland
bFacultyofMedicine,UniversityofGeneva,Geneva,Switzerland
cDivisionofNeurosurgery,GenevaUniversityHospitals,Geneva,Switzerland
1. Introduction
Imaging protocols are less standardized forthe spine and spinecordthanforthebrain.Themostimportantdifficulties for the optimization of sequences are due to the many interfacesthatexistinthisregion,suchasbone-cerebrospinal fluid(CSF)andspinalcord-CSF,theproximityofthelungs,as wellasthemobilecharacterandsizeofthespinalcordandits adjacentstructures.
Inthisreview,wedescribethedifferentMRItechniquesby the various anatomical structures (i.e. white matter, gray
matter,CSF,vessels,leptomeninges,nervousstructure,bone anddiskstructures),themostadequatetechnicalprotocols, thespecificitiesofeachsequence,inwhichclinicalsituation they should be used with which disease, and in which situationstheadditionofcontrastagentisnecessary.
2. Sequences: general concepts
There are sequences indispensable to a basic MRI clinical protocol of any spine or spinal cord examination. These sequencesarefastspinecho(FSE)T2andspinecho(SE)T1.In revue neurologique xxx (2020) xxx–xxx
*Correspondingauthorat:UnitofDiagnosticNeuroradiology,DivisionofNeuroradiology,UniversityHospitals,GabriellePerretGentil4, 1205Geneva,Switzerland.
E-mailaddress:maria.i.vargas@hcuge.ch(M.I.Vargas).
info article
Articlehistory:
Received5July2020 Accepted17July2020 Availableonlinexxx
Keywords:
Spine Spinalcord MRI Tumors Inflammation
Vascularmalformations
abstract
Thisreviewwilldiscussconventionalandadvancedmagneticresonance(MRI) imaging techniquesusedtostudythespineandspinalcordaccordingtotheanatomicalstructures andclinicalindications.Clinicalchallengesthatneuroradiologistsmayfacearealsodis- cussed,suchasthe‘‘when’’and‘‘where’’concerningtheuseofeachtechnique,andin whichpathologyorclinicalscenarioeachtechniqueisuseful.Finally,some‘‘tipsandtricks’’
toovercomethechallengesareprovidedwithclinicalexamples.
#2020TheAuthor(s).PublishedbyElsevierMassonSAS.Thisisanopenaccessarticleunder theCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).
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Availableonlineat
ScienceDirect
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https://doi.org/10.1016/j.neurol.2020.07.005
0035-3787/#2020TheAuthor(s).PublishedbyElsevierMassonSAS.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http://
creativecommons.org/licenses/by-nc-nd/4.0/).
addition,allspinalinvestigationsshouldhavesequencesin bothsagittalandaxialplanes,whichhelptoidentifytheexact locationandabettervisualizationofthelesions(Fig.1).
Advanced sequences are:diffusion and diffusiontensor imaging (DTI); vascular sequences or angio-dynamic MRI;
constructiveinterferenceinsteadystate(CISS)orT2(sampling perfectionwithapplication-optimizedcontrastsbyusingflip angle evolution [SPACE], 3D STIR SPACE sequence; phase contrastMRI;perfusionsequences;spectroscopyandfunctio- nalimaging.
2.1. ShortTauInversionRecovery(STIR)
Short tau inversion recovery (STIR) is also a conventional sequencewhereabnormalitiesappearashyperintensitiesin the spinal cord and in the bone and disk structures. This sequencehasahighsensitivity,butalowerspecificity.Ithelps todetectabnormalitiesofdifferentorigins,suchasinfections orprimaryorsecondarytumorlesionsofthespine,particu- larly atthe level ofthevertebral body. Italso hasabetter capacitytodetectmostspinalcordlesionsinpatientswith multiplesclerosisthanothersequences[1].
2.2. DiffusionTensorImaging(DTI)
Diffusiontensorimaging(DTI)isanadvancedsequencethat canbeperformedat1.5Tand3T.Thebisnotthesameasfor
the brainandalowerbisused(between500to800mm/s), principallyduetothefactthatthediffusionofwatermolecules inthespinalcordoccursmainlyinthecranio-caudaldirection [2,3].Both1.5Tand3Tmagneticfieldshaveadvantagesand disadvantages;inthe1.5T,geometricartefactsarelessmarked, butahigherfieldallowsbetterspatialandtemporalresolution.
Furthermore, geometric distortion has now been partially solvedbytheavailabilityofnewsequencetypesbasedonthe readoutsegmentationoflongvariableecho-trains(RESOLVE) or zoomed echoplanarimaging. Bothfieldsare affectedby inhomogeneity artifacts. For DTI, although the number of directions varies from one author to another, at least six directionsarenecessarytocalculatefractionalanisotropyor meandiffusivityandtheapparentdiffusioncoefficient(ADC).A reasonablenumberwouldseemtobe20,andinourhospital, we use between 25–30. Principal clinical indications are ischemia (Fig. 2), surgical planning for spinal cord tumors, differentiation between spondylodiscitis and inflammatory degenerativechangesofthevertebralbodyendplates,andthe follow-upofdegenerativecervicalmyelopathy[4–8].
2.3. VascularsequencesorangiodynamicMRI
Vascular sequences or angiodynamic MRI are 3D time- resolved imaging of contrast kinetics (TRICKS), 4D time- resolvedangiographyusingkeyhole(TRAK),ortime-resolved acquisition (TRAQ). In our hospital, we have developed a Fig.1–Forty-year-oldwomanwithneuromyelitsoptica(NMO).SagitalT2WI(a),T1WI(b)andT1Gd(c)aswellasaxialT2WI (d)andT1Gd(e)imagesshowsevereandwidespreadlowercervicalandthoraciccordinvolvement(arrows)withcord tumefaction,prominentedemashownasT2WIhyperintensity(aandd)andmarkedenhancement.
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three-phasessequencemadein-house,witharterial,venous andlateacquisitionsassociatedwithadelayedhigh-resolu- tion sequence. Thissequence isisotropic, with atemporal resolution of 1min and is used in cases of arteriovenous malformations or for the localization of the Adamkiewicz arterybeforeaspinesurgery[5,8,9].
2.4. CISSorT2SPACE
CISSorT2SPACEareheavilyT2-weighedsequenceswherethe flow-artifacts are less visible than inconventional MRI T2 sequences. They are very useful to view thin and tiny structures, such as cyst walls of congenital or traumatic origin, dural herniation of the spinal cord (Fig. 3), cystic tumors,arachnoidwebs,synechiae,post-traumaticpseudo- meningoceles,duralbreach,CSFleaks,andnormalordilated vessels.
2.5. Phase-contrastMRI
Phase-contrast MRI allows qualitative and quantitative imagingoftheCSFandthestructureswithinandsurround- ingit.Visualizationcanbeinstaticformorcineview,the
latterfortheanalysisofCSFflow.Thephysicalprincipleof thissequenceisthatmotioninavoxelinducesadditional dephasingofthesignal.Withanappropriatesequencethat providesphaseimagesinadditiontomagnitudeimages,itis possibletomeasuretheflowvelocityinavoxel[10].Aphase- encoding gradient can be applied in one of the three directionsofspacetodetectflowinthatspecificdirection.
Iftheflowpassingthroughtheimagingplaneneedstobe measured, thephase-encodinggradient shouldbeapplied in the slice-encoding direction. Clinical indications are arachnoid webs, post-traumatic synechia, and Chiari malformations.
2.6. Perfusionsequences
Perfusionsequenceswithdynamiccontrast-enhancementT1 arepreferabletoT2-basedperfusionatthespinelevel.This techniqueallowsadynamicvisualizationofcontrast-behavior inthetissues.Itisusedtoanalyzeprimarytumorsinorder toevaluatehigh-gradecomponents (Fig. 4)andtoevaluate extraduralspinalmetastasesandtheirvascularization,which, in turn, helps in the selection of patients amenable to endovasculartreatment[11].
Fig.2–Fifty-seven-year-oldmanwithcordischemiasecondarytoaorticdissection.CoronalCTA(a)showsStanfordtypeA aorticdissection(aorticarchdissectionnotshown)withanintimalflapatthelevelofthethoracicandabdominal descendingaorta(arrowheads).Sagittal(b)andaxial(d)DWIb800imageshowsdiffusionrestrictionoftheupperthoracic cordreflectingischemia(arrows).Notethattheadjacentvertebraealsorestrictdiffusion(whiteasteriksinb)confirming coexistingboneinfarct.Anunaffectedsegmentofthecervicalspinalcord(blackasterisks)isshowninsagittal(b)andaxial (c)DWIb800inordertoallowcomparison.AxialT2WI(eandf)oftheaffectedcordshowhyperintensity(arrows)reflecting irreversibleischemia.
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Fig.4–Sixty-one-year-oldwomanwithanependymomaofthecervicalcord.Thereisaheterogeneousintramedullarysolid andcysticmassontheuppercervicalcordatthelevelofC2(arrows)associatedwithcordedemaseenashyperintensityon sagittalT2WI.Thesolidcomponentofthemassenhancesstrongly(arrowsincandf).Perfusion-weightedimaging(PWI) wasperformedshowinghypervascularityofthesolidenhancingcomponent(arrowheads),demonstratedby
superimposingthecorrectedbloodvolumemaponthesagittalnon-contrastT1Wimage(b).
Fig.3–Thirty-six-year-oldmanwithspinalcordherniation.SagittalT2WI(a)andT1WI(b)showspontaneousherniationof thespinalcordintotheanteriorepiduralspace(arrows)throughadefectinthedura.Thisisbetterdepictedonsagittal(c) andaxial(d)highresolutionT23DSPACEimagesinwhichtheduracanbeclearlyseen(arrowheadinc).
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2.7. Spectroscopyandfunctionalimaging
Spectroscopyandfunctionalimagingarecurrentlyusedonly forresearchpurposes.
3. Recommended sequences and ‘‘Tips and tricks’’ to overcome challenges in imaging of the spine
3.1. Whitematter(WM)ofthespinalcord
Whitematter(WM)islocalizedintheperipheryofthespinal cordandcontainssensoryandmotorneurons.Conventional MR imaging techniques, such as FSE T2, STIR, gradient- recalled echo T2(GRE T2), insagittal and axial planes are generallyrecommendedtodetectlesionsandtodefinetheir exactlocationandextension(Figs.1,3–5).FSET2,STIRandGE T2sequencesareusedinmultiplesclerosisandneuromyelitis optica,aswellasininfectiousandischemia.Thesesequences areusefulforlocalizationandquantificationoflesions,andto help detect vascular malformations, edema in the case of dural fistula, or the nidus in the case of arteriovenous malformation,andvitamindeficits.3Dphase-sensitiveinver- sion recovery (PSIR) is a new sequence that significantly
improvesthedetectionoflesionsinmultiplesclerosis[12].DTI showsinfiltrationanddeformationofwhitemattertractsby tumors and is useful for surgical planning as it helps to differentiatelow-andhigh-gradetumorareas.
Tips and tricks: use the axial gradient-echo in an axial planeincervicalandthoraciclocationsasthiscanavoidfirst- flux artifacts [13] and increase the signal of water. Flow artifactscanmimictumorsorprominentvessels,particularly whenposteriortothespinalcordatthethoraciclevelandin children[13].
3.2. Graymatter(GM)
Gray matter (GM) has a characteristic ‘‘H’’ or butterfly- appearance on the axial plane, which is particularly well visibleontheGEsequence.SpinalcordGMcontainsneuronal cell bodies, dendrites, axons, and nerve synapses and is surroundedbyWM.Sequencesin3Dat3TMRaffordabetter visualizationofanatomicstructures[14].
Inadvancedstagesofdegenerativecervicaldisease,spinal cord myelopathy appears due to a decreased spinalcanal diameter, inadditiontoboneanddiskmanifestations.Itis visibleonT2andSTIRasalocalizedhighsignal,isointenseon T1.However,itgenerallydoesnothaveassociatedenhance- ment, as opposed totumors or inflammatory disease and Fig.5–Forty-nine-year-oldmanwithcompressivemyelopathy.Discherniationanddegenerativefacetjointchangesatthe lowerthoraciclevelareresponsibleforcordcompressionwithsignsofmyelopathy(arrow)seenasT2WIhyperintensityof thecordinthesagittal(a)andaxial(b)images.Followingsurgicaldecompressionofthespinalcanal,thesignsof myelopathypersistwithT2WIhyperintensity(cande)andenhancementafteradministrationofGd(dandf)seenasaflat hyperintensityonsagittalT1Gd(d),whichisusuallyreferredtoasthe‘‘pancakesign’’.
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whenitisassociatedthatcangenerateamisunderstanding particularlywithtumors(Fig.5).Insomecases,thecompres- sedGMisdifficulttodistinguish.
PoliomyelitisisobservedasahighsignalonT2andSTIR.It may or may not be associated with enhancement of the anteriorhorn ofthespinal GM.Ofnote,enterovirusesand flavi-viruseshaveapredilectionforthislocation[15].Pyogenic and tuberculous abscesses are frequently associated with enhancementandtheirlocationisindistinctlyGMorWM.In the case of chronic inflammatory or degenerative disease, segmentationofdifferentcomponentsofthespinalcordto determine the volumeof its different structures isa good alternative when discussing prognosis; 3D GRE is used to performthissegmentation[16].
Tipsandtricks:donotconfusecontrast-enhancementdue tomyelopathywithatumor[17].
3.3. Vessels
Computedtomography(CT)angiographyandMRIangiogra- phy(MRA)illustratenormalvessels,suchastheAdamkiewicz artery incasesof suspicionofischemia (Fig. 2), or forthe planningofspinalsurgery[5,8,9]. MRIhastheadvantageof showingthespinalcordand potentialcomplications.High- field(3T)MRAhasaclearadvantagetoperformangio-dynamic sequences,asithasthehighspatialandtemporalresolution necessary to visualize these types of tiny structures. Fur- thermore,acorrecttimingforeachphaseiscrucialinorderto makethecorrectdiagnosis,e.g.,inspinalduralarteriovenous fistulas(dAVFs).DynamicMRAisusefultoshowdissectionsor partiallythrombosedaneurysmsofthe aorta.Forthediag- nosis of pathologies such as dAVFs and arteriovenous malformations (AVMs), morphological sequences, such as SET2,areneededtodetectvasogenicedemathattranslate intoincreasedvenouspressureindAVFs,ortoshowthenidus orbleedinginthecaseofAVMs.
Tips and tricks: multiplan reformatting and maximum intensity projection ofMRA improve the understanding of vascular pathologies.dAVFs may not be associated with swellingandedemaofthespinalcord[18].
3.4. Cerebrospinalfluid(CSF)
The rate of CSF formation in humans is approximately 0.3–
0.4ml/min(about500ml/day).ThetotalCSFvolumeis90–150ml inadultsand10–60mlinneonates[19].Threesequencesarepart ofthetechnicalclinicalprotocolthatallowsadynamicstudyof theCSF: T2 SPACE andCISS, which are heavily T2-weighed sequence, and phase-contrast MRI. The first two sequences allowdifferentiationbetweenflowartifactsandtruestructurein theCSF,e.g. synechiae,cystictumor walls,duralherniations (Fig.3),delineationofsolidtumors,andduralCSFfistulaafter surgery or trauma. The recommended plane is coronal or sagittal,asthisallowsalargerfield-of-view.Phase-contrastMRI allowsthedynamicvisualizationofCSFandclinicalapplications areChiarimalformationtype1,arachnoidwebs,andarachnoid cysts.Thesesequencesareavailableat1.5and3T.
Tipsandtricks:ECGtriggeringisindispensabletoobtaina good phase-contrastimaging since theblood and CSFflow velocitiesvaryduringthecardiaccycle.
3.5. Leptomeninges
To illustrate leptomeningeal lesions, different sequences mightbenecessary,dependingonthetypeofpathology.In the caseofasuspicionofsiderosisdue tobleedingfroma vascularlesion,aGREsequenceinsagittaloraxialplanesis recommended.However,wehavetobeawarethatsequences suchas3DT2-SPACEcanmimicasiderosis[20].If thereis asuspicionoftumordissemination,werecommendusinga contrastmediumandsequencesinfatsaturation(Fat-Sat),as thisallowsthedetectionofthinenhancements.Thissequence isalsousedinthecaseofinfectionasitpermitsdetectionof epiduralabscessesthatwouldbeverydifficulttodetectinaT1 non-Fat-Sat sequence, since enhancementand epidural fat bothhavehighsignal.
Tipsandtricks:Fat-Satsequencesaremandatorytodetect leptomeningealenhancement.
Theaxial planeismostuseful at thelevel ofthecauda equinaandenhancementofnerverootscanbeobservedas smalldots.Ingeneral,smoothenhancementsuggestsinfec- tionwhereasirregularortearshapedenhacement,suggests secondarytumororiginatthislocation.
Normalvascularstructures,particularlyveinsthatfollow theL1,L2orL3rootsofthecaudaequinaandthosethatdrain theconusmedullaris,shouldnotbeconfusedwithpatholo- gicalenhancement[13].
3.6. Nervousstructure
In addition to nerve roots and rootlets, there are larger structures, suchas the brachialand lumbosacral plexuses, that require isotropicsequences witha largerfield-of-view (Fig.6)duetotheirsizeandorientation(generallyoblique).In thiscase,weadda3DSTIRSPACEsequencetothetechnical protocol.Furthermore,weshoulddifferentiatebetweenintra- andextradurallocationwhendecidingthetechnicalprotocol.
Forintradurallocationintraumaticpathologies,theutiliza- tionofanisotropichighresolution3DT2sequenceishelpfulto detectavulsionsoftheintraduralroot,aswellasvisualization ofpseudomeningoceles[21].Intheextraduralspace,theuseof the3DT2-SPACEsequencesisrecommendedtodetecttumors (Fig.6),hematomas,partialandcompletenerveruptures,and neuromas[20,22–24].Itisnotrecommendedtoperformthe MRIstudyintheacutephaseincaseoftrauma,asitisvery difficulttodifferentiateedemafromapartialruptureofthe nerveroots,trunks,divisionsandcordsorfromahematoma [22,23].SequencessuchasDTIarehelpfultoanalyzetissue microstructureandalsointerruption(trauma),deformationor infiltration (tumors)ofthe extradural portionsof theroots trunksandcords.
Tips and tricks: MRIofthe brachialor lumbar plexuses should not be performed immediately after an injury as pseudomeningoceleswillnothavehadtimetoformandthe rate of false-negatives would increase. Furthermore, treat- mentisnotperformedintheacutephase.Inaddition,itis difficulttodifferentiatebetweenpartialrupture,edema,and hematomaintheextradurallocationinthisphase.
Itisimportanttonotethatspinalganglionsappearstrongly enhancedintheirnormalstateandshouldnotbeconfused withtumors.
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3.7. Boneanddiskstructures
Bonestructuresaremainlyaffectedbyneoplasticandinfectious pathologies.Conventionalsequences,suchasT1,T2andSTIRare essential.T1 withoutcontrasthas ahighsensitivity todetect secondarylesions.Infectiousandtumorpathologiesappearasa lowsignal onT1 anda high signalon T2and thus contrast mediumisveryusefulinbothsituations.Intumorpathologies, contrastmediumprovidesanexactextensionofdisease.Inin- fections, it shows infiltrations of the leptomeninges and abscesses. DWI helps to discriminate spondylodiscitis from degenerative MODIC type 1 signal changes. A claw signal is observedindegenerationanditsabsencesuggestsspondylodis- citis[25].Aperfusionsequencedoesnotbringanyaddedvalue.
Tipsandtricks:inthecaseofasuspectedsecondarylesion, the entire spine and not only the symptomatic segment shouldbestudied,asitiscommonthatotherregionsmaybe affectedandthuscomplicationssuchasacompressedspinal cordwouldbemultifocal.
Funding
None.
Contributors
Maria Isabel Vargas: conception and design,acquisition of data,analysisandinterpretationofdata,draftingthearticle, finalapprovaloftheversiontobesubmitted.
Jose´ Boto:acquisitionofdata,analysisandinterpretationof data,finalapprovaloftheversiontobesubmitted.
TorsteinR.Meling:draftingthearticle,revisingitcritically forimportant intellectualcontentandfinal approvalofthe versiontobesubmitted.
Disclosure of interest
Theauthorsdeclarethattheyhavenocompetinginterest.
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