Spinal magnetic resonance angiography (MRA) is difficult to perform because of the size of the spinal cord vessels. High-field MR improves resolution and imaging speed. We examined 17 patients with spinal vascular diseases with dynamic contrast-enhanced three-dimensional MR sequences. In three patients, the artery of Adamkievicz could be seen; we could also detect all arteriovenous malformations and dural fistulas. MRA has the potential to replace diagnostic spinal angiography and the latter should be used only for therapeutic purpose

Kulcsár, Zolt

Lovblad, Karl

Nguyen, Duy

Rilliet, Benedict

Rufenacht, Daniel

Tessitore, Enrico

Vargas, Maria

Viallon, Magalie

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Eur Radiol (2010) 20: 2491–2495DOI 10.1007/s00330-010-1815-6 NEUROMaria Isabel VargasDuy NguyenMagalie ViallonZolt KulcsárEnrico TessitoreBenedict RillietDaniel RufenachtKarl LovbladReceived: 2 February 2010Revised: 7 April 2010Accepted: 13 April 2010Published online: 16 May 2010# European Society of Radiology 2010Dynamic MR angiography (MRA) of spinalvascular diseases at 3TAbstract Spinal magnetic resonanceangiography (MRA) is difﬁcult toperform because of the size of thespinal cord vessels. High-ﬁeld MRimproves resolution and imagingspeed. We examined 17 patients withspinal vascular diseases with dynamiccontrast-enhanced three-dimensionalMR sequences. In three patients, theartery of Adamkievicz could be seen;we could also detect all arteriovenousmalformations and dural ﬁstulas.MRA has the potential to replacediagnostic spinal angiography and thelatter should be used only for ther-apeutic purposes.Keywords DynamicMRangiography . Spinal vascularmalformations . Dural ﬁstula .Arteriovenous malformation .Adamkievickz arteryIntroductionThe small size of the structures in the spine [spinal cord10–12 mm of diameter, spinal anterior artery 0.2–0.8 mm,Adamkievicz artery (AKA) 05–1.0 mm] [1, 2] makes itdifﬁcult to perform magnetic resonance angiographic(MRA) sequences in the spinal cord . The use of a highermagnetic ﬁeld signiﬁcantly improves the quality of imageswith a reduction in acquisition time [3]. This enables highresolution images of the different vascular phases (arterial,venous and late) to be obtained that are necessary for thestudy of the normal vessels and of vascular malformationsin the spinal cord.Materials and methodsWe have examined 17 patients (for details see Table 1),eight female and nine male, aged 26–82 years, median age52 years on a 3-Tesla MR system (Trio, Siemens,Forchheim, Germany); the patients were referred betweenJanuary 2006 and October 2008 to the Department ofNeuroradiology, Geneva University Hospital, with knownspinal problems. The patients underwent the followingimaging procedures after having been informed andaccording to our institutions guidelines. The protocol usedwas composed of sagittal T2-weighted imaging (T2WI)(TE 120, TR 3,500, 4-mm thickness, nine slices) and axialT2WI (TE 120, TR 4,000, 4-mm thickness, 20 slices),sagittal T1WI (TE 13, TR 626, 4-mm thickness, nineslices), diffusion tensor imaging (DTI) with 30 directions,three-dimensional (3D) MRA sequences (see detailsbelow) and fat-saturated T1WI in the sagittal (TE 12, TR400, 4-mm thickness, nine slices) and axial (TE 12, TR400, 4-mm thickness, 20 slices) planes after administra-tion of contrast.Three MRA acquisitions based on a 3D contrastenhanced gradient echo sequence were sequentiallyperformed (Fig. 1) after a bolus injection of an intra-vascular contrast agent (0.2 mmol/kg, Vasovist; BayerSchering, Berlin, Germany). The sequence was fatsaturated and therefore it was not centrically reordered.A test bolus was then performed in order to determine theM. I. Vargas ()) :D. Nguyen :K. LovbladDepartment of Neuroradiology, DISIM,Geneva University Hospital,4 Gabrielle-Perret-Gentil, 1211, Genève 14,Switzerlande-mail: maria.i.vargas@hcuge.chTel.: +41-22-3723775Fax: +41-22-3727072M. ViallonDepartment of Radiology,Geneva University Hospital, Geneva,SwitzerlandE. Tessitore :B. RillietDepartment of Neurosurgery,Geneva University Hospital, Geneva,SwitzerlandZ. Kulcsár · D. RufenachtKlinik Hirslanden, Neurozentrum,Zurich, Switzerlandarrival time of the contrast agent in the arteries feeding thespinal cord, and the acquisition was started adequately sothat the acquisition of the k-space centre matched thebolus arrival time. For the arterial and venous 3D gradientecho MR sequence, the parameters were TE/TR/ﬂip angle=1.52 ms/3.98 ms/20°, a matrix size of 384, pixel size=1.2×1.0×0.9 mm, ﬁeld of view (FOV)=380 mm, norectangular FOV, 88 slices, 0.9-mm slice thickness,bandwidth (BW)=410 Hz/px. The phase encoding direc-tion was chosen in the cranio-caudal direction to avoidﬂow and motion artefacts from the ascending hyperintenseaorta projecting on the spinal cord, with an additional 33%oversampling. The sequence was acquired at the isocentreand required 1 min for a single phase.For the high resolution late enhanced 3D gradient echoMR sequence, the parameters were TE/TR/ﬂip angle=1.89 ms/4.95 ms/20°, two averages, a matrix size of 512,pixel size=0.7×0.6×0.6 mm, FOV=330 mm, no rectan-gular FOV, 72 slices, 0.6 mm slice thickness, BW=410 Hz/px. The sequence was also performed systemati-cally at the isocentre. MPR reformatting and thin MIPreconstructions were realized for all acquisitions.All cases, with the exception of AKA localization andpatients with ischemic lesions, had a conventionalangiography. The tumours were proven by histology.ResultsIn all patients the main spinal vessels were seen andabnormal vascular lesions were visualized (see Table 1).In two out of three patients examined for localization ofthe AKA, the visualization was easily done (Fig. 2),whereas in the third patient differentiation between arteryand vein was more difﬁcult, but possible by performingmaximum intensity projection (MIP) and multiplanarreconstruction (MPR).In four cases of dural ﬁstula the exact localization ofthe ﬁstula was possible (Fig. 3).In three cases with AVM, the level of malformation andthe intra- and perimedullary localization was done as wellas the arteries implicated (Fig. 4). The little shunts insidethe nidus could not be individualized.Cavernomas are not seen on MRA and on conventionalangiography; therefore, the realization of angiographicsequences is not necessary. In tumours such as hemangio-mas or hemangioblastomas, hypervascularization wasdetected in addition to morphology and location of themasses.In ischaemia [4], the parenchymal anomalies werevisible early on diffusion imaging but unfortunately theimplicated vessel was not detectable by MRA.Table 1 Patient imaging ﬁndings (AKA Adamkievicz artery, AVM arteriovenous malformation)Sex Age Symptoms MRA ﬁndings MRI ﬁndingsM 50 Transient recurrentparaparesiesLocalization AKA NoneF 30 Back pain Localization AKA Extradural cystF 75 Back pain Localization AKA Metastasis from colon carcinoma Th11–Th12M 58 Progressive paraplegia Dural ﬁstula Th6 left Hyperintensity Th5 of the spinal cord and dilatation ofperimedullary vesselsM 57 Progressive paraplegia Dural ﬁstula Th9 right Hyperintensity in the whole spinal cord associated withdilated perimedullary vesselsM 80 Progressive paraplegia andback painDural ﬁstula Th11 left Hyperintensity in the dorsal segment and medullary coneassociated a with dilated perimedullary vesselsF 70 Progressive paraplegia Dural ﬁstula Th6 left Hyperintensity in the medullary cone with enhancement andslight dilatation of perimedullary vesselsF 26 Dysesthesia left superiorextremity and motor deﬁcitof the left legCervical AVM Dilated vessel and nidus in perimedullary right spaceassociated with bone erosionM 29 Motor deﬁcit and spasticityof right inferior extremityAVM Th4–Th6 Flow-voids in the spinal cord and dilated perimedullaryvesselsM 50 Neck pain and paresthesiasof both superiorextremitiesAVM C1–C3 Flow-voids in the spinal cord and dilated perimedullaryvesselsF 41 Back pain and suddenparaplegiaNone Spinal cord cavernomaM 57 Paresthesia of two lowerextremitiesDilated vessels inside themassEpidural heterogeneous mass (hemangioma) at Th3–Th5with ﬂow voids inside and medullary compressionF 38 Paraparesis, constipation andbladder dysfunctionDilated vessel around themasses and in theperimedullary spaceMultiple hypervascular heterogeneous masses associatedmedullary compression and intramedullary hyperintensity(hemangioblastomas)M 52 Sudden tetraplegia None Cervical spinal cord ischemiaF 82 Sudden paraplegia andbowel/bladder dysfunctionNone Medullary cone ischemiaF 60 Sudden paraplegia andbowel/bladder dysfunctionNone Medullary cone ischemiaM 73 Sudden paraplegia andbowel/bladder dysfunctionNone Medullary cone ischemia2492DiscussionThe main advantage of spinal MRA is a better imagequality and resolution, which improves the visualizationof small-size vessels. The utilization of high vascularremanence contrast agent permits visualization of thearterial and venous phases as well as to obtain high-resolution late enhanced 3D gradient echo MR images.Currently we could detect both the normal arteries (i.e.the AKA, Fig. 2) and the abnormal vessels as in the priorstudies realized at 1.5 Tesla [5, 6]. While the “goldstandard” for the evaluation of spinal vessels is conven-tional angiography, this procedure is still accompanied byrisks and requires experience to perform. Dynamic MRAavoids an unnecessary angiography with superselectiveinjections at numerous levels in the case, for example,Fig. 1 A 29-year-old man with AVM: dynamic MRA, arterial-phase (a), venous-phase (b) and high-resolution images (c) with 3Dreconstructions (d)Fig. 2 A 30-year-old woman: the MRA shows clearly an AKA(arrows, a) passing over the cyst (asterisk, a, b)Fig. 3 A 57-year-old man with a dural ﬁstula at the level of Th9right illustrated by MRA (a) and angiography (b)2493where a dural ﬁstula (Fig. 3) or an AVM (Fig. 4) aresuspected [7–9]. Usually in our hospital, only the over-lying and underlying segments are catheterized for thestudy of eventual feeder arteries. Krings [10] recommen-ded the utilization of sequences such as CISS 3D orFIESTA, but the problem with these sequences is thatdifferentiation between the veins and the arteries is notpossible. When the localization of AKAs is necessary forthe surgery of tumours or in the case of aortic aneurysm[11, 12] we avoid the risk of plaque embolization by notperforming conventional angiography.The real advantage of 3D dynamic vascular sequencesis the capacity to non-invasively evaluate the shuntlocation which is extremely helpful to guide invasiveconventional angiography [2]. Bowen and Kochan [13]described in 1995 that spinal contrast-enhanced MRA hasgreatly contributed to localizing these lesions and helpingto avoid unnecessary multiple superselective injections;the drawback of the technique used by this author is thenon-utilization of the dynamic phase component essentialfor the classiﬁcation and subsequent treatment of thevascular malformations.Recent technical improvements in contrast-enhancedMRA ,such as the use of SENSE or other parallel imagingtechniques at 3 T, have allowed to greatly accelerateimaging, thus obtaining both a high spatial and temporalresolution [7, 9]; this can help to better depict feedingarteries as well as anatomy and ﬂow velocity of earlyvenous drainage, thus allowing improved classiﬁcation ofvascular malformations. Also, due to the high resolutionof the technique, in the case with a very small structuresuch as a spinal cord cavernoma, the combination of MRand MRA allowed to help exclude another kind ofvascular malformation.Finally MIP and MPR reconstructions are crucial forthe detection and analysis of the vascular malformation;for this purpose it is necessary for the physician to betrained in this kind of reconstruction.ConclusionCurrently, MRA can provide the exact localization of avascular malformation and AKA, and thus help detect andcharacterize spinal vascular lesions before conventionalangiography for the diagnosis, thus avoiding an unneces-sary intervention and decreasing the risk of embolism ordissections. Standard angiography should be used only fortherapeutic purposes.References1. Lazorthes G (1983) Le systéme nerveuxcentral, 3 edn. Masson, Paris, p 352. Backes W, Nijenhuis R (2008)Advances in spinal cord MRangiography. AJNR Am J Neuroradiol29:619–6313. Vargas MI, Delavelle J, Kohler R,Becker C, Lovblad K (2009) Brain andspine MRI artifacts at 3Tesla. JNeuroradiol 2:74–814. Vargas MI, Delavelle J, Jlassi H et al(2008) Clinical applications of diffusiontensor tractography of the spinal cord.Neuroradiology 50:25–295. Mull M, Nijenhuis R, Backes W, KringsT, Wilmink J, Thron A (2007) Valueand limitations of contrast-enhancedMR angiography in spinal arteriovenousmalformations and dural arteriovenousﬁstulas. AJNR Am J Neuroradiol7:1249–1258Fig. 4 A 26-year-old womanwith a cervical AVM: theMRA (a) showing the feeder,nicely demonstrated in the3D reconstruction (b),corresponding to what isseen on DSA (c)24946. Hyodoh H, Shirase R, Kawaharada N etal (2009) MR angiography for detectingthe artery of Adamkiewicz and itsbranching level from the aorta. MagnReson Med Sci 8:159–1647. Petkova M, Gauvrit J, Trystram D et al(2009) Three-dimensional dynamictime-resolved contrast-enhanced MRAusing parallel imaging and a variablerate k-space sampling strategy inintracranial arteriovenousmalformations. J Magn Reson Imaging29:7–128. Parmar H, Ivancevic M, Dudek N,Gandhi D, Mukherji S (2009) DynamicMRA with four-dimensional time-resolved angiography using keyhole at3 Tesla in head and neck vascularlesions. J Neuroophthalmol 29:119–1279. Willinek W, Hadizadeh D, VonFalkenhausen M et al (2008) 4D time-resolved MR angiography with keyhole(4D-TRAK): more than 60 timesaccelerated MRA using a combinationof CENTRA, keyhole, and SENSE at3.0 T. J Magn Reson Imaging 27:1455–146010. Krings T, Geibprasert S (2009) Spinaldural arteriovenous ﬁstulas. AJNR Am JNeuroradiol 4:639–64811. Nijenhuis RJ, Leiner T, Cornips EM etal (2004) Spinal cord feeding arteries atMR angiography for thoracoscopicspinal surgery: feasibility study andimplications for surgical approach.Radiology 2:541–54712. Kunihiro Y, Hiroyuki N, Atsushi O et al(2003) MR angiography and CTangiography of the artery ofAdamkiewicz: noninvasive preoperativeassessment of thoracoabdominal aorticaneurysm. Radiographics 23:1215–122513. Bowen B, Fraser K, Kochan J (1995)Spinal dural arteriovenous ﬁstulas:evaluation with MR angiography. AJNRAm J Neuroradiol 16:2029–20432495

Dynamic MR angiography (MRA) of spinal vascular diseases at 3T

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