63ournal of Neurology, Neurosurgery, and Psychiatry 1996;61:632-635

SHORT REPORT

Spinal cord MRI in multiple sclerosis withmulticoil arrays: a comparison between fast spinecho and fast FLAIR

Massimo Filippi, Tarek A Yousry, Hatem Alkadhi, Michael Stehling, Mark A Horsfield,Raymond Voltz

Department ofNeurology, ScientificInstitute Ospedale SanRaffaele, University ofMilan, Milan, ItalyM FilippiDepartment ofNeuroradiologyT A YousryH AlkadhiDepartment ofDiagnostic RadiologyM StehlingDepartment ofNeurology, KlinikumGrosshadern,University ofMunich,Munich, GermanyR VoltzDivision of MedicalPhysics, University ofLeicester, Leicester,UKM A HorsfieldCorrespondence to:Dr Massimo Filippi,Department of Neurology,Scientific Institute OspedaleSan Raffaele, Via Olgettina,60, 20132 Milan, Italy.Received 22 April 1996and in revised form15 July 1996Accepted 20 August 1996

AbstractObjectives-To compare the sensitivity offast spin echo (FSE) and of fast fluidattenuated inversion recovery (fastFLAIR) in detecting spinal cord lesions inmultiple sclerosis.Methods-With a 1 5 Tesla machine and amulticoil receiver array, FSE images(with two different pixel sizes) and fastFLAIR images of the spinal cord wereobtained from 13 patients with multiplesclerosis.Results-Twenty three lesions (10 cervi-cal, 12 thoracic, and one lumbar) werefound in seven patients (54%) using FSEwith the larger pixel size. Seventeenlesions (seven cervical and 10 thoracic)were detected in the same seven patientsusing FSE with smaller pixel size. Ninelesions (five cervical and four thoracic)were found using fast FLAIR in sixpatients (46%). All the lesions found usingfast FLAIR were detected using the othertwo techniques and all the lesionsdetected by FSE with smaller pixel sizewere detected using FSE and greater pixelsize.Conclusion-Fast FLAIR sequencesdetect substantially fewer cord lesions inpatients with multiple sclerosis.

(J Neurol Neurosurg Psychiatry 1996;61:632-635)

Keywords: multiple sclerosis; magnetic resonanceimaging; spinal cord; fast spin echo; fast fluid attenu-ated inversion recovery

Recent developments in MRI techniques havedramatically improved the resolution of spinalcord MRI. In multiple sclerosis, this achieve-ment is of particular interest, as the ability toimage reliably lesions within the spinal cordmay have a major impact on the understand-ing of the pathophysiology of the disease.Using a multicoil receiver array and fast spinecho (FSE) sequences, it is now possible todemonstrate spinal cord lesions in about 75%of patients with clinically definite multiplesclerosis' and to exclude other possible causesof spinal cord damage in patients who are sus-pected clinically of having the disease.2

Fluid attenuated inversion recovery(FLAIR) sequences produce heavily T2weighted images with suppression of CSF sig-nal by combining a long inversion time inver-sion recovery sequence with a long echo time.The fast FLAIR sequences have greatlyimproved the sensitivity of MRI for the detec-tion of multiple sclerosis lesions in the brain. I I

Both the number of lesions and their total vol-ume are larger in fast FLAIR images of thebrain compared with conventional spin echo.Using surface coils, FLAIR was shown to bemore sensitive than conventional spin echosequences in detecting multiple sclerosislesions in the cervical cord.67 The suppressionof the signal from the CSF was thought toimprove the sensitivity of spinal cord imagingby reducing CSF related artefacts whichpotentially mask the lesions. The time savinggiven by fast FLAIR compared with standardFLAIR makes fast FLAIR much more attrac-tive for practical applications. Similarly, it wasthought that improvements in the inplane reso-lution made possible by the FSE sequencewould also lead to an increase in sensitivity fordetecting intrinsic cord lesions.2 The use ofmulticoil arrays also allows images of thewhole spinal cord to be obtained with goodsignal to noise ratio and resolution.The aim of this study was to compare the

sensitivities of fast FLAIR and FSE with dif-ferent inplane resolutions in detecting spinalcord lesions in patients with multiple sclerosis.

Patients and methodsPATIENTSThirteen (five men and eight women) consecu-tive outpatients with clinically definite multi-ple sclerosis8 entered the study. Nine hadrelapsing-remitting and four had secondaryprogressive multiple sclerosis. The mean agewas 34 4 (SD 9-3) years, the median durationof the disease was four (range 1-14) years, andthe median expanded disability status scale(EDSS)9 was 2-0 (range 0-7 0). Patients whohad experienced an acute relapse or who hadtaken steroids during the preceding six monthswere excluded from the study. Writteninformed consent was obtained from all thepatients before inclusion.

632 on A

ugust 31, 2020 by guest. Protected by copyright.

http://jnnp.bmj.com

/J N

eurol Neurosurg P

sychiatry: first published as 10.1136/jnnp.61.6.632 on 1 Decem

ber 1996. Dow

nloaded from

Spinal cord MRI in multiple sclerosis with multicoil arrays: a comparison between fast spin echo andfast FLAIR

MRIAll MRI was were carried out using a 1-5Tesla superconducting system (Vision,Siemens, Erlangen, Germany). The receivercoil array consisted of six separate coils,although only four of the elements were active.The slice thickness was 3 mm, with a field ofview (FOV) greater than 500 mm in the supe-rior-inferior direction in all cases, enabling theentire cord to be visualised. For the fastFLAIR images, two separate acquisitions werenecessary to give enough slices to completelycover the spinal cord; these two acquisitionswere therefore performed with alternatingslices interleaved. A total of nine slices wasobtained for all the sequences used. Theimage acquisition parameters were as follows:

(1) FSE with larger pixel size: TR =3817 ms, TE = 112 ms, echo train length =15. The phase encoded direction was supe-rior-inferior with FOV = 655 x 500 (phaseencode x readout), raw data matrix =512 x 512, pixel size = 1-279 x 0-976 mm(phase encode x readout), number of signalaverages = 1, acquisition time = 2 min 13 s.This sequence incorporated gradient momentnulling (flow compensation) in the readoutand slice selection directions. The short acqui-sition time for this sequence allowed the phaseencoding to be in the superior-inferior direc-tion, thus reducing the possibility of motion

related artefacts from being superimposed onthe spinal cord. Phase encoding oversamplingwas used to remove the wrap artefact, and thefinal image was displayed with 500 x 500 mmFOV.

(2) FSE with smaller pixel size: TR =5000 ms, TE = 112 ms, echo train length =15, FOV = 500 x 500, raw data matrix size =720 x 1024, pixel size = 0-694 x 0-488 mm(phase encode x readout), number of signalaverages = 1, acquisition time = 4 min 5 s.This sequence incorporated gradient momentnulling only in the readout direction. Phaseencoding was anterior-posterior.

(3) fast FLAIR sequence: TR = 9000 ms,TE = 105 ms, TI = 2200 ms, echo trainlength = 7, FOV= 250 x 500 mm, rawdata matrix size = 210 x 512, pixel size =1 190 x 0-976 mm (phase encode x readout),number of signal averages = 1, total acquisi-tion time = 9 min 18s. This sequence had nogradient moment nulling. Phase encoding wasanterior-posterior.The TR, TE, and TI we used are similar to

those of a previous comparative study withconventional spin echo and FLAIR.6 How-ever, there were some implementational differ-ences; in particular, the fast FLAIR sequencewe used incorporated slice selective inversionpulses, whereas the FLAIR sequence used byThomas et al 6 used non-selective inversion

C D E F

Contiguous coronal slices obtained with FSE and large pixel size (A-C) and with fast FLAIR (D-F) in patient 2 (see table). In A-C many intrinsiclesions are seen both in the cervical and thoracic cord; only few of them are seen in D-F (see table forfurther details).

A B

633 on A

ugust 31, 2020 by guest. Protected by copyright.

http://jnnp.bmj.com

/J N

eurol Neurosurg P

sychiatry: first published as 10.1136/jnnp.61.6.632 on 1 Decem

ber 1996. Dow

nloaded from

Filippi, Yousry, Alkadhi, Stehling, Horsfield, Voltz

Spinal cord lesions seen on the three different scans *

Patient FSE with larger FSE with smallerno pixel size pixel size Fast FLAIR

I C2 small C2 small C2 smallC4 small

2 C4-C5 large T4-T5 large T7 smallT4-T5 large T7 small T9 smallT6 small T9 smallT7 small T9 smallT9 smallT9 small

3 T4 small T4 small no lesions4 C5 intermediate C5 intermediate C5 intermediate5 C3 small C3 small C3 small6 C3 intermediate C3 intermediate C5 small

C5 small C5 small7 C2 small C2 small C2 small

C2 small C2 small T8 intermediateC7 intermediate T4 intermediate Ti 1 intermediateT4 intermediate T6 smallT6 small T7 intermediateT7 intermediate T8 intermediateT8 intermediate T 1 1 intermediateTI 1 intermediateT12 smallLI small

*Only patients with at least one lesion in one of the three sequences are reported. See text forfurther details.

pulses with the result that CSF suppressionwas optimal only in the central slice of their 12slice data set.Two of us (MF and TAY) evaluated the

number, size, and location of lesions by con-sensus. Firstly, the fast FLAIR and the twosets of FSE sequences for all the patients wereevaluated in a random order. Next, for eachpatient, the different sequences were com-pared side by side. Only hyperintense areaswhich were considered to be lesions by boththe raters with a high degree of confidencewere counted as lesions. The site (cervical,thoracic, or lumbar with the correspondinglevels) and the extent (small: smaller than onespinal segment; intermediate: extending overone spinal segment; large: longer than onespinal segment) of each lesion were recorded.

ResultsTable 1 presents the number, location, andsize of cord lesions for each patient. Twentythree lesions were found in seven patients(54%) using FSE with the larger pixel size (fig-ure). Ten lesions were located in the cervicalcord (six small, three intermediate, and onelarge), 12 in the thoracic cord (seven small,four intermediate, and one large), and onesmall lesion in the lumbar cord. Seventeenlesions were detected in the same sevenpatients using FSE with the smaller pixel size.Seven lesions were in the cervical cord (fivesmall and two intermediate) and 10 in the tho-racic cord (five small, four intermediate, andone large). Nine lesions were found in sixpatients (46%) using fast FLAIR. Five lesionswere cervical (four small and one intermedi-ate) and four were thoracic (two small and twointermediate). All the lesions detected usingfast FLAIR were seen using the other twotechniques and all the lesions detected by FSEwith smaller pixel size were detected usingFSE and larger pixel size. In one patient, con-sidered to have no abnormalities in the cordwhen fast FLAIR was used, one small lesionlocated at T4 was detected by both the FSEsequences.

DiscussionA complete assessment of spinal cord lesionsin multiple sclerosis may have a major impacton the understanding of the pathophysiologyof the disease. It is indeed conceivable that thelesions located in the spinal cord may be mostrelevant in determining severe physical disabil-ity, thus explaining the clinical/MRI discrep-ancy found in previous studies comparingbrain MRI lesion load on T2 weighted scansand disability measured with the EDSSscore.10

Recently, new sequences (magnetisationtransfer gradient recalled echo, FSE with betterinplane resolution, and FLAIR) have beenproposed to increase further the sensitivity ofMRI in detecting intrinsic spinal cordlesions.2671' Contrary to expectations, ourstudy, which is the first carrying out a system-atic comparison between FSE and fast FLAIRusing a multicoil array in patients with multi-ple sclerosis, shows that fast FLAIR and FSEwith smaller pixel size detect fewer spinallesions compared with FSE with larger pixelsize. Whereas there were some implementa-tion differences between these threesequences, it is not thought that these couldaccount for our findings. For example, thelower resolution FSE sequence incorporatedgradient moment nulling in the readout andslice selection directions, and thus we mightexpect this to lead to more false positivelesions in the other two sequences because offlow artefacts; this was clearly not the case.The different sensitivities of the two FSEsequences might be explained by the fact thatthe better inplane resolution obtained with asmaller pixel size is offset by the poorer resul-tant signal to noise ratio. In addition, use ofmultiple echo acquisition may influence thedetection of small objects.'2 The intensity ofsmall objects and edges is enhanced in thephase encoded direction on multiechosequences with long echo times. Because thespinal cord is a narrow object, the orientationof the cord with respect to the phase encodeddirection may influence the severity of edgeartifacts. Thus when the long dimension of thecord is in the phase encoded direction (as forthe low resolution FSE images) the severity ofthe edge artefacts should be reduced. Theseartefacts may mask cord lesions when thephase encoded direction lies across the cord.On the other hand, it is perhaps more diffi-

cult to explain why the sensitivity of fastFLAIR is inferior to that of FSE. There arethree aspects of the image acquisition whichmight go some way towards accounting for thepoor performance of the fast FLAIR sequenceused here. Firstly, it is possible that a longerecho time might improve FLAIR sensitivity,although the echo time we used was similar tothat in a previous study with conventionalFLAIR.6 The optimum echo time for fastFLAIR of the cerebrum in multiple sclerosis issomewhat longer than that used by US.3 13

Secondly, as spinal cord relaxation times aredifferent from those in the brain,'4 it may bethat a shorter TI would result in better lesiondetection, even at the expense of some com-

634 on A

ugust 31, 2020 by guest. Protected by copyright.

http://jnnp.bmj.com

/J N

eurol Neurosurg P

sychiatry: first published as 10.1136/jnnp.61.6.632 on 1 Decem

ber 1996. Dow

nloaded from

Spinal cordMRI in multiple sclerosis with multicoil arrays: a comparison between fast spin echo andfast FLAIR

promise on CSF suppression.'5 Thirdly,because of the CSF suppressing properties ofthe fast FLAIR sequence, the edges of thecord are sharper, and the edge enhancementartefact noted above may be more severe,potentially further masking the internal fea-tures of the cord. It was not possible to makethe phase encoding direction superior-inferiorfor either the fast FLAIR sequence or the highresolution FSE sequence, as this would haveled to an intolerably long acquisition time.However, it might be expected that the lack ofgradient moment nulling could result in flowartefacts on the fast FLAIR images. The factthat fewer lesions were seen on fast FLAIRimages suggests that there were no "false"lesions resulting from flow artefacts. It may bethat, because of the CSF suppression in fastFLAIR, the use of flow compensation isunnecessary.

These sequence related aspects, however,are probably not enough to explain the greatlyreduced sensitivity of fast FLAIR. We know,from previous experience with the brain, thatthe sensitivity of fast FLAIR compared withconventional spin echo is variable in differentanatomical regions: fast FLAIR is much moresensitive than conventional spin echo indetecting cortical/subcortical lesions, whereasthe reverse is true for lesions located in theposterior fossa.5 It is therefore conceivable thatin CNS areas located below the tentorium, forreasons which remain unknown, multiple scle-rosis lesions may have intrinsic characteristicsdifferent from those located in the supratento-rial brain. The MRI properties of the lesionsmay therefore be very different and the pulsesequences would have to be further optimisedfor these areas. If these speculations are con-firmed by further studies, the different behav-iour of multiple sclerosis lesions whendifferent sequences are applied might lead to abetter understanding of the pathophysiology ofthe disease. On the other hand, lesions in theposterior fossa and spinal cord may, becauseof their location, play an important part in the

development of disability in multiple sclerosis.The poor sensitivity of fast FLAIR in theseareas is of serious concern if it is to be used tomonitor the natural evolution of the disease,or the effect of treatment.

This work derives in part from the collaboration made possibleby the EC funded (ERBCHRXCT 940684) EuropeanMagnetic Resonance Network in Multiple Sclerosis(MAGNIMS).

1 Kidd D, Thorpe JW, Thompson AJ, et al. Spinal cord MRIusing multi-array coils and fast spin echo. II. Findings inmultiple sclerosis. Neurology 1993;43:2632-7.

2 Thorpe JW, Kidd D, Kendall BE, et al. Spinal cord MRIusing multi-array coils and fast spin echo. I. Technicalaspects and findings in healthy adults. Neurology 1993;43:2625-31.

3 Rydberg JN, Hammond CA, Grimm RC, et al. Initial expe-rience in MR imaging of the brain with a fast fluid-atten-uated inversion-recovery pulse sequence. Radiology 1994;193: 173-80.

4 Hashemi RH, Bradley WG, Chen DY, et al. Suspectedmultiple sclerosis: MR imaging with a thin-section fastFLAIR pulse sequence. Radiology 1995;196:505-10.

5 Filippi M, Yousry T, Baratti C, et al. Quantitative assess-ment of MRI lesion load in multiple sclerosis: a compari-son of conventional spin-echo with fast-fluid-attenuatedinversion recovery. Brain 1996;119:1349-55.

6 Thomas DJ, Pennock JM, Hajnal JV, et al. Magnetic reso-nance imaging of spinal cord in multiple sclerosis byfluid-attenuated inversion recovery. Lancet 1993;341:593-4.

7 White SJ, Hajnal JV, Young IR, Bydder GM. Use of fluid-attenuated inversion-recovery pulse sequences for imag-ing the spinal cord. Magn Reson Med 1992;28:153-62.

8 Poser CM, Paty D, Scheinberg L, et al. New diagnostic cri-teria for multiple sclerosis: guidelines for research proto-cols. Ann Neurol 1983;13:227-31.

9 Kurtzke JF. Rating neurologic impairment in multiple scle-rosis: an expanded disability status scale (EDSS).Neurology 1983;33:1444-52.

10 Filippi M, Horsfield MA, Tofts PS, et al. Quantitativeassessment of MRI lesion load in monitoring the evolu-tion of multiple sclerosis. Brain 1995;118:1601-12.

11 Finelli DA, Hurst GC, Karaman BA, et al. Use of magneti-zation transfer for improved contrast on gradient-echoMR images of the cervical spine. Radiology 1994;193:165-71.

12 Constable RT, Gore JC. The loss of small objects in vari-able TE imaging: implications for FSE, RARE, and EPI.Magn Reson Imaging 1992;28:9-24.

13 Rydberg JN, Riederer SJ, Hammond CA, Jack CR.Contrast optimization in fluid attenuated inversionrecovery (FLAIR) imaging. Magn Reson Med 1995;34:868-77.

14 Ho PSP, Shivei Y, Czervionke LF, et al. MR appearance ofgray and white matter at the cervicomedullary region.AJNRAmJf Neuroradiol 1989;10: 1051-5.

15 Baratti C, Barkhof F, Hoogenraad F, Valk J. Partially satu-rated fluid attenuated inversion recovery (FLAIR)sequences in multiple sclerosis: comparison with fullyrelaxed FLAIR and conventional spin-echo. Magn ResonImaging 1995;13:513-21.

635 on A

ugust 31, 2020 by guest. Protected by copyright.

http://jnnp.bmj.com

/J N

eurol Neurosurg P

sychiatry: first published as 10.1136/jnnp.61.6.632 on 1 Decem

ber 1996. Dow

nloaded from