AINR Am I Neuroradiol 23:393-399, March 2002

Influence of Imaging Parameters onHigh-Intensity Cerebrospinal Fluid Artifacts in

Fast-FLAIR MR Imaging

Hsiu-Mei Wu, David M. Yousem, Hsiao-Wen Chung, Wan-Yuo Guo, Cheng-Yen Chang, andChene-Yu Chen

BACKGROAND AND PURPOSE; High-intensity CSF artifacts at the basal cisterns on MRimages are often seen when a fast fluid-attenuated inversion recovery (FLAIR) technique isused. We investigated the influences of four optional fast-FLAIR sequence parameters on the

high-intensity CSF artifacts.METHODS: A total of 377 patients (age range, 1 week to 91 years; mean 40.6 years; 186

female, 191 male) were examined with axial fast-FLAIR images obtained (TRyTE"rflI, 8800/13312200) with a 1.5-T system during 6 months. The effects of the optional addition of inferior

inflow saturation (thickness, 80 mm), section flow compensation, and tailored radiofrequency(TRF) pulses, plus the choice of interleaving acquisition factors of 2 or 3, were evaluated for thepresence of high-intensity CSF artifacts on the fast-FI"AIR images. Two radiologists indepen'dently reviewed the fast-FLAIR images in 76 patientsl afterward, a single observer reviewed theremainder of the images.

RESULTS: The interobserver agreement rate in 76 cases was more than907o. The use of TRFand/or three interleaving acquisitions resulted in a substantial _reduction in the incidence ofhigh-intensity CSF artifacts from about 80Vo to 40Vo (P < .05, two'-sample two'sided Z tesJ).

Inferior inflow saturation and section flow compensation did not signi{icantly improve imagequality (P > .05). The results were consistent with the image quality ranking obtained in five

healthy volunteers.CONCLUSION: The appropriate choice of sequence parameters in fast-FLAIR imaging

reduces the incidence of high-intensity CSF artifacts that are frequently encountered in thepresence of rapid CSF flow.

The advent of fluid-attenuated inversion recovery(FI-A.IR) imaging has improved the detection of in-traparenchymal abnormalities in the brain by high-lighting hyperintense lesions opposite the low-signal-intensity CSF (1-3). Because of the conspicuous

Received July 10, 2001; accepted after revision November 6.From the Department of Radiology (H.M.W., D.M.Y.), Johns

Hopkins University, Baltimore, MD; the Department of Radiology(H.-M.W., W.-Y.G., C.-Y. Chang), Veterans General Hospital-Taipei, Taiwan, ROC; the Department of Radiology (H'-M.W.,W.-Y.G., C,-Y. Chang.), School of Medicine, National Yang-MingUniversity, Taipei, Taiwan, ROC; the Department of ElectricalEngineering (H.-W.C.), National Taiwan University, Taipei, Tai-wan, ROC; the Department of Radiology (H.-W.C, C.-Y. Chen.),Tri-Service General Hospital, Nei-Hu, Taipei, Taiwan, ROC.

H.-M.W. received support from Tjing-Ling Neurological Foun-dation. H.-W.C. received support from the National Science Coun-cil, grant NSC90-2320-8002-043-M08.

Address reprint requests to Hsui-Mei Wu, MD, Department ofRadiolog5r, Veterans General Hospital-Taipei, No. 201, Section 2,Shih-Pai Road, Taipei, Taiwan 112, ROC.

@ American Society of Neuroradiology

lesion contrast, the FLAIR sequence has become astaple in the evaluation of intracranial pathologicconditions (a-\.In particular, the incorporation offast spin-echo imaging to FLAIR imaging, the so-called fast-FLAIR technique (8, 9), has made the useof this method feasible in clinical practice because ofa substantial reduction in the imaging time. Findingsfrom recent studies suggest that the fast-FI-AIR im-ages can be used to detect diseases within the sub-arachnoid space, such as subarachnoid hemorrhage(5, 10), meningitis (7, 9), and subarachnoid seeding ofneoplasms (7). Consequently, an integrated MR ex-amination including FLAIR and MR angiographywould be helpful for the examination of patients withpossible subarachnoid hemorrhage, as well as differ-ent types of aneurysms.

Despite the relative success of the fastFLAIRtechnique in lesion detection within the convexity ofthe subarachnoid space, CSF suppression with fast-FLAIR at the basal cisterns is less successful. Arti-factual high signal intensity can often be found in the

394 WU AJNR: 23. March 2002

TABLE 1: Incidence of high-intensity CSF artifacts at the basal cisterns in image groups classified according to combinations of pulse sequenceparameters

Parameters*Mean Patient

Aee (y)No. of

PatientsNo. with High-Intensity CSF

Artifacts at the Basal Cisterns Incidence (Vo)

+FC/+TRF/2/-I sat+FC/+TRF/2/+I sat-FC/-TRF/2/+I sat-FC/-TRF/2/-I sat_FC/*.rRF/3/+I sat-FC/+TRF/2/+I sat+FC/-TRF/U-I sat

AL.J

43.647.438.235.644.837.4

8439

104)z

482743

361872262212JZ

42.946.269.281.345.844.474.4

* +FC indicates with FC along section direction; -FC, without FC; +I sat, with inferior inflow saturation; -I sat, without inferior inflowsaturation; +TRF, with TRF pulses; -TRF, without TRF pulses; and 2 or 3, the interleaving acquisition factor.

prepontine and perimesencephalic regions (3, 8, 11),and the diagnosis of focal subarachnoid hemorrhageat these locations becomes difficult, if not impossible.Therefore, the purpose of this study was to investigatethe effects of various imaging parameters on fast-FLAIR high-intensity CSF artifacts at the basal cis-terns. The incidence of high-intensity CSF artifactsfor each set of sequence parameter combinations wasalso determined.

MethodsA total of 377 individuals (age range, one week to 91 years;

186 females with a mean age of 40 years, 191 males with a meanage of.4L years) were examined with a 1.5-T MR system duringa 6-month period. We excluded patients who had undergoneintracranial surgery within 6 months prior to the date of theimaging examination to eliminate the influence of meningealpathologic conditions on the evaluation of fast-FLAIR perfor-mance. In addition, all patient records were reviewed to ensurethat, if lumbar punctures were performed, the findings werenormal.

Axial fast-FLAIR images were acquired by using a standardquadrature head coil'with the following imaging parameters:TRyTE,rrlTI of 8800113312200, readout bandwidth 16 kHz, oneNEX, 192 x 256 matrix, 22 x 22 or 24 x 24-cm field of view,and 5-mm section thickness with interleaved imaees (two ac-quisitions). All images were reconstructed by uring'u ,.ro-filling interpolation process to a display matrix of 5t2 x 5l2toenhance the apparent image resolution. Four pulse sequenceparameters that were thought to potentially affect the extent ofhigh-intensity CSF artifacts on fast-FLAIR images were varied,and their effects on the imaging appearance was investigated.The changes included the optional addition ofthe following; 1)inferior inflow saturation with a thickness of 80 mm, whichcould potentially suppress signals from through-plane inflow ofCSF; 2) flow compensation (FC) along the section direction,which was thought to affect the degree of intravoxel phasedispersion due to CSF motion in the presence of imaginggradients; 3) tailored radiofrequency (TRF) pulses in an echo-amplitude stabilization scheme with flip-angle adjustment in afast spin-echo sequence (12); and 4) an interleaving acquisitionfactor of 2 (manufacturer's default) or 3. Here, the inteileavingacquisition factor specifically repiesented the number of imlage-acquisition passages for whole-brain coverage. For exam-ple, by choosing an interleaving acquisition factor of 3, imagingwas divided into three steps; during each, mutually adjacentimages were acquired with a section gap of twice the sLctionthickness. The theoretical basis of the above four parametersrelated to high-intensity CSF artifacts are further addressed inthe Discussion.

. These parameters were changed on a weekly basis duringthe 6-month period to achieve sufficient statisiical power to

evaluate the parameter effects. Note that we did not change allof the parameters in any single patient; instead, we chose toevaluate a cohort of patients with each set of parameter com-binations. In addition, not all combinations of the four param-eters were investigated for two reasons: First, because of theimaging time, the interleaving factor of 3 was not the preferredchoice. Thus, we did not specifically use the interleaving factorof 3 with all possible combinations of the other parameters.Second, some parameters that were found during the investi-gation to minimally affect the incidence of high-intensity CSFartifacts were subsequently fixed in later cases. Therefore, thetotal number of combinations investigated in this study wasseven (Table 1). Also, the effect of cardiac gating on high-intensity CSF artifacts was not investigated, for reasons statedin the Discussion.

The fast-FLAIR images were evaluated for the presence ofhigh-intensity CSF artifacts in the subarachnoid space, espe-cially the prepontine and perimesencephalic cisterns. The pres-ence of high-intensity artifacts was defined as CSF with signalintensity higher than that ofgray matter, either focally or difftrsely.Although sagittal Tl-weighted, axial fast spin-echo T2-weighted,axial Tl-weighted, and contrast-enhanced axial Tl-weighted im-ages were acquired in most patients, these images were not rou-tinely reviewed during the evaluation for fast-F[,AIR artifacts.Two neuroradiologists (H.-M.W., D.M.Y.) initially interpretedthe fast-FLAIR images to evaluate the interobserver variabilityin the analysis of high-intensity CSF artifacts in the perimes-encephalic and prepontine regions. After the initial evaluationof the images in 76 patients, for which the agreement rate wasgteater than 90Vo (the interobserver agreement regarding thepresence of high signal intensity in the basal cistems was 937o),a single observer (H,-M.W.) reviewed the remaining images.The results obtained after the completion of all case reviewswere subsequently divided into groups according to the com-binations of the four sequence parameters being investigated.The statistical significance of differences in artifact incidencesbetween the groups was assessed by using two-sample two-sided Z test.

In addition to the patient examinations, fast-FI-AIR imagingwith different combinations of pulse sequence parameters wasperformed in five healthy volunteers for an evaluation of imageappearances in a subject-independent manner. In this part ofthe investigation, two neuroradiologists (H.-M,W., D.M.Y.)independently reviewed and ranked the presence of high-in-tensity CSF artifacts at the basal cisterns. Each neuroradiolo-gist were blinded the pulse sequence parameters and the resultsof the other neuroradiologist. A final ranking of image qualityfor each subject was reached by consensus.

ResultsOf the 377 patients whose images were reviewed,

meningeal disease was suspected in none. Accordingto the chosen pulse sequence parameters, the images

AJNR: 23.March2002 CEREBROSPINAL FLUID ARTIFACTS Jy)

TABLE 2; Comparison of the incidence of high-intensity CSF artifacts at the basal cisterns between groups

Comparison of Parameters Changed*ParametersMaintained* Z Yahte P Value

SignificantDifference

NoNoYesNoNoYesYesYesYesNo

* *FC indicates with FC along section direction; -FC, without FC; +I sat, with inferior inflow saturation; -I sat, without inferior inflowsaturation; +TRF, with TRF pulses; -TRF, without TRF pulses; and 2 or 3, the interleaving acquisition factor.

TABLE 3: Ranking of irnage quality in five bealthy volunteers*

Rankf Volunteer 1 Volunteer 2 Volunteer 3 Volunteer 4 Volunteer 5

+I sat vs -I sat+I sat vs -I sat2 v s 3+FC vs -FC

+FC vs -FC

+TRF vs -TRF

+TRF vs -TRF+FC/+TRF vs -FC/-TRF

+FCI+TRF vs -FC/-TRF

+FC/+TRF/2/-I sat vs -FC/-TRF/31+I sat

+FC/+TRF/2_FC/-TRF/2-FC/-TRF/+I sat+TRF/2/+I sat-TRF/2/-I sat+FC/21-I sat-FCD/+| satA+I sat2l-l satNone

0.1481.1092.58J.

-0.114

0.4203.1,872.1.68? ? { 1

3.5300.148

.882

.268

.010

.909

. b / )

.001

.030

.019<.001

.882

2

I

)o'7

8

FC/TRF/3TRF/2FC/TRF/2FC/l sat/TRF/2FC,{-S sat/TRF/2None/2FCI2NA

FC/TRF/3FC,{-S sat[RF/2FC/I sat[RF/2FC/TRF/2TRF/2FCI2NANA

FC/TRF13FCIIsatlTRI.l2FC/TRF/2FCA-S sat/TRF/2TRF/2None/2FCNNA

FqTRF/3TF'.F12FC/I-S sat/TRF/2FCA sat/TRF/2FC/TRF/2None/2FCI2NA

FC/TRF/3T!'.F12FC/TRF/2FCA sat/TRF/2FC/I-S saVTRF/2None/2FC2I-S sat/2

* FC indicates FC along section direction; I-S sat, with both inferior and superior inflow saturation; NA, not applicable; and 2 or 3, the intetleavingacquisition factor.

t 1 indicates the least high-intensity CSF artifacts.

were divided into seven groups. Statistical analysisshowed that the groups did not significantly differ inage and sex distribution. The incidences of high-in-tensity CSF artifacts at the basal cisterns in all groupsare shown,in Table 1. Note that the high-intensityCSF artifacts occurred with rates sreater {han 40Vo inall groups. With inappropriate c-hoices of pulse se-quence parameters (eg, no TRF, no FC, two acquisitions), however, the incidence ofartifacts increased toaboutS0Vo. The fast-FLAIR imases obtained withoutthe TRF option seemed to yield i trigh". incidence ofartifacts, unless an interleaving acquisition factor of 3was used. Such consequences are evident in Table 2,which shows the statistical differences of artifact in-cidence between groups, as assessed by using the Ztest. As Table 2 shows, the use of inferior inflowsaturation and/or section flow compensation did notaffect the incidence of high-intensity CSF artifacts.The use of TRF or an interleaving acquisition of 3significantly reduced the high-intensity CSF artifactsat the basal cisterns. The presence of artifacts onimages acquired with an interleaving acquisitionfactor of 3 without TRF pulses was not significantlydifferent from those on images obtained by using aninterleaving acquisition factor of 2 with the TRF option.

Results from the five volunteers demonstrated thatthe fast-FLAIR images obtained with section FC,TRF, and an interleaving acquisition factor of 3 con-sistently had the best image quality with the leasthigh-intensiry CSF artifacts at the basal cisterns (Ta-

ble 3). The images acquired with TRF pulses and aninterleaving acquisition factor of 2 were ranked asbeing slightly inferior to those obtained with TRFpulses and three interleaving acquisitions. Note thatall fast-FI-AIR imaging acquired with a TRF pulseand an interleaving acquisition factor of 2 were sim-ilar, even with different combinations of section FC,inferior inflow saturation, and/or supedor inflow sat-uration (Fig 1). Hence, the rankings for these se-quence parameter combinations were more or lesSinterchangeable. Imaging without the TRF optionalways result in the worst high-intensity CSF artifacts.

DiscussionImaging of the brain with the fast-Fl,AIR tech-

nique provides a unique advantage of high sensitivityto hemorrhage in the subarachnoid space (5,7,l0).The existence of plasma protein shortens the T1 ofthe subarachnoid fluid (13); this leads to high signalintensity on the fast-Fl,AIR images of the hemor-rhagic lesions opposing the low-signal CSF (3, 5,7,10). Consequently, previous groups have found thatfast-FI-AIR imaging is superior to CT scanning (5,10), proton-density-weighted imaging, and T2-weighted imaging (8, 14) in demonstrating subarach-noid hemorrhage, particularly with subacute sub-arachnoid hemorrhage (15). In the presence of CSFmotion, however, inflow of noninverted (and hencenon-nullified) CSF into the imaging section is likely to

396 WU AJNR: 23,March2002

Fte 1. Comparison of images parameters in terms of high-intensity CSF artifacts on fast-FLAIR images obtained in a 37-year-oldhealthy male volunteer (volunteer 5).

. A' lmage obtained with section FC, TRF, and interleaving acquisition factor of 3 shows better CSF nulling at prepontine cistem (arrow)than the images in B or C. Notably, in pulse sequences with better CSF nulling at prepontine cistern, fewdr hign-intensity CSf artitact6are present at the aqueducl (anowhead).

B, lmage obtained with FC, TRF, and an interleaving acquisition factor of 2.C, lmage obtained with only TRF.D' Additional superior and inferior presaturation doe_s no! decrease the high-intensity CSF artifacts (see image in B)..E andiimages obtained with FC alone without TRI-(9 or with superioi and inferior presaturations (saturition bands of g0 mm)

without TRF (D demonstrate substantial high-intensity CSF artifacts at the prepontine cisiern.

occur during the 2-second TI, particularly at places the flow-related high-intensity CSF artifacts fre-wiere fast pulsatile flows are present (3, 11). Such a quently encountered-at the basal cisterns.phenomenon manifests.as high-intensity CSF artifacts

' Of ihe four optional sequence parameters investi-

on fast-FLAIR images (1, 8), causing nonspecificity in gated in this study, inflow iaturation and section FChemorrhage detection and, possibly, motion. ghosts did not significanily affect the incidence of high-in-that h^amper accurate image interpretatiol (:, tO). tensity CS"F artifacis. tn principte, the application ofTherefore, in addition to an optimiiation of standard inflow saturation presaiurate's ihe magnetizationim.aging parameters such as the TR,.TI, TE_(17), and from upstream flow'(usually in major btoJd vessels),^e..c^!o lrain ]"nq,,h, (18) toward effective CSF iuppres- thereby eliminating iignats'from ihe through-planeslon, one should be cognizant of the various optional flowing fluid. For CSp at the basal cisterns, fr'o*"v"t,sequence parameters that can be chosen to eradicate the flow is generally bidirectional (ie, to and fro), and

AJNR: 23,March2002

RF

G(slice)

AI st spin echo 2nd spin echo

H F

G(slice)

Bstimulated echo

Fta 2. Schematic diagrams of the fast spin-echo sequenceshow the effects of section selection gradients on the formationof spin echoes and stimulated echoes.

A, Diagram shows the spin echoes produced with RF excita-tion by the 90' pulse and refocusing by the B pulses. At evenechoes, the section selection gradient shows a 1-(-2)-1 wave-form (dotted-dashed-dotted areas, respectively). Hence, thespin echoes are have inherent motion compensation at evenechoes.

B, Diagram shows stimulated echo formation from RF excita-tion by the 90" pulse and refocusing by the composite of twosuccessive B pulses. For stimulated echoes, the magnetizationvector is stored in the longitudinal direction in between the twoB pulses and, thus, the gradient has no effect on the phase distri-bution. The resultant 1-(-1) waveform (dotted-dashed areas, re-spectively) shows no inherent motion compensation. Note that,with flip angle reduction of the B pulses, as with the selection of theTRF pulse, the signals have a decreased contribution from the spinecho and increases the stimulated echo portion. Therefore, thenoncompensated stimulated echo reduces the high-intensity CSFartifacts due to rapid inflow of CSF in the prepontine cistems.

the velocity is much lower (on the order of 5-L0 cm/s)than that in the major blood vessels. The effectivenessof inflow saturation to reduce high-intensity CSF ar-tifacts, therefore, is anticipated to be limifed, asshown in Tables 2 and 3.

Similar to inflow saturation, the results from thisstudy indicate that section FC did not significantlyinfluence the quality of fast-FI-AIR images. One pos-sible reason is that the signals in fast spin-echo se-quences are inherently motion-compensated at evenechoes along the section direction (19) (Fig 2A),hence yielding no discernible difference with furtheraddition of the through-plane FC gradients. The in-effectiveness of additional section FC in fast spin-echo sequences is expected to be especially promi-nent when the flow is slow and does not contain asubstantial portion of higher-order flow acceleration,as in the case of CSF motion. Also note that, althoughfindings in the volunteer study showed that fast-FI-AIR images obtained with section FC, TRF, andthree interleaving acquisitions had the best imagequality, FC is not thought to play an essential role inreducing the artifacts because of two reasons: First,because of the imaging time, we did not performimaging in the volunteers by using TRF pulses and

CEREBROSPINAL FLUID ARTIFACTS 397

three interleaving acquisitions without FC (Table 3)for a comprehensive comparison. Second, as havealready been stated, results from the patient studysuggested that FC did not significantly alter the inci-dence of high-intensity CSF artifacts.

The reason why TRF helped to suppress non-nul-lified CSF signals is anticipated to be associated withthe formation of stimulated echoes in fast spin-echosequences. To appreciate this point, note first thattwo major components contribute to the receivedsignals in fast spin-echo sequences: spin echoes andstimulated echoes (Fig 2). In contrast to spin echothat arises from one excitation RF pulse followed byone refocusing pulse, the stimulated echo is formedby three consecutive RF pulses: The first one servesas the excitation pulse, whereas the latter two serve asa composite refocusing pulses. Along the section-selection direction, the spin echoes are inherentlymotion compensated at even echoes (Fig 2A) (19),whereas the stimulated echoes are not (Fig 2B). Thisis because the gradient e4perienced by the magneti-zation vector exhibits a l-(-2)-I waveform (ie, thegradient waveform for FC) at even spin echoes (20).On the other hand, the stimulated echoes experienceonly a 1-(-1) waveform (similar to that of commongradient-echo imaging); hence, they are not motioncompensated (Fig 2B). Consequently, for through-plane flow, strong signals are expected for the spinechoes, whereas the stimulated echoes experienceintravoxel phase dispersion leading to signal loss (21).The TRF technique is a method that was originallydeveloped to stabilize fast spin-echo signal ampli-tudes (12), including those in fast-Fl,AIR. The designinvolves varying the flip angles of the first two refo-cusing pulses, along with a flip-angle reduction for theremaining ones. Compared with standard fast spin-echo with 180o refocusing pulses, the reduction of theflip angle in the TRF method decreases the spin-echocontribution to the signals and concomitantly in-creases the stimulated echo portion (22). In otherwords, selection of the TRF option in the fast-FLAIRsequence had the effect of increasing the stimulatedecho, whereas no significant visible change occurred onT2-weighted image. Because the high-intensity CSF ar-tifacts at the basal cisterns on fast-F[,AIR images comepredominantly from the through-plane motion thatcauses non-nullified CSF, these artifactual signals areoptimally be dephased with the use of the noncompen-sated stimulated echoes. The results from this studysuggest that the selection of TRF in fast-FI-A,IR imag-ing had the effect of increased stimulated-echo compo-nents, which achieved effective CSF suppression. Onefurther note is that the TRF mentioned in this studyrefers to the echo amplitude stabilization scheme pro-posed by Le Roux and Hinks (12), and it should not beconfused with the same terminology used to describedRF pulseswith a quadraticphase distributionwithin theselected section (23).

Another effective method to prevent inflow of non-inverted CSF into the image section is to increase thethickness of the inversion pulse. This change can beaccompanied by an increased intersection gap to min-

imize possible "cross-talking" befween adjacent inver-sion pulses. When the intersection gap is not desir-able, the image acquisition must be interleaved, at thepenalty of a longer imaging time. For contiguoussections with an interleaving acquisition factor of N,the thickness of the inversion pulse can be increasedto approximately N times the image section; this isexactly the recommendation of the manufacturer ofthe MR system that was used in this study. The in-crease in the inversion section thickness thus accountsfor the better CSF suppression at the basal cisternsnoted in this studywhen we increased the interleavinsacquisition factor from 2 to 3. However, in this studvlchanging the interleaving acquisition factor from2io3 increased the imaging time from 4 minutes 42 sec-onds to 7 minutes 3 seconds; this increase may not befavorable in busy clinical settings.

We did not investigate the effects of cardiac gatingas a potential method to reduce high-intensity CSFartifacts. In fact, even with the knowledee that CSFmotion is driven by cardiac pulsation (2i), the usualimplementation of cardiac gating to synchronize im-qge acquisition,is not anticipated to help in reducingthe igh-intensity CSF artifacts at fast-FLAIR imag-ing. To elucidate this point, note that tvro approachesto cardiac gating are generally used. The first is tosynchronize image acquisition with the cardiac cycle,and the second is to perform FI-A.IR readout duringdiastole of the cardiac cycle. Both methods are exlpected to minimize amplitude fluctuations of the re-ceived signals along the phase-encoding direction.Therefore, motion ghosts along the phaie-encodingdirection could be reduced to a minimum with cardiaigating. However, neither of these gating approachesis related to the inflow of noninverted CSF into theimaging section that occurs during the 2-second TLHence, cardiac gatihg should not be used to reducehigh-intensity CSF artifacts and does not need to becompatible with the fast-FLAIR technique, as is thecase for the MR system used in our study.

. If cardiac gating is implemented in a way to reducehigh-intensify CSF artifacts at fast-FlAlil imaging,the separation of the inverting L80" and excitation 90"pulses should be synchronized (ie, TI equal to aninteger multiple of the cardiac cycle). Although thisapproach is possible, it is complicated by the follow-ing: 1) Changes in TI itself may lead to imperfectnulling of the CSF signal (17), which creates morehigh-intensity CSF aitifacts,

'even for nonmovins

CSF; and 2) multisection interleaving within TI belcomes less flexible when TI chanses all the time. Onthe other hand, if the CSF signal &n be appropriatelysuppressed, motion ghosts would also have zero sig-nal intensity and, hence, not be a problem at all. As aresult, the fact that the manufacturer of our MRllst= does not implement cardiac gating with thefasLFLAIR sequenie seems fully coripreh"ensible.

One final note is that the influence bf the imagingparameters invesligated in this study is specificallyrestricted to fasrFLAIR imaging with seleciive inver-sion. Recent studies (25-27) har,*e involved the use ofnonselective inversion pulses for an effective elimina_

AJNR: 23,March2002

tion of high-intensity CSF artifacts at the expense ofaltered image contrast (25), which is correctable witha k-space reordering scheme (26,27).In FI-AIR withnonselective inversion, a single inversion pulse wasused in all imaging sections, whereas in FI-AIR withselective inversion, one inversion pulse was used foreach imaging section. Because of intrinsically differ-ent inversion schemes, effects of imaging parameterson high-intensity CSF artifacts, as found in our study,do not apply to the FI-AIR sequence with nonselec-tive inversion. By the same token, the k-space reor-dering technique to improve image quality (26,27) isirrelevant to the fast-FLAIR method investigated inthis study. On the other hand, the use of adiabaticinversion pulse to correct an imperfect pulse profileat the edge of the RF coil (28) can theoretically bedirectly applied to the fast-F[.AIR sequence used inour study to further improve the suppression of CSFsignals.

Our findings suggest that, even with our preferredchoice of TRF and two interleaving acquisitions inthe routine clinical application of fast-FLAIR imag-ing, the incidence of high-intensity CSF artifacts atthe basal cisterns (>40%, Table 1) is still notable.Although most aneurysmal subarachnoid hemorrhagesoccur in the suprasellar cistems, where the high inci-dence of artifacts does not seem to be a problem be-cause CSF suppression remains largely successful in thisarea. Approximately 10Vo of the cases with subarach-noid hemorrhage from aneuysms in the basilar s'stemoccur as isolated prepontine hemorrhage (29). There-fore, the possibility that the high-intensity CSF artifactson fast-FLAIR images can obscure hemorrhagic lesionsshould be given special attention, particularly so withsubacute subarachnoid hemorrhages in which the fast-FL-AIR signal intensity may not be as high as that in theacute lesion (10).

ConclusionThe findings of this study showed thar high-inten-

sity CSF artifacts at the basal cisterns occur at a rateof about 40-80% on fast-FL,AIR imases. Thev arefrequently encountered in the presencjof rapiO CSfflow and may obscure hemorrhagic lesions. The ap-propriate choice of optional sequence parameters infast-FLAIR imaging helps reduce the incidence ofartifacts.

References1. De Coene B, Hajnal JV, Gatehouse P, et al. MR of the brain using

fluid-attenuated inversion recoverT €I"AIR) pulse sequences.A.INR Am J Neuroradiol 1992;13:1555-1564

2. Tsuchiya K, Mizutani Y, Hachiya J. Preliminary evaluation offluid.attenuated inversion-recovery MR in the diagnosis of intra-cranial tumors. L/NR Am J Neuroradiol 1996;17:1081-1086

3. Bakshi R, Kamran S, Kinkel PR, et al. Euid-attenuated inversion-recovery MR imaging in acute and subacute cerebral intraventric-ular hemorrhage, AJNR Am J Neworadiol 1999:20:629-636

4. Hajnal JV, Bryant DJ, Kasuboski I. et al. Use of fluid attenuatedinversion recovetT GLAIR) pulse sequences in MRI of the brain.J Comput Assist Tomogr 1992;16:841-844

5. Noguchi K, Ogawa T, Inugami A, et al. Acute subarachnoid hem-orrhage: MR imaging with fluid-attenuated inversion recovery

398 WU

AJNR: 23, March 2002

pulse sequences. Radiologt 1995;1,96:773-7'/76. Brant-Zawadzki M, Atkinson D, Detrick M, et al. Fluid-attenuated

inversion recovery (FLAIR) for assessrnent of cerebral infarction:initial clinical experience in 50 patients. Stroke 1996;27:1187-1,191

7. Singer MB, Atlas SW, Drayer BP. Subarachnoid space disease:diagnosis with fluid-attenuated inversion-recovery MR imagingand comparison with gadolinium-enhanced spin-echo MR imag-ing-bfinded reader study. Radiologt 1998;208:417- 422

8. Rydberg JN, Hammond CA, Grimm RC, et al. Initial clinicalexperience in MR imaging of the brain with a fast lluid-attenuatedinversion-recovery pulse sequence. Radiologt 1994;193:17T180

9. Tsuchiya K, Inaoka S, Mizutani Y, Hachiya J. Fast fluid-attenuatedinversion-recovery MR of intracranial infections. AINR Am J Neu-ro rad,iol 1997 ;18:909 -913

10. Noguchi K, Ogawa T, Seto H, et al. Subacute and chronic sub-arachnoid hemorrhage: diagnosis with fluid-attenuated inversion-recovery MR imaging. Radiologt 199'7 ;203:257-262

11. Adans JG, Melhem ER. Clinical usefulness of T2-weighted fluid-attenuated inversion recovery MR imaging of the CNS. AIR Am JRo entgeno I 1999 ;17 2:529 -53 6

12. Le Roux P, Hinks RS. Stabilization of echo amplitudes in FSEsequences. Magn Reson Med 1993;30:183-191,

13. Melhem ER. Jara H. Eustace S. Fluid-attenuated inversion recov-ery MR imaging: identification ofprotein concentration thresholdsfor CSF hlperintensity. L/R Am J Roentgenol 1997;\69:859-862

14. Essig M, Hawighorst H, Schoenberg SO, et al. Fast fluid-attenu-ated inversion-recovery @I-AIR) MRI in the assessment of in-traaxial brain tlrrmots. J Magn Reson Irnaging 1998;8:789-798

15. Waga S, Shimosaka S, Sakakura M. Intracerebral hemorrhageremote from the site of the initial neurosurgical procedure. Nez-ro sutgery 1983;13:662- 665

16. Bakshi R, Caruthers SD, Janardhan V, Wasay M. IntraventricularCSF pulsation artifact on fast fluid-attenuated inversion recoveryMR images: analysis of 100 consecutive normal studies.AlNRAm JNeuroradiol 2000;21 :503-508

L7. Rydberg JN, Riederer SJ, Rydberg CH, Jack CR. Contrast optimi-zation of fluid-attenuated inversion recovery OLAIR) imaging.Magn Reson Med 1995;34:868-8'77

18" Melhem ER, Jara H, Shakir H, Gagliano TA. Fast inversion-

CEREBROSPINAL FLUID ARTIFACTS 399

recovery MR: the effect ofhybrid RARE readout on the null pointsof fat and cerebrospinal fluid. IJNR Am J Neuroradiol 7997 18:L627-1633

19. Katz J, Peshock RM, Malloy CR, Schaeffer S, Parkey RW. Even-echo rephasing and constant velocity flow. Magn Reson Med 1,987;4:422-430

20. Haacke EM, Lenz GW. Improving image quality in the presence ofmotion by using rephasing gradients.,4,IR;4m J Roentgenol 1987;148:1251-1258

21. Hinks RS, Constable RT. Gradient moment nulling in fast spinecho. Magn Reson Med 1994;32:698-706

22. Hennig J. Multiecho imaging sequences with low refocusing flipangles. I Magn Reson 1988;78:397-407

23. Cho ZH, Ro YM. Reduction of susceptibility artifact in gradient-echo imaging. Magn Reson Med 1992;23:193-200

24. Bradley WG Jr, Scalzo D, Queralt J, Nitz WN, Atkinson DJ, WongP. Normal-pressure hydrocephalus: evaluation with cerebrospinalfluid llow measurements at MR imaging. Radiologt 1996;198:523-529

25. Tanaka N, Abe T, Kojima I( Nishimura H, Hayabuchi N. Appli-cability and advantages of fl ow artifact-insensitive fl uid-attenuat€dinversion-recovery MR sequences for imaging the posterior fossa.AJNR Am J Neuroradiol 2000;21:1095-1098

26. Herlihy AH, Oatridge A, Curati WL, Puri BK Bydder GM, HajnalJV. FLAIR imaging using nonselective inversiotr pulses combinedwith slice excitation order cycling and k-space reordering to reduceflow artifacts. Magn Reson Med 2001;46:354-364

27. Hetlihy AH, Hajnal JV, Curati WL, et al. Reduction of CSF andblood flow artifacts on FL{IR images of the brain with k-spacereordered by inversion time at each slice position (KRISP),A|NRAm J Neuroradiol 200J,;22:896-904

28. Hajnal JV, Oatridge A, Herlihy AH, Bydder GM. Reduction ofCSF artifacts on FLAIR images by using adiabatic inversionpdses. AJNR Am J Neuroradiol 2001;22:317-322

29. Kallmes DF, Clark HP, Dix JE, et al. Ruptured vertebrobasilaraneurysms: frequency of the nonaneurysmal perimesencephalicpattern of hemorrhage on CT scans. Radiologt 1996;201,:657-660