com pars ion of image quality of tof and ce mra

8/8/2019 Com Pars Ion of Image Quality of TOF and CE MRA

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Comparison of image quality, diagnostic confidence and

interobserver variability in contrast enhanced MR angiography and

2D time of flight angiography in evaluation of carotid stenosis

1D MITRA, FRCR, 1D CONNOLLY, FRCR, 1S JENKINS, FRCR, 1P ENGLISH, DCR, 1D BIRCHALL, FRCR,1C MANDEL, FRCR, 1K SHRIKANTH, MD, 2B GREGSON, PhD and 1A GHOLKAR, FRCR

1Department of Neuroradiology, Regional Neurosciences Centre, Newcastle General Hospital,

Westgate Road, Newcastle upon Tyne NE4 6BE and 2 Academic Department of Neurosurgery, School

of Surgical and Reproductive Sciences, University of Newcastle upon Tyne NE1 7RU, UK

ABSTRACT. The aim of this study was to compare image quality, level of diagnosticconfidence and interobserver agreement in assessment of carotid stenosis with contrastenhanced MR angiography (CE MRA) in comparison with 2D time of flight MRangiography (2D TOF MRA). 60 carotid arteries in 30 patients were examined by threeobservers. Image quality and diagnostic confidence were assessed on the basis of avisual analogue scale. Interobserver variability was assessed with the help of intraclasscorrelation coefficient. Median values on the visual analogue scale for image qualityand diagnostic confidence were higher for CE MRA compared with 2D TOF MRA for allthree observers. Higher intraclass correlation values were recorded for interobservervariability for CE MRA compared with 2D TOF MRA both for visual estimation of carotidstenosis as well as for measurement of carotid stenosis on the basis of North AmericanSymptomatic Carotid Endarterectomy Trial (NASCET) and European Carotid SurgeryTrial (ECST) criteria. CE MRA provides better image quality, higher level of diagnosticconfidence and more interobserver agreement compared with 2D TOF MRA.

Received 3 February 2005Revised 14 June 2005Accepted 15 July 2005

DOI: 10.1259/bjr/72842752

’ 2006 The British Institute of

Radiology

An atherosclerotic lesion at the carotid bifurcation is

one of the major causes of ischaemic strokes. The NorthAmerican Symptomatic Carotid Endarterectomy Trial [1](NASCET) and European Carotid Surgery Trial [2](ECST) have demonstrated that surgical intervention ismore beneficial compared with medical management insymptomatic patients with more that 70% carotidstenosis. The value of carotid endarterectomy has beenextended to include asymptomatic carotid stenosisgreater than 60% after the Asymptomatic CarotidAtherosclerosis Study [3] (ACAS). Accurate pre-opera-tive assessment of the degree of carotid stenosis istherefore of crucial importance as the benefit of surgeryis not proven in lesser degrees of stenosis.

Conventional catheter angiography (CA) is accepted asthe gold standard in assessment of carotid stenosis and isthe modality used in the measurement of stenosis inNASCET and ECST trials. However, due to the knownrisks of CA (overall 1–2% risk of thromboemboliccomplication, risks increasing with age and presence of generalized atherosclerosis), increasing numbers of centres are using non-invasive methods for pre-operativeevaluation of carotid stenosis. Doppler ultrasound (DUS)is routinely used as the screening technique in manycentres. MR angiography (MRA) is another technique,which is used either to confirm or supplement DUSfindings.

Time of flight MRA (TOF MRA) uses inflow of unsaturated protons in blood to generate signal withina blood vessel. However, due to dependence on flow,

TOF MRA is prone to flow related artefacts such as

signal dropout caused by turbulence in a severelystenosed artery. The technique is also prone to move-ment artefacts due to relatively long scan time.

Contrast enhanced MRA (CE MRA) uses the T 1shortening effect of intravenous paramagnetic contrastagent gadolinium to generate the signal. It is, therefore,less prone to, although not completely free of, the flowrelated artefacts in TOF MRA. CE MRA also requires lessscan time and covers a wider field of view, which allowsassessment of the aortic arch and proximal commoncarotid arteries.

A number of studies have been carried out to evaluatespecificity and sensitivity of CE MRA using CA as the

gold standard [4–12]. However, there are relatively fewstudies [13, 14], which have compared TOF and CE MRAdirectly. These latter studies have looked at the compar-ison of the two techniques in terms of delineation of morphological details and observer confidence but havenot included interobserver variability assessment. Theaim of the current study is to evaluate the image quality,diagnostic confidence of the observer and interobservervariability of the two techniques.

Materials and methods

30 consecutive patients with suspected carotid bifur-cation disease were prospectively included in this study.A DUS study was performed in all the patients. DUS

The British Journal of Radiology, 79 (2006), 201–207

The British Journal of Radiology, March 2006 201



results were available in all but three patients. Allpatients had 2D TOF MRA of the carotid bifurcation and3D CE MRA from the aortic arch to the skull base. All theMRA studies were performed in a Philips 1.5 Teslascanner (Philips, Best, The Netherlands) using flexiblephased array coil.

For CE MRA, an 18-gauge cannula was inserted in the

ante-cubital vein. A power injector (Medrad Spectris;Medrad Inc., Maastricht, The Netherlands) was used toadminister 15 ml of Magnevist (Gadopentate; ScheringAG, Berlin, Germany) at a rate of 1.5 ml s21. Bolustracking technique was used for image acquisition,whereby a single coronal slice was acquired at a rate of 1.67 frames per second while the contrast was beinginjected and acquisition of CE MRA was triggered aftercontrast was seen in the aortic arch. A fast gradient echosequence (3D FFE; Philips; repetition time (TR)55.2 ms,echo time (TE)51.8 ms, flip angle 40 ,̊ field of view270 mm and matrix size 3366 512) in the coronal planewas acquired using 50% slice interpolation giving a voxelsize of 1 mm6 0.5 mm6 0.5 mm. Data in the central k-space was acquired first using an elliptocentric k-spacefilling technique (CENTRA; Phillips). As central k-spaceholds data with high amplitude and low spatial resolu-tion, this technique allows most of the contrast informa-tion to be obtained while gadolinium was in the arterialphase. Total acquisition time for CE MRA sequence was1 min 27 s.

An axial 2D TOF MRA (TR517 ms, TE53.4 ms, flipangle 60 ,̊ field of view 200 mm and matrix size 224 6512) study incorporating overlapping 3 mm slices tocover the carotid bifurcation was obtained in the samesession. Venous contamination was prevented by using a15 mm ‘‘travelling’’ superiorly positioned pre-saturation

pulse. Total acquisition time for the TOF MRA sequencewas 2 min.

Apart from the different scanning parameters men-tioned above, CE MRA can be visually distinguishedfrom TOF MRA by the coronal plane of acquisition of thesource images (as opposed to axial acquisition for TOFMRA), larger anatomical coverage and more backgroundsuppression.

Hard copy images were produced for both CE MRAand TOF MRA with 9 maximum intensity projection(MIP) reconstructions at 40˚ steps and assessment of stenosis was made from the hard copies.

In all 120 sets of images (60 carotids in 30 patients

imaged with two MRA technique for each carotid) wereindependently assessed by 3 radiologists. Image orderwas completely randomized so that images of the leftand the right carotids as well as the images in the twomodalities (i.e. CE and TOF MRA) were scatteredthroughout the 120 sets of images thereby reducing the

bias affecting the assessment of the degree of stenosis. Ittook several sittings by each radiologist to complete theassessments.

Image quality was assessed by visual analogue scale(VAS). The VAS consisted of a 5 cm long line withmaximum quality at 5 and minimum quality at 0. Theimages were specifically assessed for slice misregistration,

pulsation artefact, venous flow signal, presence of plaqueulceration, visualization of external carotid artery (ECA) branches(superior thyroid andlingual) and signal dropout.

Carotid stenosis was assessed both by visual estima-tion and by measurements on the basis of NASCET andECST criteria. Stenosis was measured with the film on ahorizontal viewing box. Electronic callipers (DigimaxMeasy 2000; Swissprecision) were used to ensureaccurate measurement of stenosis. Visual estimationwas graded from 1 to 6 on the basis of NASCET criteria

(1, 0%; 2,,

50%; 3, 50–70%; 4, 70–95%; 5,.

95%; and 6,100%). Calliper measurements were carried out at thelevel of maximum stenosis, distal normal internal carotidartery, common carotid artery and estimated carotid

bulb. Percentage of stenosis was then calculated on the basis of NASCET and ECST criteria.

Level of observer confidence on assessment of stenosiswas scored both for visual estimation and estimation onthe basis of measurements described above. This wasagain done on a VAS described above with mostconfident at 5 and least confident at 0.

Statistical analysisData were transferred to a Microsoft Access database

and statistical analysis performed with SPSS software(SPSS Inc., Chicago, IL). Differences between the twotechniques in terms of image quality and observerconfidence were assessed using paired t-tests.Interobserver variability between observers was calcu-lated with the help of intraclass correlation coefficient.Mean, median, mode and standard deviation werecalculated on the VAS scores and displayed in box plots.

Results

The study was performed on 30 patients, including 21males and 9 females. In all 60 carotid arteries wereassessed. Initial screening DUS demonstrated ,50%stenosis in 24 carotids, 50–70% stenosis in 5 carotidsand .70% stenosis in 25 carotids. DUS results were notavailable in 6 carotids (3 patients).

Image quality

The median scores of image quality for CE MRA by thethree raters were 4.0, 3.5 and 2.65 and those for TOF MRAwere 2.05, 2.0 and 1.05, respectively (Figure 1). All three

differences were statistically significant ( p,0.00001).For further assessment of image quality, visualization of

the superiorthyroid and lingual branchesof external carotidarteries by the two techniques were assessed (Table 1).

Observer confidence for visual assessment of stenosis

Median scores for confidence level for visual assess-ment of stenosis by the three raters were 4.0, 3.7 and 4.0for CE MRA. Corresponding scores for TOF MRA were2.8, 1.9 and 2.8 (Figure 2). All three differences were

statistically significant ( p,

0.00001). Results of visualassessment of stenosis by three observers by both TOFMRA and CE MRA are given in Table 2.

D Mitra, D Connolly, S Jenkins et al

202 The British Journal of Radiology, March 2006



Observer confidence for assessment of stenosis by measurement

The median scores for confidence level for assessmentof stenosis by measurement by the three raters were CEMRA were 4.0, 3.55 and 3.5. Corresponding scores forTOF MRA were 2.65, 1.95 and 1.7, respectively

(Figure 3). Again, all the differences were highlystatistically significant ( p,0.00001). Results of assess-ment of stenosis by both NASCET and ECST methods bythree observers with both TOF MRA and CE MRA aregiven in Table 2.

Image artefacts

Image artefacts observed in the two techniques wereanalysed (Table 3). The figures in the table are out of 60carotid bifurcations analysed in this study.

Table 1. Visualization of ECA branches (all values out of 60)

TOF MRA CE MRA

Superior thyroid artery 13(21%) 37(62%)Lingual artery 11(18%) 49(81%)

TOF MRA, time of flight MR angiography; CE MRA, contrastenhanced MR angiography.

Figure 2. Box plots showing distribution of visual analoguescores for observer confidence (for visual estimation of

stenosis) from each of the three raters for contrast enhancedMR angiography (CE MRA) and time of flight MR angio-graphy (TOF MRA).

Table 2. Results of assessment of carotid stenosis by threeobservers (A, B and C) with the three methods (NASCET, ECSTand visual estimation) for both CE MRA and TOF MRA.Numbers under columns A, B and C denote number ofcarotids under each category of stenosis. Visual estimationwas based on 6 grades depending on the severity of stenosis

CE MRA

NASCET % A B C E CS T% A B C Visual % (grade) A B C

0% 1415 8 0% 1113 8 0%(Grade1) 1114 8,50% 151620 ,50% 151515 ,50%(Grade2) 18181750–70% 510 8 50–70% 5 8 8 50–70%(Grade3) 7 5 670–95% 11 7 9 70–95% 151213 70–95%(Grade4) 9111195–99% 10 810 95–99% 9 8 11 95–99%(Grade5) 10 813100% 5 4 5 100% 5 4 5 100%(Grade6) 5 4 5

TOF MRANASCET % A B C E CS T% A B C Visual % (grade) A B C

0% 1312 3 0% 1311 3 0%(Grade1) 1311 3,50% 151918 ,50% 111120 ,50%(Grade2) 14261850–70% 131119 50–70% 81111 50–70%(Grade3)12111570–95% 13 1 8 70–95% 22 616 70–95%(Grade4)14 2 12

95–99% 113 7 95–99% 117 7 95–99%(Grade5) 2 2 9100% 5 4 5 100% 5 4 3 100%(Grade6) 5 8 3

TOF MRA, time of flight MR angiography; CE MRA, contrastenhanced MR angiography; NASCET, North AmericanSymptomatic Carotid Endarterectomy Trial; ECST,European Carotid Surgery Trial.

Figure 1. Box plots showing distribution of visual analoguescores for image quality from each of the three raters forcontrast enhanced MR angiography (CE MRA) and time offlight MR angiography (TOF MRA).

Figure 3. Box plots showing distribution of visual analoguescores for observer confidence (for stenosis estimation on the

basis of measurements) from each of the three raters forcontrast enhanced MR angiography (CE MRA) and time offlight MR angiography (TOF MRA).

CE MRA and TOF MRA in carotid stenosis




The presence of signal dropouts were analysedseparately as this particular artefact caused significantproblems in the accurate assessment of the degree of stenosis (Table 4). Lower incidence of signal dropoutwas noted with CE MRA both at the level of stenosis(46.7% with TOF MRA, 18.3% with CE MRA) as well as

beyond the level of stenosis (58.3% with TOF MRA, 15%with CE MRA).

13 patients had normal carotid bulbs. Five of thesepatients demonstrated signal dropout in TOF MRA butnone showed signal dropout in CE MRA.

Plaque ulceration was detected more frequently withCE MRA compared with TOF MRA. An average of 18.6plaque ulcers in 60 carotids were detected with CE MRAcompared with 12.3 plaque ulcers in 60 carotids withTOF MRA by the three observers.

Interobserver variability

Interobserver agreement was measured with the helpof intraclass correlation using a two way mixed effectmodel for absolute agreement. Measurements weremade for visual evaluation of stenosis, NASCET gradingof stenosis and ECST grading of stenosis (Table 5). The

intraclass correlation values for CE MRA (0.893 for visualestimation, 0.890 for NASCET grading and 0.800 forECST grading) were consistently higher compared withTOF MRA (0.730, 0.758 and 0.737, respectively).

Discussion

The morbidity associated with carotid endarterectomyis dependent on the complication rate of surgery as wellas any complication from pre-operative investigation.Therefore, if CA is used in the pre-operative evaluationof carotid stenosis, a complication rate of 1–2% is addedto the surgical complication rate of 1–2%. Reducing therisk related to CA would, therefore, improve patientoutcome. Furthermore, although CA was used as a goldstandard in NASCET and ECST, its position as a goldstandard investigation for carotid stenosis is no longerincontrovertible. The limited projections of carotid

bifurcation obtained in CA can underestimate the degreeof stenosis caused by eccentric plaques. This may be oneof the factors causing the reported overestimation of stenosis by MRA compared with CA [11]. Currentpractice is moving towards non-invasive evaluation of degree of stenosis, with CA reserved only for selectedcases. In this scenario, it is of utmost importance tooptimize the modality of the non-invasive investigation

to prevent misclassification of patients and the resultantinappropriate treatment.

DUS has been advocated by some investigators [15] asa method of evaluating carotid stenosis prior toendarterectomy. However, DUS is limited by operatordependency, difficulty in identifying sub-total occlusionwith very slow flow as well as difficulty in clearlydefining the morphology of lesions in the carotid

bifurcation. In many centres, therefore, DUS is used intandem with MRA, with the latter often being theconfirmatory investigation [9].

Time of flight imaging is a well-established MRAtechnique. This is based on the signal generated from the

inflowing unsaturated protons. As this technique doesnot require external contrast injection, the image qualitydoes not depend on factors such as the timing of the

bolus injection, volume of contrast injected, etc. Thistechnique also has improved sensitivity to slow flow [16]and is more accurate in defining the morphology of theproximal internal carotid artery compared with DUS. Wehave used 2D TOF technique as it has been validated asan accurate method [9, 17] in this context and was thestandardized technique used in our department at thetime of the study.

Both 2D and 3D TOF MRA, however, have limitations.The most serious limitation is the loss of signal caused bycomplex flow pattern in the stenotic segment of the

artery causing over-estimation of the degree of stenosis.In order to produce a signal the inflowing blood should

be perpendicular to the scan plane. However, severestenosis results in turbulent flow where many of theprotons in the arterial blood are no longer flowingperpendicular to the scan plane and therefore do notproduce a signal. Furthermore, signal is only produced

by fresh protons flowing into the scan-plane, which havenot received saturation pulses. If, as in a subtotalocclusion, the flow is slow enough, these protons losetheir signal due to in-plane saturation. Long scan timesalso result in movement artefacts (mostly due toswallowing) (Figure 4) as well as slice misregistration.

In the present study, problematic slice misregistrationwas seen in 17 carotids with TOF MRA technique butnone with CE MRA technique.

Table 3. MR artefacts in the two techniques

TOF MRA CE MRA

Slice misregistration 32 NAProblematic slice

misregistration17 NA

Pulsation artefact 29 0Venous signal 3 23Problematic venous signal 0 1

NA, not applicable; TOF MRA, time of flight MR angiogra-phy; CE MRA, contrast enhanced MR angiography.

Table 4. Incidence of signal dropouts in the two techniques(all values out of 60)

TOF MRA CE MRA

At stenosis 28 11Beyond stenosis 35 9Tortuosity 32 0

TOF MRA, time of flight MR angiography; CE MRA, contrast

enhanced MR angiography.

Table 5. Intraclass correlation values for agreementbetween observers

TOF MRA CE MRA

Visual estimation 0.730 0.893NASCET grading 0.758 0.890ECST grading 0.737 0.800

TOF MRA, time of flight MR angiography; CE MRA, contrast

enhanced MR angiography; NASCET, North AmericanSymptomatic Carotid Endarterectomy Trial; ECST,European Carotid Surgery Trial.





CE MRA uses the T 1 shortening effect of gadolinium toproduce signal from a vessel. It is, therefore, not directlydependent on flow to produce a signal and has less of theflow related artefacts described above. However, as an

external contrast agent is administered, the timing of theinjection, volume injected and the flow rate are of crucialimportance. One of the major problems in CE MRA

technique is presence of venous signal, which can causedifficulty in image interpretation (Figure 5). Venoussignal was seen in three carotids with TOF MRAtechnique compared with 23 carotids with CE MRA in

this study. However, in only 1 out of the 23 carotids didthe venous signal prove to be a problem in imageinterpretation. This is in variance with another study [14]

(a) (b)

Figure 4. (a) Time of flight MR angiography (TOF MRA) and (b) contrast enhanced MR angiography (CE MRA) showing obliqueprojections of the carotid arteries. Note the significant degradation of the image in TOF MRA (arrows) due to movement, whichis not seen in the CE MRA image.

(a) (b)

Figure 5. (a) Anteroposterior (AP) and (b) oblique projections of contrast enhanced MR angiography (CE MRA) of carotidarteries showing presence of venous signal (arrows). Note that despite the presence of venous signal the visualization of thecarotid arteries is not significantly impaired.





where 27% of the contrast enhanced MRA images of thecarotid bifurcation was deemed non-diagnostic due tomasking of the carotid bifurcation by veins.

Specific techniques have been used in order to avoidthis phenomenon and to optimize signal from thearteries imaged. One such technique is called timeresolved CE MRA where image is acquired repeatedly

at a certain rate in a method akin to DSA (hence thetechnique is also known as MR DSA). In this techniquethe timing of the bolus injection is not criticallyimportant. In the present study, a bolus-trackingtechnique was used in order to optimize the timing of the injection. This technique is considered to be animprovement on the time resolved CE MRA [4].Furthermore, the central k-space data (i.e. the highamplitude and low resolution data) was acquired first,to make sure that high contrast information was acquiredwhile gadolinium was still in the arterial phase.

CE MRA provides a much wider field of viewcompared with TOF MRA (Figure 6) and allows assess-ment from the arch to the base of the skull and if

necessary up to the circle of Willis. This allows thecoverage from CE MRA to be on par with CA and helpsdetect any concomitant intracranial disease, which mayalter the decision to proceed to end-arterectomy.

QualityofimagesinbothTOFMRAandCEMRAdependon the spatial and contrast resolution as well as on thepresence or absence of artefacts. Loss of signal caused bynon-linear flow and in-plane saturation can result in poorresolution in TOF MRA. Signal dropouts in the stenotic andpost-stenotic segments were also seen more frequently withthe TOF technique than with the CE MRA technique(Table 4). Signal voids were also seen in some normal bulbsas well as a significant numberof tortuous carotid arteries in

TOF MRA but not seen with CE MRA (Table 4).

The higher spatial resolution of CE MRA comparedwith TOF MRA is also indicated by the better ability todemonstrate branches of the external carotid artery(Table 1 and Figure 6). In addition, plaque ulcerationwas also seen more frequently by CE MRA techniquethan TOF MRA. This is consistent with findings of anearlier study comparing the two techniques [13].

Slice misregistration, another known problem of 2DTOF MRA [16], resulted in difficulty in image inter-pretation in 17 out of 60 carotid bifurcations in this study.This problem is not encountered with CE MRA, as it is avolume acquisition technique. With all the factorsdescribed above, it is not surprising that the level of diagnostic confidence of all three raters have beenconsistently higher with CE MRA than TOF MRA, bothfor visual estimation and estimation based on measure-ment (Figures 2 and 3). This is in keeping with thefindings of a similar study [13] where on a scale of 1 to 3(1 being the best and 3 being the worst technique) themean diagnostic confidence score was 1.10 for CE MRA1.90 for pooled 2D and 3D TOF images ( p,0.01).

Any imaging technique also needs to be assessed forinterobserver variability, particularly a relatively newtechnique such as CE MRA. High observer variability insome imaging techniques such as DUS has resulted incriticism and lack of wide acceptance. Low observervariability of DSA [18] on the other hand is one of thefactors favouring the use of this technique for pre-operative carotid stenosis assessment. In the presentstudy, interobserver variability has been studied

between all three observers as well as for all threemethods of assessment of stenosis, i.e. visual assessment,calliper measurement by NASCET and calliper measure-ment by ECST criteria. Interobserver variability was

measured with the help of the intraclass correlation

(a) (b)

Figure 6. (a) Time of flight MR angiography (TOF MRA) and (b) contrast enhanced MR angiography (CE MRA) showing oblique

projections of the carotid arteries. Note the much larger field of view of CE MRA demonstrating vessels from the arch of theaorta to the base of the skull and the better demonstration of the external carotid branches on CE MRA (long arrows) comparedwith TOF MRA (short arrows).





coefficient as it is considered to be a better test thankappa statistic when there are more than two observers.Intraclass correlation values are consistently higher in CEMRA compared with TOF MRA suggesting betterinterobserver agreement. With CE MRA, agreementwas best for visual assessment followed by NASCETgrading with the lowest agreement with ECST grading.

Greatest difference between CE MRA and TOF MRAwith regard to intraclass correlation values was in visualassessment of stenosis with very high agreement in CEMRA and only moderate agreement in TOF MRA.

Variability between different observations by the sameobserver (i.e. intraobserver variability) can also be animportant tool in assessing the reliability of a technique.This assessment was not included in the present studyand this may be considered a shortcoming of the study.

In current radiological practice, assessment of stenosisis made by looking at the reconstructed images in aworkstation. However, it is possible that each observerwould use a different set of projections compared withother observers for estimation of carotid stenosis.Therefore, in this study, assessment of images was madefrom hard copies so that each observer saw exactly thesame MIP projections and therefore eliminated any biasin the estimation of interobserver variability.

The lack of comparison of the techniques describedwith CA could be considered to be a weakness of thestudy. CA was not performed in these patients becausethis was not part of the normal diagnostic protocol forassessment of carotid stenosis in the centre where thestudy was carried out. In view of the risks associatedwith CA, it would have been difficult to obtain ethicalapproval to perform CA just for the purpose of the study.

The technique of performing CE MRA has evolved

from the time of this study. The technique of CE MRAdescribed in this paper was one that was being used atthe time in the department where the study was carriedout. However, the results show that even with thetechnique used, CE MRA method was better than TOFMRA in terms of higher image quality, higher level of diagnostic confidence and less interobserver variability.

Conclusion

CE MRA provides better image quality, higher level of diagnostic confidence and less interobserver variability

compared with 2D TOF MRA. The CE MRA techniquehas now replaced TOF MRA and CA as the modality of choice in pre-surgical evaluation of extracranial carotidstenosis in the centre where this study was carried out.

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com pars ion of image quality of tof and ce mra

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