Nonenhanced ECG-gated time-resolved 4D steady-state free precession (SSFP) MR angiography (MRA) of cerebral arteries: Comparison at 1.5 T and 3 T

European Journal of Radiology 81 (2012) e531–e535

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Nonenhanced ECG-gated time-resolved 4D steady-state free precession (SSFP) MR angiography (MRA) of cerebral arteries: Comparison at 1.5 T and 3 T R.S. Lanzman a,∗ , P. Kröpil a,1 , P. Schmitt b,2 , H.J. Wittsack a,1 , D. Orzechowski a,1 , J. Kuhlemann a,1 , C. Buchbender a,1 , F.R. Miese a,1 , G. Antoch a,1 , D. Blondin a,1 a b

Department of Diagnostic and Interventional Radiology, University Düsseldorf, Medical Faculty, Moorenstr. 5, 40225 Düsseldorf, Germany Siemens AG, Healthcare Sector, Allee am Roethelheimpark 2, 91052 Erlangen, Germany

a r t i c l e

i n f o

Article history: Received 17 March 2011 Accepted 7 June 2011 Keywords: Nonenhanced MRA Steady-state free precession (SSFP) 3T Cerebral artery

a b s t r a c t Purpose: To compare image quality of nonenhanced time-resolved 4D steady-state free precession MR angiography (4D SSFP MRA) of cerebral arteries at 1.5 T and 3 T. Materials and methods: 12 healthy subjects (mean age 29.4 ± 6.9 years) were studied at both 1.5 T and 3 T. Two different positions of the acquisition slab were evaluated; in one acquisition the imaging slab included the carotid siphon (“Slow ”), in the other acquisition the imaging slab was placed superior to the carotid siphon (“Shigh ”). Subjective image quality of cerebral arteries was assessed independently by two readers on a 4-point scale. Relative Signal-to-Noise-Ratio (SNR) was determined for the M1 segment of the middle cerebral artery. Results: Subjective image quality of the anterior cerebral artery (segments A1, A2) was significantly higher at 1.5 T as compared to 3 T, while 3 T provided significantly higher image quality for segment P3 of the posterior cerebral artery. For the middle cerebral artery (segments M1–M3), image quality was significantly higher at 1.5 T than at 3 T when the carotid siphon was included in the acquisition slab (“Slow ”), while no significant difference was found between 1.5 T and 3 T with “Shigh ”. Relative SNR was significantly higher at 1.5 T (23.1 ± 5.1) as compared to 3 T (12.1 ± 7.8) for “Slow ” and significantly higher at 3 T (29.8 ± 5.9) than at 1.5 T (24.2 ± 3.6) for “Shigh ”. Conclusion: Our results indicate that 4D SSFP MRA should preferably be performed at 1.5 T with inclusion of the carotid siphon in the acquisition slab, which might be required for the assessment of intracranial collateral flow. © 2011 Elsevier Ireland Ltd. All rights reserved.

1. Introduction Dynamic angiograms of the cerebral vasculature are valuable tools for diagnosis and treatment planning of vascular pathologies, as for example arterio-venous malformations (AVMs) or stenoocclusive disease of brain-supplying arteries [1,2]. In patients with arteriosclerosis of cervical and cerebral arteries, the presence of intracranial collateral flow can help to assess the risk and prognosis of stroke [3]. Due to its high temporal and spatial resolution, conventional digital subtraction angiography (DSA) is still considered the diagnostic reference standard, but exposes patients to ionizing radiation, iodinated contrast material as well as potential procedural risks, as for example thromboembolic complications [4]. Time-resolved contrast-enhanced MRA has been used with increasing interest for dynamic visualization of the cerebral vasculature

∗ Corresponding author. Tel.: +49 211 81 17754; fax: +49 211 81 19487. E-mail address: [email protected] (R.S. Lanzman). 1 Tel.: +49 211 81 17754; fax: +49 211 81 19487. 2 Tel.: +49 9131 84 7564; fax: +49 9131 84 8411. 0720-048X/$ – see front matter © 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ejrad.2011.06.044

[1,5]. However, even with the use of parallel imaging and modern undersampling techniques, the temporal resolution typically ranges between 0.5 and 2 s. In addition, in patients with decreased renal function the application of gadolinium-based contrast agent is considered problematic due to the potential risk for the development of nephrogenic systemic fibrosis (NSF) [6,7]. Arterial spin labelling (ASL) techniques are usually applied to determine tissue perfusion using blood as an endogenous contrast material. ASL techniques with varying delay times in combination with ECGgated SSFP MRA techniques have recently been introduced for dynamic MR angiography [8–10], providing both hemodynamic and anatomical information simultaneously. The purpose of the present study was to evaluate image quality of 4D SSFP MRA at 1.5 T and 3 T in healthy subjects using two different positions of the acquisition slab.

2. Materials and methods P.S., who assisted in the development of the utilized sequence, is an employee of Siemens AG, Healthcare Sector (Erlangen,

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Fig. 1. Scheme showing the two different slab positions. Slab position “Shigh ” (A) was placed superior to the carotid siphon, slab position “Slow ” (B) included the carotid siphon.

Germany). All the other authors had full control over the entire information and data submitted for publication. This study was approved by the local ethics committee and written informed consent was obtained from all participants. Twelve healthy subjects (5 men, 7 women, mean age 29.4 ± 6.9 years) without any history of cerebrovascular diseases participated in this study. In order to assess the effect of mucosal thickening in the paranasal sinus on image quality, one patient with chronical sinusitis was scanned at 1.5 T and 3 T, but was not considered for statistical analysis. All subjects were examined with a 12-element head matrix coil in a random order on a 1.5 T and 3 T MR scanner (Magnetom Avanto and Magnetom Trio Tim System, Siemens AG, Healthcare Section, Erlangen, Germany). Subjects were studied in supine position and ECG-electrodes were attached to their chest. For nonenhanced 4D SSFP MRA, the technique described by Bi et al. was applied [8], which is based on the acquisition of two magnetization-prepared and ECG-triggered segmented 3D TrueFISP CINE datasets. In each cardiac cycle, upon detection of the ECG R-wave, an inversion preparation pulse is played out followed by acquisition of N temporal phases, in which a certain number of segments is acquired. With this procedure, two series of 3D datasets are sampled sequentially, one during recovery after nonselective inversion and another after slab-selective inversion. Static tissues experience both non-selective and slab-selective inversion and show identical signal in both experiments, while inflowing blood is only exposed to the non-selective inversion. By subtraction of the two datasets, static signal from background tissues is cancelled out, but inflowing blood appears with bright signal due to the difference between inverted and non-inverted blood. This labelling scheme corresponds to the FAIR principle [11]. The time series of subtracted 3D datasets are then subjected to inline MIP processing in three orientations (transverse, sagittal, coronal). Identical scan parameters were used for the 4D SSFP MRA protocols at 1.5 T and 3 T. A total of 52 slices and 9 temporal phases were acquired with a temporal resolution of 105 ms using the following imaging parameters: field of view (FOV) 165 mm × 220 mm, voxel size 1.0 mm × 1.0 mm × 1.0 mm, TE 1.4 ms, constant flip angle of 35◦ at 1.5 T and constant flip angle of 18–27◦ at 3 T, bandwidth 745 Hz/pixel, parallel imaging with a GRAPPA factor of 2. At both 1.5 and 3 T, two parallel oblique axial acquisitions were performed; in one acquisition the imaging slab included the carotid siphon (“Slow ”), in the other acquisition the lower boundary was placed superior to the carotid siphon to include the distal portions of the carotid and basilar artery (“Shigh ”, Fig. 1). Both slab positions are displayed in Fig. 1.

2.1. Image analysis All MR images were analyzed by two radiologists that were blinded to the field strength used for 4D SSFP MRA acquisitions. Subjective image quality of axial MIP reconstructions of 4D SSFP MRA was assessed independently by two radiologists for the following predefined vessel segments: M1 segment of the middle cerebral artery (MCA) (from internal carotid artery bifurcation to main division of the MCA); M2 segment of MCA (from main division to insula); M3 segment of MCA (from insula to opercular turn of MCA branches); A1 segment of anterior cerebral artery (from internal carotid artery bifurcation to anterior communicating artery); A2 segment of anterior cerebral artery (from anterior communicating artery to genu of corpus callosum); P1 segment of posterior cerebral artery (from basilar artery bifurcation to posterior communicating artery); P2 segment of posterior cerebral artery (from posterior communicating artery to back of midbrain); P3 segment of posterior cerebral artery (from back of midbrain to division into posterior temporal and parieto-occipital arteries). In addition, subjective image quality was assessed for the distal internal carotid artery (ICA). For each segment, subjective image quality was rated using a four-point scale as follows: 4 = excellent (sharp and complete delineation of vessel borders, homogenous vessel signal without artifacts), 3 = good (good delineation of vessel borders with slight irregularities, homogenous vessel signal with slight artifacts), 2 = fair (vessel borders scarcely definable, inhomogeneous vessel signal) and 1 = non-diagnostic (vessel borders not definable). For quantitative analysis, region-of-interest (ROI) measurements were performed on subtracted 3D datasets in the M1 segment of the right middle cerebral artery to determine signal intensity (SI). An additional ROI was drawn in the adjacent cerebral parenchyma and the standard deviation (SD) was determined as noise. Relative signal-to-noise ratio (SNR) was calculated as follows: SNR = SI(artery)/SD(parenchyma).

2.2. Statistical analysis Wilcoxon signed rank test was performed to determine differences in subjective image quality at 1.5 T and 3 T for slab positions “Slow ” and “Shigh ”. Differences in relative SNR between acquisitions at 1.5 T and 3 T were assessed with paired student’s t-test. -Values were used to determine agreement between both readers. A value of less than 0.50 corresponds to poor agreement, a value of 0.50–0.75 corresponds to good agreement and a value greater than 0.75 corresponds to excellent agreement.

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Fig. 2. Representative 4D SSFP MR Angiographies of a healthy subject at different time points: (A) 1.5 T, “Slow ”; (B): 3 T, “Slow ”; (C): 1.5 T, “Shigh ”; (D): 3 T, “Shigh ”. Note the poor visualization of the middle cerebral artery at 3 T with “Slow ” (B, arrow).

3. Results Image acquisition was completed successfully in all subjects at both 1.5 T and 3 T within an acquisition time of approx. 5 min. Fig. 2 shows representative 4D SSFP MRA datasets. Subjective image quality of the A1 and A2 segments of the anterior cerebral artery was significantly higher at 1.5 T as compared to 3 T (Table 1). At 3 T, image quality of segment A1 and A2 was rated not diagnostic in 3 of 12 (75%) and 10 of 12 (83.3%) subjects with slab position “Shigh ”, respectively. With slab position “Slow ”, image quality of segment A1 and A2 was non-diagnostic in 6 of 12 (50%)

and 11 of 12 (91.7%) subjects at 3 T, respectively. In contrast, at 1.5 T non-diagnostic image quality was only observed in 2 of 12 (16.7%) subjects for segment A2 with slab position “Slow ”. When slab position “Slow ” was applied, image quality of the middle cerebral artery (segments M1–M3) was significantly higher at 1.5 T than at 3 T. Image quality of segment M1 was non-diagnostic in 4 of 12 subjects at 3 T with slab position “Slow ”. Though not statistically significant, peripheral branches of the middle cerebral artery (segment M3) were visualized better at 3 T than at 1.5 T with “Shigh ” (Table 1), while segments M1 and M2 were rated better at 1.5 T than at 3 T.

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Table 1 Mean subjective image quality for each segment. M1 1.5 T “Shigh ” 3 T “Shigh ” 1.5 T “Slow ” 3 T “Slow ” * #

3.92 3.50 3.79 2.29

M2 ± ± ± ±

0.28 0.77 0.38 0.99*

3.83 3.33 3.38 1.92

M3 ± ± ± ±

0.37 1.05 0.65 1.04*

2.96 3.21 2.46 1.58

A1 ± ± ± ±

0.48 1.18 0.90 0.96*

3.92 2.92 3.71 1.88

A2 ± ± ± ±

0.28 1.24# 0.52 1.04*

3.17 1.17 2.42 1.08

P1 ± ± ± ±

0.69 0.37# 0.89 0.28*

4.0 4.0 3.92 4.0

P2 ± ± ± ±

0 0 0.28 0

3.75 3.92 3.71 3.92

P3 ± ± ± ±

0.43 0.28 0.52 0.28

3.09 3.75 2.83 3.54

± ± ± ±

0.57 0.60# 0.69 0.63*

p < 0.05 as compared to 1.5 T “Slow ”. p < 0.05 as compared to 1.5 T “Shigh ”.

Table 2 Number (n) of subjects with non-diagnostic image quality for each segment.

1.5 T “Shigh ” 3 T “Shigh ” 1.5 T “Slow ” 3 T “Slow ”

4. Discussion

M1

M2

M3

A1

A2

P1

P2

P3

n=0 n=0 n=0 n=4

n=0 n=2 n=0 n=6

n=0 n=2 n=1 n=8

n=0 n=3 n=0 n=6

n=0 n = 10 n=2 n = 11

n=0 n=0 n=0 n=0

n=0 n=0 n=0 n=0

n=0 n=0 n=0 n=0

For segment P3, image quality was significantly higher for both positions (“Slow ” and “Shigh ”) at 3 T as compared to 1.5 T. Image quality did not differ between field strengths for segments P1 and P2 (Tables 1 and 2). For subjective analysis, agreement between both readers was excellent ( = 0.86) For position “Slow ”, relative SNR of the middle cerebral artery (M1) was significantly higher at 1.5 T (23.1 ± 5.1) as compared to 3 T (12.1 ± 7.8). Conversely, relative SNR of segment M1 was significantly higher at 3 T (29.8 ± 5.9) than at 1.5 T (24.2 ± 3.6) when slab position “Shigh ” was applied. In one patients suffering from chronic sinusitis, image quality was comparable for both acquisition schemes at 1.5 T and 3 T and the anterior cerebral artery (A1, A2) was visualized better at 3 T as compared to healthy subjects (Fig. 3).

Fig. 3. 4D SSFP MRA in the transversal, coronal and sagittal plane of a subject suffering from chronic sinusitis. Note the excellent image quality for all segments at time point 630 ms: (A): 1.5 T, “Slow ”; (B): 3 T, “Slow ”; (C): 1.5 T, “Shigh ”; (D): 3 T, “Shigh ”. CT scan (E) showing mucosal thickening in the sphenoid sinus (arrow), which might explain the excellent visualization of the anterior cerebral artery at 1.5 T and 3 T.

In this study we have investigated the image quality of an ECGgated nonenhanced 4D SSFP MRA at 1.5 T and 3 T using two different positions of the acquisition slab. Using the lower slab position (“Slow ”) which included the carotid siphon, image quality was significantly lower at 3 T as compared to 1.5 T for the anterior and middle cerebral artery. Furthermore, the anterior cerebral artery was visualized better at 1.5 T than at 3 T when the acquisition slab was placed superior to the carotid siphon (“Shigh ”). These findings are most probably related to higher susceptibility effects at 3 T in the proximity of air-filled sinus, which might lead to spin dephasing in the carotid siphon [12]. This hypothesis is supported by findings in a patient suffering from chronic sinusitis, in which comparably high image quality was achieved for the anterior and middle cerebral artery at 1.5 T and 3 T for both slab positions. Reliable visualization of the carotid siphon and the basilar artery as well as the circle of Willis is crucial for the assessment of cerebral hemodynamics in patients with steno-occlusive disease of brain-supplying arteries [13]. Although only healthy volunteers were included in our study, our results suggest that 1.5 T might be superior to 3 T for the assessment of intracranial collateral flow patterns in the circle of Willis. In a recent study, 4D SSFP MRA has shown a high sensitivity and specificity for detection of primary collateral flow in patients with steno-occlusive disease at 1.5 T [13]. When the acquisition slab was placed superior to the carotid siphon (“Shigh ”), the relative SNR of the middle cerebral artery (M1segment) was 23% higher at 3 T as compared to 1.5 T. In theory, the gain in SNR should be twofold when transitioning from 1.5 T to 3 T due to higher B0. However, with bSSFP techniques, vessel contrast depends on the T2/T1 ratio. The longer T1 relaxation times at 3 T might explain the less pronounced SNR gain. For segments P1 and P2, image quality was comparable between 1.5 T and 3 T, whereas segment P3 was visualized significantly better at 3 T with both slab positions. Furthermore, M3 branches were visualized better at 3 T than at 1.5 T with the higher slab position (“Shigh ”), although the difference was not statistically significant. These findings indicate that 3 T might possess an advantage over 1.5 T for the visualization of vascular pathologies located peripherally in the vascular territories of the middle and posterior cerebral artery, provided optimal positioning of the acquisition slab. In a recent study, Yan et al. have used a nonenhanced time-resolved SSFP MRA at 3 T for visualization of an AVM located peripherally in the occipitoparietal lobe at [9]. The presented nonenhanced 4D SSFP MRA has several advantages over time-resolved 4D contrast-enhanced MR angiography (4D CE-MRA). The temporal resolution of 4D SSFP MRA is higher than the temporal resolution generally obtained with 4D CE-MRA [1,5]. In addition, 4D SSFP does not require the administration of gadolinium-based contrast material. Therefore, measurements can be repeated in case of poor image quality and patients with impaired renal function are not exposed to the potential risk of nephrogenic systemic fibrosis (NSF). On the other hand, the 4D SSFP MRA sequence applied in our study suffers from technical constraints. As the depicted vessel

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length depends on flow velocity and delay times following the labelling pulse, it seems not to be suitable for coverage of a large volume in the direction of blood flow, as for example for the peripheral arteries. With the FAIR labelling technique that was applied in our study, venous inflow from the upper border of the acquisition window is visualized and might impair the assessment of cerebral arteries. Venous inflow can be eliminated with alternative arterial spin labelling techniques, as for example signal targeting with alternating radiofrequency (STAR) ASL [14]. However, we cannot predict to which extent our results are transferable to other labelling techniques. There are limitations to our study. Although we intended to use identical imaging parameters at 1.5 T and 3 T, a reduced flip angle was applied at 3 T due to SAR constraints. Numerical simulations have shown that the dependence of the signal on flip angles is rather small for late temporal phases [15]. However, we cannot exclude that our results were biased by the difference in flip angles. Furthermore, due to the use of parallel imaging, determination of vessel SNR is complicated. With parallel imaging, noise is nonuniformly distributed across the image and ROI-based noise measurements in a region outside the body are not reliable [16]. Therefore we performed ROI measurement in the brain parenchyma on subtracted images. The standard deviation of this ROI is a good estimate of noise in close proximity to the middle cerebral artery and allows for calculation of a relative SNR [17]. However, our measurements might not reflect the signal-to-noise ratio for the entire image. 5. Conclusion In conclusion, our results in healthy subjects suggest that for dynamic visualization of collateral flow, 4D SSFP MRA should be preferably performed at 1.5 T rather than at 3 T. However, the higher image quality of peripheral segments of the posterior cerebral artery at 3 T indicate that 3 T might be superior to 1.5 T in assessment of vascular pathologies located peripherally in the brain (e.g. AVM), provided optimized positioning of the acquisition slab.

[2]

[3] [4]

[5]

[6]

[7]

[8]

[9]

[10]

[11]

[12]

[13]

[14]

[15]

[16]

References [17] [1] Hadizadeh DR, von Falkenhausen M, Gieseke J, et al. Cerebral arteriovenous malformation: Spetzler–Martin classification at subsecond-temporal-

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resolution four-dimensional MR angiography compared with that at DSA. Radiology 2008;246:205–13. Henderson RD, Eliasziw M, Fox AJ, Rothwell PM, Barnett HJ, for the North American Symptomatic Carotid Endarterectomy Trial (NASCET) Group. Angiographically defined collateral circulation and risk of stroke in patients with severe carotid artery stenosis. Stroke 2002;31:128–32. Liebeskind DS. Collateral circulation. Stroke 2003;34:2279–84. Kaufmann TJ, Huston III J, Mandrekar JN, Schleck CD, Thielen KR, Kallmes DF. Complications of diagnostic cerebral angiography: evaluation of 19,826 consecutive patients. Radiology 2007;243:812–9. Willinek WA, Hadizadeh DR, von Falkenhausen M, et al. 4D time-resolved MR angiography with keyhole (4D-TRAK): more than 60 times accelerated MRA using a combination of CENTRA, keyhole, and SENSE at 3.0 T. J Magn Reson Imaging 2008;27(6):1455–60. Grobner T. Gadolinium – a specific trigger for the development of nephrogenic systemic fibrosing dermopathy and nephrogenic systemic fibrosis? Nephrol Dial Transplant 2006;21:1104–8. Marckmann P, Skov L, Rossen K, et al. Nephrogenic systemic fibrosis: suspected causative role of gadodiamide used for contrast-enhanced magnetic resonance imaging. J Am Soc Nephrol 2006;17(9):2359–62. Bi X, Weale P, Schmitt P, Zuehlsdorff S, Jerecic R. Non-contrast-enhanced fourdimensional (4D) intracranial MR angiography: a feasibility study. Magn Reson Med 2010;63(3):835–41. Yan L, Wang S, Zhuo Y, et al. Unenhanced Dynamic MR angiography: high spatial and temporal resolution by using true FISP-based spin tagging with alternating radiofrequency. Radiology 2010;256(1):270–9. Hori M, Shiraga N, Watanabe Y, et al. Time-resolved three-dimensional magnetic resonance digital subtraction angiography without contrast material in the brain: initial investigation. J Magn Res Imaging 2009;30: 214–8. Kim SG. Quantification of relative cerebral blood flow change by flow-sensitive alternating inversion recovery (FAIR) technique: application to functional mapping. Magn Reson Med 1995;34(3):293–301. Bi X, Desphande V, Simonetti O, Laub G, Li D. Three-dimensional breathhold SSFP coronaty MRA: a comparison between 1.5 T and 3 T. J Magn Res Imaging 2005;22:206–12. Lanzman RS, Kröpil P, Schmitt P, et al. Nonenhanced ECG-gated time-resolved 4D Steady-state free precession (SSFP) MR angiography (MRA) for assessment of cerebral collateral flow: comparison with digital subtraction angiography (DSA). Eur Radiol 2011. Jan 12 [Epub ahead of print]. Edelman RR, Siewert B, Adamis M, Gaa J, Laub G, Wielopolski P. Signal targeting with alternating radiofrequency (STAR) sequences: application to MR angiography. Magn Res Med 1994;31:233–8. Schmitt P, Speier P, Bi X, Weale P, Müller E. Non-contrast-enhanced 4D intracranial MR angiography: optimizations using a variable flip angle approach. In: Proceedings of the 18th ISMRM Scientific Meeting. 2010. p. 402. Dietrich O, Raya JG, Reeder SB, Reiser MF, Schoenberg SO. Measurement of signal-to-noise ratios in MR images: influence of multichannel coils, parallel imaging and reconstruction filters. J Magn Reson Imaging 2007;26: 375–8. Heverhagen JT. Noise measurement and estimation in MR imaging experiments. Radiology 2007;245:638–9.