Accelerated dual-venc 4D flow MRI for neurovascular applications
Corresponding Author
Susanne Schnell PhD
Department of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA
Address reprint requests to: S.S., Department of Radiology, Northwestern University, 737 N. Michigan Ave., Ste. 1600, Chicago, IL 60611. E-mail: [email protected]Search for more papers by this authorSameer A. Ansari MD, PhD
Department of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA
Department of Neurosurgery, Northwestern University, Chicago, Illinois, USA
Search for more papers by this authorCan Wu PhD
Department of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA
Department of Biomedical Engineering, McCormick School of Engineering, Northwestern University, Chicago, Illinois, USA
Search for more papers by this authorJulio Garcia PhD
Department of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA
Department of Cardiac Sciences – Stephenson Cardiac Imaging Centre, Cumming School of Medicine, University of Calgary, Calgary, Canada
Search for more papers by this authorIan G. Murphy MD
Department of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA
Search for more papers by this authorOzair A. Rahman MD
Department of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA
Search for more papers by this authorAmir A. Rahsepar MD
Department of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA
Search for more papers by this authorMaria Aristova
Department of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA
Search for more papers by this authorJeremy D. Collins MD
Department of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA
Search for more papers by this authorJames C. Carr MD
Department of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA
Search for more papers by this authorMichael Markl PhD
Department of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA
Department of Neurosurgery, Northwestern University, Chicago, Illinois, USA
Search for more papers by this authorCorresponding Author
Susanne Schnell PhD
Department of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA
Address reprint requests to: S.S., Department of Radiology, Northwestern University, 737 N. Michigan Ave., Ste. 1600, Chicago, IL 60611. E-mail: [email protected]Search for more papers by this authorSameer A. Ansari MD, PhD
Department of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA
Department of Neurosurgery, Northwestern University, Chicago, Illinois, USA
Search for more papers by this authorCan Wu PhD
Department of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA
Department of Biomedical Engineering, McCormick School of Engineering, Northwestern University, Chicago, Illinois, USA
Search for more papers by this authorJulio Garcia PhD
Department of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA
Department of Cardiac Sciences – Stephenson Cardiac Imaging Centre, Cumming School of Medicine, University of Calgary, Calgary, Canada
Search for more papers by this authorIan G. Murphy MD
Department of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA
Search for more papers by this authorOzair A. Rahman MD
Department of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA
Search for more papers by this authorAmir A. Rahsepar MD
Department of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA
Search for more papers by this authorMaria Aristova
Department of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA
Search for more papers by this authorJeremy D. Collins MD
Department of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA
Search for more papers by this authorJames C. Carr MD
Department of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA
Search for more papers by this authorMichael Markl PhD
Department of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA
Department of Neurosurgery, Northwestern University, Chicago, Illinois, USA
Search for more papers by this authorAbstract
Purpose
To improve velocity-to-noise ratio (VNR) and dynamic velocity range of 4D flow magnetic resonance imaging (MRI) by using dual-velocity encoding (dual-venc) with k-t generalized autocalibrating partially parallel acquisition (GRAPPA) acceleration.
Materials and Methods
A dual-venc 4D flow MRI sequence with k-t GRAPPA acceleration was developed using a shared reference scan followed by three-directional low- and high-venc scans (repetition time / echo time / flip angle = 6.1 msec / 3.4 msec / 15°, temporal/spatial resolution = 43.0 msec/1.2 × 1.2 × 1.2 mm3). The high-venc data were used to correct for aliasing in the low-venc data, resulting in a single dataset with the favorable VNR of the low-venc but without velocity aliasing. The sequence was validated with a 3T MRI scanner in phantom experiments and applied in 16 volunteers to investigate its feasibility for assessing intracranial hemodynamics (net flow and peak velocity) at the major intracranial vessels. In addition, image quality and image noise were assessed in the in vivo acquisitions.
Results
All 4D flow MRI scans were acquired successfully with an acquisition time of 20 ± 4 minutes. The shared reference scan reduced the total acquisition time by 12.5% compared to two separate scans. Phantom experiments showed 51.4% reduced noise for dual-venc compared to high-venc and an excellent agreement of velocities (ρ = 0.8, P < 0.001). The volunteer data showed decreased noise in dual-venc data (54.6% lower) compared to high-venc, and improved image quality, as graded by two observers: fewer artifacts (P < 0.0001), improved vessel conspicuity (P < 0.0001), and reduced noise (P < 0.0001).
Conclusion
Dual-venc 4D flow MRI exhibits the superior VNR of the low-venc acquisition and reliably incorporates low- and high-velocity fields simultaneously. In vitro and in vivo data demonstrate improved flow visualization, image quality, and image noise.
Level of Evidence: 2
Technical Efficacy: Stage 1
J. MAGN. RESON. IMAGING 2017;46:102–114
Supporting Information
Additional Supporting Information may be found in the online version of this article.
| Filename | Description |
|---|---|
| jmri25595-sup-0001-suppinfo1.tif869.3 KB |
Supporting Figure S1: Trend plots for comparing the change of peak velocity depending on applied 4D flow method (left: high-venc, right: dual-venc) occurring at all measurement locations. ICA = internal carotid arteries, MCA = middle cerebral arteries, ACA = anterior cerebral arteries, PCA = posterior cerebral arteries, VA = vertebral arteries, BA = basilar artery, TS = transverse sinus, StrSin = straight sinus, SagSin = superior sagittal sinus. |
| jmri25595-sup-0002-suppinfo2.tif287.1 KB |
Supporting Figure S2: Trend plots for comparing the change of net flow depending on applied 4D flow method (left: high-venc, right: dual-venc) occurring at all measurement locations. ICA = internal carotid arteries, MCA = middle cerebral arteries, ACA = anterior cerebral arteries, PCA = posterior cerebral arteries, VA = vertebral arteries, BA = basilar artery, TS = transverse sinus, StrSin = straight sinus, SagSin = superior sagittal sinus. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- 1 Wu C, Schnell S, Markl M, Ansari SA. Combined DSA and 4D flow demonstrate overt alterations of vascular geometry and hemodynamics in an unusually complex cerebral AVM. Clin Neuroradiol 2016; 26: 471–475.
- 2 Wu C, Ansari SA, Honarmand AR, et al. Evaluation of 4D vascular flow and tissue perfusion in cerebral arteriovenous malformations: influence of Spetzler-Martin grade, clinical presentation, and AVM risk factors. AJNR Am J Neuroradiol 2015; 36: 1142–1149.
- 3 Markl M, Wu C, Hurley MC, et al. Cerebral arteriovenous malformation: complex 3D hemodynamics and 3D blood flow alterations during staged embolization. J Magn Reson Imaging 2013; 38: 946–950.
- 4 Schuchardt F, Schroeder L, Anastasopoulos C, et al. In vivo analysis of physiological 3D blood flow of cerebral veins. Eur Radiol 2015; 25: 2371–2380.
- 5 Harloff A, Zech T, Wegent F, Strecker C, Weiller C, Markl M. Comparison of blood flow velocity quantification by 4D flow MR imaging with ultrasound at the carotid bifurcation. AJNR Am J Neuroradiol 2013; 34: 1407–1413.
- 6 Hope TA, Hope MD, Purcell DD, et al. Evaluation of intracranial stenoses and aneurysms with accelerated 4D flow. Magn Reson Imaging 2010; 28: 41–46.
- 7 Boussel L, Rayz V, Martin A, et al. Phase-contrast magnetic resonance imaging measurements in intracranial aneurysms in vivo of flow patterns, velocity fields, and wall shear stress: comparison with computational fluid dynamics. Magn Reson Med 2009; 61: 409–417.
- 8 Schnell S, Ansari SA, Vakil P, et al. Three-dimensional hemodynamics in intracranial aneurysms: influence of size and morphology. J Magn Reson Imaging 2014; 39: 120–131.
- 9 Kecskemeti S, Johnson K, Wu Y, Mistretta C, Turski P, Wieben O. High resolution three-dimensional cine phase contrast MRI of small intracranial aneurysms using a stack of stars k-space trajectory. J Magn Reson Imaging 2012; 35: 518–527.
- 10 Isoda H, Ohkura Y, Kosugi T, et al. In vivo hemodynamic analysis of intracranial aneurysms obtained by magnetic resonance fluid dynamics (MRFD) based on time-resolved three-dimensional phase-contrast MRI. Neuroradiology 2010; 52: 921–928.
- 11 Hollnagel DI, Summers PE, Poulikakos D, Kollias SS. Comparative velocity investigations in cerebral arteries and aneurysms: 3D phase-contrast MR angiography, laser Doppler velocimetry and computational fluid dynamics. NMR Biomed 2009; 22: 795–808.
- 12 Lee AT, Pike GB, Pelc NJ. Three-point phase-contrast velocity measurements with increased velocity-to-noise ratio. Magn Reson Med 1995; 33: 122–126.
- 13 Markl M, Harloff A, Bley TA, et al. Time-resolved 3D MR velocity mapping at 3T: improved navigator-gated assessment of vascular anatomy and blood flow. J Magn Reson Imaging 2007; 25: 824–831.
- 14 Nett EJ, Johnson KM, Frydrychowicz A, et al. Four-dimensional phase contrast MRI with accelerated dual velocity encoding. J Magn Reson Imaging 2012; 35: 1462–1471.
- 15 Ha H, Kim GB, Kweon J, et al. Multi-VENC acquisition of four-dimensional phase-contrast MRI to improve precision of velocity field measurement. Magn Reson Med 2016; 75: 1909–1919.
- 16 Callaghan FM, Kozor R, Sherrah AG, et al. Use of multi-velocity encoding 4D flow MRI to improve quantification of flow patterns in the aorta. J Magn Reson Imaging 2016; 43: 352–363.
- 17 Johnson KM, Markl M. Improved SNR in phase contrast velocimetry with five-point balanced flow encoding. Magn Reson Med 2010; 63: 349–355.
- 18 Nilsson A, Bloch KM, Carlsson M, Heiberg E, Stahlberg F. Variable velocity encoding in a three-dimensional, three-directional phase contrast sequence: Evaluation in phantom and volunteers. J Magn Reson Imaging 2012; 36: 1450–1459.
- 19 Binter C, Knobloch V, Manka R, Sigfridsson A, Kozerke S. Bayesian multipoint velocity encoding for concurrent flow and turbulence mapping. Magn Reson Med 2013; 69: 1337–1345.
- 20 Knobloch V, Binter C, Gulan U, et al. Mapping mean and fluctuating velocities by Bayesian multipoint MR velocity encoding-validation against 3D particle tracking velocimetry. Magn Reson Med 2014; 71: 1405–1415.
- 21 Knobloch V, Binter C, Kurtcuoglu V, Kozerke S. Arterial, venous, and cerebrospinal fluid flow: simultaneous assessment with Bayesian multipoint velocity-encoded MR imaging. Radiology 2014; 270: 566–573.
- 22 Bernstein MA, Shimakawa A, Pelc NJ. Minimizing TE in moment-nulled or flow-encoded two- and three-dimensional gradient-echo imaging. J Magn Reson Imaging 1992; 2: 583–588.
- 23 Huang F, Akao J, Vijayakumar S, Duensing GR, Limkeman M. k-t GRAPPA: a k-space implementation for dynamic MRI with high reduction factor. Magn Reson Med 2005; 54: 1172–1184.
- 24 Jung B, Ullmann P, Honal M, Bauer S, Hennig J, Markl M. Parallel MRI with extended and averaged GRAPPA kernels (PEAK-GRAPPA): optimized spatiotemporal dynamic imaging. J Magn Reson Imaging 2008; 28: 1226–1232.
- 25 Jung B, Stalder AF, Bauer S, Markl M. On the undersampling strategies to accelerate time-resolved 3D imaging using k-t-GRAPPA. Magn Reson Med 2011; 66: 966–975.
- 26 Schnell S, Markl M, Entezari P, et al. k-t GRAPPA accelerated four-dimensional flow MRI in the aorta: effect on scan time, image quality, and quantification of flow and wall shear stress. Magn Reson Med 2014; 72: 522–533.
- 27 Bernstein MA, Zhou XJ, Polzin JA, et al. Concomitant gradient terms in phase contrast MR: analysis and correction. Magn Reson Med 1998; 39: 300–308.
- 28 Walker PG, Cranney GB, Scheidegger MB, Waseleski G, Pohost GM, Yoganathan AP. Semiautomated method for noise reduction and background phase error correction in MR phase velocity data. J Magn Reson Imaging 1993; 3: 521–530.
- 29 Bock JK, Hennig J, Markl M. Optimized pre-processing of time-resolved 2D and 3D phase contrast MRI data. Proceedings Scientific Meeting ISMRM, Berlin; 2007. p 3138.
- 30 Moran PR. A flow velocity zeugmatographic interlace for NMR imaging in humans. Magn Reson Imaging 1982; 1: 197–203.
- 31 Hardy CJ, Bolster BD Jr, McVeigh ER, Iben IE, Zerhouni EA. Pencil excitation with interleaved fourier velocity encoding: NMR measurement of aortic distensibility. Magn Reson Med 1996; 35: 814–819.
- 32 Macgowan CK, Liu GK, van Amerom JF, Sussman MS, Wright GA. Self-gated Fourier velocity encoding. Magn Reson Imaging 2010; 28: 95–102.
- 33 Swan JS, Weber DM, Grist TM, Wojtowycz MM, Korosec FR, Mistretta CA. Peripheral MR angiography with variable velocity encoding. Work in progress. Radiology 1992; 184: 813–817.
- 34 Bammer R, Hope TA, Aksoy M, Alley MT. Time-resolved 3D quantitative flow MRI of the major intracranial vessels: initial experience and comparative evaluation at 1.5T and 3.0T in combination with parallel imaging. Magn Reson Med 2007; 57: 127–140.
- 35 Wise RG, Newling B, Gates AR, Xing D, Carpenter TA, Hall LD. Measurement of pulsatile flow using MRI and a Bayesian technique of probability analysis. Magn Reson Imaging. 1996; 14: 173–185.
