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Published in: Current Cardiovascular Imaging Reports 4/2014

01-04-2014 | Molecular Imaging (G Strijkers, Section Editor)

Measuring Wall Shear Stress Using Velocity-Encoded MRI

Authors: Wouter V. Potters, Henk A. Marquering, Ed VanBavel, Aart J. Nederveen

Published in: Current Cardiovascular Imaging Reports | Issue 4/2014

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Abstract

This study reviews the application of velocity-encoded magnetic resonance imaging (MRI) for the calculation of wall shear stress (WSS). The basics of velocity-encoded MRI and WSS are reviewed and calculation methods for estimation of the WSS from 2D or 3D (cine) velocity-encoded MRI data are presented. In recent years, there has been a trend towards 3D WSS quantification methods. Current clinical applications of WSS are discussed, including an overview of estimated WSS magnitudes in different patient groups at multiple anatomical locations (aorta, carotid arteries, and intracranial aneurysms). A large variation was found between different WSS calculation methods. The future of MRI-based WSS calculations depends on its prognostic and diagnostic value, both of which need to be further explored in clinical studies. In this context, both further improvement of the quality of velocity-encoded MRI data and scan time reduction are pivotal.
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Literature
1.
go back to reference Peiffer V, Sherwin SJ, Weinberg PD. Does low and oscillatory wall shear stress correlate spatially with early atherosclerosis? a systematic review. Cardiovasc Res. 2013;99:242–50.PubMedCentralPubMed Peiffer V, Sherwin SJ, Weinberg PD. Does low and oscillatory wall shear stress correlate spatially with early atherosclerosis? a systematic review. Cardiovasc Res. 2013;99:242–50.PubMedCentralPubMed
2.
go back to reference Silber HA, Bluemke DA, Ouyang P, Du YP, Post WS, Lima JA. The relationship between vascular wall shear stress and flow-mediated dilation: endothelial function assessed by phase-contrast magnetic resonance angiography. J Amer Coll Cardiol. 2001;38:1859–65.CrossRef Silber HA, Bluemke DA, Ouyang P, Du YP, Post WS, Lima JA. The relationship between vascular wall shear stress and flow-mediated dilation: endothelial function assessed by phase-contrast magnetic resonance angiography. J Amer Coll Cardiol. 2001;38:1859–65.CrossRef
3.
go back to reference Silber HA, Ouyang P, Bluemke DA, Gupta SN, Foo TK, Lima JAC. Why is flow-mediated dilation dependent on arterial size? assessment of the shear stimulus using phase-contrast magnetic resonance imaging. Am J Physiol Heart Circ Physiol. 2005;288:H822–8.PubMedCrossRef Silber HA, Ouyang P, Bluemke DA, Gupta SN, Foo TK, Lima JAC. Why is flow-mediated dilation dependent on arterial size? assessment of the shear stimulus using phase-contrast magnetic resonance imaging. Am J Physiol Heart Circ Physiol. 2005;288:H822–8.PubMedCrossRef
4.
go back to reference Malek AM, Alper SL, Izumo S. Hemodynamic shear stress and its role in atherosclerosis. JAMA. 1999;282:2035–42.PubMedCrossRef Malek AM, Alper SL, Izumo S. Hemodynamic shear stress and its role in atherosclerosis. JAMA. 1999;282:2035–42.PubMedCrossRef
5.
go back to reference Silber HA, Ouyang P, Bluemke DA, Gupta SN, Foo TK, Lima JAC. A novel method for assessing arterial endothelial function using phase contrast magnetic resonance imaging: vasoconstriction during reduced shear. J Cardiovasc Magnet Reson. 2005;7:615–21.CrossRef Silber HA, Ouyang P, Bluemke DA, Gupta SN, Foo TK, Lima JAC. A novel method for assessing arterial endothelial function using phase contrast magnetic resonance imaging: vasoconstriction during reduced shear. J Cardiovasc Magnet Reson. 2005;7:615–21.CrossRef
6.
go back to reference Misra S, Fu AA, Misra KD, Glockner JF, Mukhopadyay D. Evolution of shear stress, protein expression, and vessel area in an animal model of arterial dilatation in hemodialysis grafts. J Vasc Interv Radiol. 2010;21:108–15.PubMedCentralPubMedCrossRef Misra S, Fu AA, Misra KD, Glockner JF, Mukhopadyay D. Evolution of shear stress, protein expression, and vessel area in an animal model of arterial dilatation in hemodialysis grafts. J Vasc Interv Radiol. 2010;21:108–15.PubMedCentralPubMedCrossRef
7.
go back to reference Duivenvoorden R, van Bavel E, de Groot E, Stroes ESG, Disselhorst JA, Hutten BA, et al. Endothelial shear stress: a critical determinant of arterial remodeling and arterial stiffness in humans—a carotid 3.0-T MRI study. Circ: Cardiovasc Imaging. 2010;3:578–85. Duivenvoorden R, van Bavel E, de Groot E, Stroes ESG, Disselhorst JA, Hutten BA, et al. Endothelial shear stress: a critical determinant of arterial remodeling and arterial stiffness in humans—a carotid 3.0-T MRI study. Circ: Cardiovasc Imaging. 2010;3:578–85.
8.
go back to reference Wentzel JJ, Corti R, Fayad ZA, Wisdom P, Macaluso F, Winkelman MO, et al. Does shear stress modulate both plaque progression and regression in the thoracic aorta? human study using serial magnetic resonance imaging. J Amer Coll Cardiol. 2005;45:846–54.CrossRef Wentzel JJ, Corti R, Fayad ZA, Wisdom P, Macaluso F, Winkelman MO, et al. Does shear stress modulate both plaque progression and regression in the thoracic aorta? human study using serial magnetic resonance imaging. J Amer Coll Cardiol. 2005;45:846–54.CrossRef
9.
go back to reference Wu S, Ringgaard S, Pedersen EM. Three-dimensional phase contrast velocity mapping acquisition improves wall shear stress estimation in vivo. Magn Reson Imaging. 2004;22:345–51.PubMedCrossRef Wu S, Ringgaard S, Pedersen EM. Three-dimensional phase contrast velocity mapping acquisition improves wall shear stress estimation in vivo. Magn Reson Imaging. 2004;22:345–51.PubMedCrossRef
10.
go back to reference Greve JM, Les AS, Tang BT, Draney-Blomme MT, Wilson NM, Dalman RL, et al. Allometric scaling of wall shear stress from mice to humans: quantification using cine phase-contrast MRI and computational fluid dynamics. Am J Physiol Heart Circ Physiol. 2006;291:H1700–8.PubMedCrossRef Greve JM, Les AS, Tang BT, Draney-Blomme MT, Wilson NM, Dalman RL, et al. Allometric scaling of wall shear stress from mice to humans: quantification using cine phase-contrast MRI and computational fluid dynamics. Am J Physiol Heart Circ Physiol. 2006;291:H1700–8.PubMedCrossRef
11.
go back to reference Pantos I, Patatoukas G, Efstathopoulos EP, Katritsis D. In vivo wall shear stress measurements using phase-contrast MRI. Expert Rev Cardiovasc Ther. 2007;5:927–38.PubMedCrossRef Pantos I, Patatoukas G, Efstathopoulos EP, Katritsis D. In vivo wall shear stress measurements using phase-contrast MRI. Expert Rev Cardiovasc Ther. 2007;5:927–38.PubMedCrossRef
12.
go back to reference Haacke EM, Brown RW, Thompson MR, Venkatesan R. Magnetic Resonance Imaging: Physical Principles and Sequence Design, 1st Ed. John Wiley & Sons Inc. New York, USA; 1999. Haacke EM, Brown RW, Thompson MR, Venkatesan R. Magnetic Resonance Imaging: Physical Principles and Sequence Design, 1st Ed. John Wiley & Sons Inc. New York, USA; 1999.
13.
go back to reference Lotz J, Meier C, Leppert A. Cardiovascular flow measurement with phase-contrast MR imaging: basic facts and implementation. Radiographics. 2002;22:651–71. Lotz J, Meier C, Leppert A. Cardiovascular flow measurement with phase-contrast MR imaging: basic facts and implementation. Radiographics. 2002;22:651–71.
14.
go back to reference Frydrychowicz A, François CJ, Turski PA. Four-dimensional phase contrast magnetic resonance angiography: potential clinical applications. Eur J Radiol. 2011;80:24–35.PubMedCentralPubMedCrossRef Frydrychowicz A, François CJ, Turski PA. Four-dimensional phase contrast magnetic resonance angiography: potential clinical applications. Eur J Radiol. 2011;80:24–35.PubMedCentralPubMedCrossRef
15.
go back to reference Markl M, Frydrychowicz A, Kozerke S, Hope M, Wieben O. 4D flow MRI. J Magn Reson Imaging. 2012;36:1015–36.PubMedCrossRef Markl M, Frydrychowicz A, Kozerke S, Hope M, Wieben O. 4D flow MRI. J Magn Reson Imaging. 2012;36:1015–36.PubMedCrossRef
16.
go back to reference Hope MD, Sedlic T, Dyverfeldt P. Cardiothoracic magnetic resonance flow imaging. J Thorac Imaging. 2013;28:217–30.PubMedCrossRef Hope MD, Sedlic T, Dyverfeldt P. Cardiothoracic magnetic resonance flow imaging. J Thorac Imaging. 2013;28:217–30.PubMedCrossRef
17.
go back to reference Pelc NJ, Herfkens RJ, Shimakawa A, Enzmann DR. Phase contrast cine magnetic resonance imaging. Magn Reson Q. 1991;7:229–54.PubMed Pelc NJ, Herfkens RJ, Shimakawa A, Enzmann DR. Phase contrast cine magnetic resonance imaging. Magn Reson Q. 1991;7:229–54.PubMed
18.
go back to reference Bernstein MA, Zhou XJ, Polzin JA, King KF, Ganin A, Pelc NJ, et al. Concomitant gradient terms in phase contrast MR: analysis and correction. Magn Reson Med. 1998;39:300–8.PubMedCrossRef Bernstein MA, Zhou XJ, Polzin JA, King KF, Ganin A, Pelc NJ, et al. Concomitant gradient terms in phase contrast MR: analysis and correction. Magn Reson Med. 1998;39:300–8.PubMedCrossRef
19.
go back to reference Lorenz R, Bock J, Snyder J, Korvink JG, Jung BA, Markl M. Influence of eddy current, Maxwell and gradient field corrections on 3D flow visualization of 3D CINE PC-MRI data. Magn Reson Med. 2013;1–12. doi:10.1002/mrm.24802. Lorenz R, Bock J, Snyder J, Korvink JG, Jung BA, Markl M. Influence of eddy current, Maxwell and gradient field corrections on 3D flow visualization of 3D CINE PC-MRI data. Magn Reson Med. 2013;1–12. doi:10.​1002/​mrm.​24802.
20.
go back to reference O'Brien KR, Cowan BR, Jain M, Stewart RAH, Kerr AJ, Young AA. MRI phase contrast velocity and flow errors in turbulent stenotic jets. J Magn Reson Imaging. 2008;28:210–8.PubMedCrossRef O'Brien KR, Cowan BR, Jain M, Stewart RAH, Kerr AJ, Young AA. MRI phase contrast velocity and flow errors in turbulent stenotic jets. J Magn Reson Imaging. 2008;28:210–8.PubMedCrossRef
21.•
go back to reference Knobloch V, Boesiger P, Kozerke S. Sparsity transforms k-t principal component analysis for accelerating cine three-dimensional flow measurements. 2013;70:53–63. This paper shows how redundancy in the k-t-domain can be used to significantly improve the scanning times without loss of quality; an essential step towards future clinical use of 3D velocity-encoded MRI for 3D WSS quantification. Knobloch V, Boesiger P, Kozerke S. Sparsity transforms k-t principal component analysis for accelerating cine three-dimensional flow measurements. 2013;70:53–63. This paper shows how redundancy in the k-t-domain can be used to significantly improve the scanning times without loss of quality; an essential step towards future clinical use of 3D velocity-encoded MRI for 3D WSS quantification.
22.•
go back to reference Schnell S, Markl M, Entezari P, Mahadewia RJ, Semaan E, Stankovic Z, 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. 2013;1–12. doi:10.1002/mrm.24925. This paper shows how redundancy in the k-t-domain can be used to significantly improve the scanning times without loss of quality; an essential step towards future clinical use of 3D velocity-encoded MRI for 3D WSS quantification. Schnell S, Markl M, Entezari P, Mahadewia RJ, Semaan E, Stankovic Z, 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. 2013;1–12. doi:10.​1002/​mrm.​24925. This paper shows how redundancy in the k-t-domain can be used to significantly improve the scanning times without loss of quality; an essential step towards future clinical use of 3D velocity-encoded MRI for 3D WSS quantification.
23.
go back to reference Mutsaerts HJMM, Palm-Meinders IH, de Craen AJM, Reiber JHC, Blauw GJ, van Buchem MA, et al. Diastolic carotid artery wall shear stress is associated with cerebral infarcts and periventricular white matter lesions. Stroke. 2011;42:3497–501.PubMedCrossRef Mutsaerts HJMM, Palm-Meinders IH, de Craen AJM, Reiber JHC, Blauw GJ, van Buchem MA, et al. Diastolic carotid artery wall shear stress is associated with cerebral infarcts and periventricular white matter lesions. Stroke. 2011;42:3497–501.PubMedCrossRef
24.
25.
go back to reference Avril S, Huntley JM, Cusack R. In vivo measurements of blood viscosity and wall stiffness in the carotid using PC-MRI. Eur J Computation Mech. 2009;18:9–20. Avril S, Huntley JM, Cusack R. In vivo measurements of blood viscosity and wall stiffness in the carotid using PC-MRI. Eur J Computation Mech. 2009;18:9–20.
26.
go back to reference Misra S, Woodrum DA, Homburger J, Elkouri S, Mandrekar JN, Barocas V, et al. Assessment of wall shear stress changes in arteries and veins of arteriovenous polytetrafluoroethylene grafts using magnetic resonance imaging. Cardiovasc Intervent Radiol. 2006;29:624–9.PubMedCrossRef Misra S, Woodrum DA, Homburger J, Elkouri S, Mandrekar JN, Barocas V, et al. Assessment of wall shear stress changes in arteries and veins of arteriovenous polytetrafluoroethylene grafts using magnetic resonance imaging. Cardiovasc Intervent Radiol. 2006;29:624–9.PubMedCrossRef
27.
go back to reference Oshinski JN, Curtin JL, Loth F. Mean-average wall shear stress measurements in the common carotid artery. J Cardiovasc Magnet Reson. 2006;8:717–22.CrossRef Oshinski JN, Curtin JL, Loth F. Mean-average wall shear stress measurements in the common carotid artery. J Cardiovasc Magnet Reson. 2006;8:717–22.CrossRef
28.
go back to reference Box FMA, van der Geest RJ, van der Grond J, van Osch MJP, Zwinderman AH, Palm-Meinders NH, et al. Reproducibility of wall shear stress assessment with the paraboloid method in the internal carotid artery with velocity encoded MRI in healthy young individuals. J Magn Reson Imaging. 2007;26:598–605.PubMedCrossRef Box FMA, van der Geest RJ, van der Grond J, van Osch MJP, Zwinderman AH, Palm-Meinders NH, et al. Reproducibility of wall shear stress assessment with the paraboloid method in the internal carotid artery with velocity encoded MRI in healthy young individuals. J Magn Reson Imaging. 2007;26:598–605.PubMedCrossRef
29.
go back to reference van Es ACGM, van der Flier WM, Box FMA, Middelkoop HAM, Westendorp RGJ, van Buchem MA, et al. Carotid and basilar artery wall shear stress in Alzheimer's disease and mild cognitive impairment. Dement Geriatr Cogn Disord. 2009;28:220–4.PubMedCrossRef van Es ACGM, van der Flier WM, Box FMA, Middelkoop HAM, Westendorp RGJ, van Buchem MA, et al. Carotid and basilar artery wall shear stress in Alzheimer's disease and mild cognitive impairment. Dement Geriatr Cogn Disord. 2009;28:220–4.PubMedCrossRef
30.
go back to reference Oshinski JN, Ku DN, Mukundan SJ, Loth F, Pettigrew RI. Determination of wall shear stress in the aorta with the use of MR phase velocity mapping. J Magn Reson Imaging. 1995;5:640–7.PubMedCrossRef Oshinski JN, Ku DN, Mukundan SJ, Loth F, Pettigrew RI. Determination of wall shear stress in the aorta with the use of MR phase velocity mapping. J Magn Reson Imaging. 1995;5:640–7.PubMedCrossRef
31.
go back to reference Oyre S, Pedersen EM, Ringgaard S, Boesiger P, Paaske WP. In vivo wall shear stress measured by magnetic resonance velocity mapping in the normal human abdominal aorta. Eur J Vasc Endovasc Surg. 1997;13:263–71.PubMedCrossRef Oyre S, Pedersen EM, Ringgaard S, Boesiger P, Paaske WP. In vivo wall shear stress measured by magnetic resonance velocity mapping in the normal human abdominal aorta. Eur J Vasc Endovasc Surg. 1997;13:263–71.PubMedCrossRef
32.
go back to reference Masaryk AM, Frayne R, Unal O, Krupinski E, Strother CM. In vitro and in vivo comparison of three MR measurement methods for calculating vascular shear stress in the internal carotid artery. Am J Neuroradiol. 1999;20:237–45.PubMed Masaryk AM, Frayne R, Unal O, Krupinski E, Strother CM. In vitro and in vivo comparison of three MR measurement methods for calculating vascular shear stress in the internal carotid artery. Am J Neuroradiol. 1999;20:237–45.PubMed
33.
go back to reference Cheng CP, Parker D, Taylor CA. Quantification of wall shear stress in large blood vessels using Lagrangian interpolation functions with cine phase-contrast magnetic resonance imaging. Ann Biomed Eng. 2002;30:1020–32.PubMedCrossRef Cheng CP, Parker D, Taylor CA. Quantification of wall shear stress in large blood vessels using Lagrangian interpolation functions with cine phase-contrast magnetic resonance imaging. Ann Biomed Eng. 2002;30:1020–32.PubMedCrossRef
34.
go back to reference Gelfand BD, Epstein FH, Blackman BR. Spatial and spectral heterogeneity of time-varying shear stress profiles in the carotid bifurcation by phase-contrast MRI. J Magn Reson Imaging. 2006;24:1386–92.PubMedCrossRef Gelfand BD, Epstein FH, Blackman BR. Spatial and spectral heterogeneity of time-varying shear stress profiles in the carotid bifurcation by phase-contrast MRI. J Magn Reson Imaging. 2006;24:1386–92.PubMedCrossRef
35.
go back to reference Ahn S, Shin D, Tateshima S, Tanishita K, Vinuela F, Sinha S. Fluid-induced wall shear stress in anthropomorphic brain aneurysm models: MR phase-contrast study at 3T. J Magn Reson Imaging. 2007;25:1120–30.PubMedCrossRef Ahn S, Shin D, Tateshima S, Tanishita K, Vinuela F, Sinha S. Fluid-induced wall shear stress in anthropomorphic brain aneurysm models: MR phase-contrast study at 3T. J Magn Reson Imaging. 2007;25:1120–30.PubMedCrossRef
36.
go back to reference Womersley JR. Method for the calculation of velocity, rate of flow and viscous drag in arteries when the pressure gradient is known. J Physiol Lond. 1955;127:553–63.PubMedCentralPubMed Womersley JR. Method for the calculation of velocity, rate of flow and viscous drag in arteries when the pressure gradient is known. J Physiol Lond. 1955;127:553–63.PubMedCentralPubMed
37.
go back to reference Oyre S, Ringgaard S, Kozerke S, Paaske WP, Erlandsen M, Boesiger P, et al. Accurate noninvasive quantitation of blood flow, cross-sectional lumen vessel area and wall shear stress by three-dimensional paraboloid modeling of magnetic resonance imaging velocity data. J Amer Coll Cardiol. 1998;32:128–34.CrossRef Oyre S, Ringgaard S, Kozerke S, Paaske WP, Erlandsen M, Boesiger P, et al. Accurate noninvasive quantitation of blood flow, cross-sectional lumen vessel area and wall shear stress by three-dimensional paraboloid modeling of magnetic resonance imaging velocity data. J Amer Coll Cardiol. 1998;32:128–34.CrossRef
38.
go back to reference Oyre S, Paaske WPW, Ringgaard SS, Kozerke SS, Erlandsen MM, Boesiger PP, et al. Automatic accurate non-invasive quantitation of blood flow, cross-sectional vessel area, and wall shear stress by modelling of magnetic resonance velocity data. Eur J Vasc Endovasc Surg. 1998;16:517–24.PubMedCrossRef Oyre S, Paaske WPW, Ringgaard SS, Kozerke SS, Erlandsen MM, Boesiger PP, et al. Automatic accurate non-invasive quantitation of blood flow, cross-sectional vessel area, and wall shear stress by modelling of magnetic resonance velocity data. Eur J Vasc Endovasc Surg. 1998;16:517–24.PubMedCrossRef
39.
go back to reference Oyre S, Ringgaard SS, Kozerke SS, Paaske WPW, Scheidegger MBM, Boesiger PP, et al. Quantitation of circumferential subpixel vessel wall position and wall shear stress by multiple sectored three-dimensional paraboloid modeling of velocity encoded cine MR. Magn Reson Med. 1998;40:645–55.PubMedCrossRef Oyre S, Ringgaard SS, Kozerke SS, Paaske WPW, Scheidegger MBM, Boesiger PP, et al. Quantitation of circumferential subpixel vessel wall position and wall shear stress by multiple sectored three-dimensional paraboloid modeling of velocity encoded cine MR. Magn Reson Med. 1998;40:645–55.PubMedCrossRef
40.
go back to reference Potters WV, van Ooij P, Marquering HA, vanBavel E, Nederveen AJ. Volumetric arterial wall shear stress calculation based on cine phase contrast MRI. J Magn Reson Imaging. 2013;1–12. [In press]. Potters WV, van Ooij P, Marquering HA, vanBavel E, Nederveen AJ. Volumetric arterial wall shear stress calculation based on cine phase contrast MRI. J Magn Reson Imaging. 2013;1–12. [In press].
41.
go back to reference Petersson S, Dyverfeldt P, Ebbers T. Assessment of the accuracy of MRI wall shear stress estimation using numerical simulations. J Magn Reson Imaging. 2012;36:128–38.PubMedCrossRef Petersson S, Dyverfeldt P, Ebbers T. Assessment of the accuracy of MRI wall shear stress estimation using numerical simulations. J Magn Reson Imaging. 2012;36:128–38.PubMedCrossRef
42.
go back to reference Pipe JG. A simple measure of flow disorder and wall shear stress in phase contrast MRI. Magn Reson Med. 2003;49:543–50.PubMedCrossRef Pipe JG. A simple measure of flow disorder and wall shear stress in phase contrast MRI. Magn Reson Med. 2003;49:543–50.PubMedCrossRef
43.
go back to reference Dyverfeldt P, Sigfridsson A, Kvitting JPE, Ebbers T. Quantification of intravoxel velocity standard deviation and turbulence intensity by generalizing phase‐contrast MRI. Magn Reson Med. 2006;56:850–8.PubMedCrossRef Dyverfeldt P, Sigfridsson A, Kvitting JPE, Ebbers T. Quantification of intravoxel velocity standard deviation and turbulence intensity by generalizing phase‐contrast MRI. Magn Reson Med. 2006;56:850–8.PubMedCrossRef
44.
go back to reference Dyverfeldt P, Kvitting JPE, Sigfridsson A, Engvall J, Bolger AF, Ebbers T. Assessment of fluctuating velocities in disturbed cardiovascular blood flow: in vivo feasibility of generalized phase-contrast MRI. J Magn Reson Imaging. 2008;28:655–63.PubMedCrossRef Dyverfeldt P, Kvitting JPE, Sigfridsson A, Engvall J, Bolger AF, Ebbers T. Assessment of fluctuating velocities in disturbed cardiovascular blood flow: in vivo feasibility of generalized phase-contrast MRI. J Magn Reson Imaging. 2008;28:655–63.PubMedCrossRef
45.
go back to reference Carvalho JLA, Nielsen J-F, Nayak KS. Feasibility of in vivo measurement of carotid wall shear rate using spiral fourier velocity encoded MRI. Magn Reson Med. 2010;63:1537–47.PubMedCrossRef Carvalho JLA, Nielsen J-F, Nayak KS. Feasibility of in vivo measurement of carotid wall shear rate using spiral fourier velocity encoded MRI. Magn Reson Med. 2010;63:1537–47.PubMedCrossRef
46.
go back to reference Köhler U, Marshall I, Robertson MB, Long Q, Xu XY, Hoskins PR. MRI measurement of wall shear stress vectors in bifurcation models and comparison with CFD predictions. J Magn Reson Imaging. 2001;14:563–73. Köhler U, Marshall I, Robertson MB, Long Q, Xu XY, Hoskins PR. MRI measurement of wall shear stress vectors in bifurcation models and comparison with CFD predictions. J Magn Reson Imaging. 2001;14:563–73.
47.
go back to reference Papathanasopoulou P, Zhao S, Kohler U, Robertson MB, Long Q, Hoskins P, et al. MRI measurement of time-resolved wall shear stress vectors in a carotid bifurcation model, and comparison with CFD predictions. J Magn Reson Imaging. 2003;17:153–62.PubMedCrossRef Papathanasopoulou P, Zhao S, Kohler U, Robertson MB, Long Q, Hoskins P, et al. MRI measurement of time-resolved wall shear stress vectors in a carotid bifurcation model, and comparison with CFD predictions. J Magn Reson Imaging. 2003;17:153–62.PubMedCrossRef
48.
go back to reference Stalder AF, Russe MF, Frydrychowicz A, Bock J, Hennig J, Markl M. Quantitative 2D and 3D phase contrast MRI: optimized analysis of blood flow and vessel wall parameters. Magn Reson Med. 2008;60:1218–31.PubMedCrossRef Stalder AF, Russe MF, Frydrychowicz A, Bock J, Hennig J, Markl M. Quantitative 2D and 3D phase contrast MRI: optimized analysis of blood flow and vessel wall parameters. Magn Reson Med. 2008;60:1218–31.PubMedCrossRef
49.••
go back to reference Markl M, Wallis W, Harloff A. Reproducibility of flow and wall shear stress analysis using flow-sensitive four-dimensional MRI. J Magn Reson Imaging. 2011;33:988–94. This paper shows, for the first time, that 3D WSS quantification based on 3D cine velocity-encoded MRI is reproducible.PubMedCrossRef Markl M, Wallis W, Harloff A. Reproducibility of flow and wall shear stress analysis using flow-sensitive four-dimensional MRI. J Magn Reson Imaging. 2011;33:988–94. This paper shows, for the first time, that 3D WSS quantification based on 3D cine velocity-encoded MRI is reproducible.PubMedCrossRef
50.
go back to reference Boussel L, Rayz V, Martin A, Acevedo-Bolton G, Lawton MT, Higashida R, 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;61:409–17.PubMedCentralPubMedCrossRef Boussel L, Rayz V, Martin A, Acevedo-Bolton G, Lawton MT, Higashida R, 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;61:409–17.PubMedCentralPubMedCrossRef
51.•
go back to reference Bieging ET, Frydrychowicz A, Wentland A, Landgraf BR, Johnson KM, Wieben O, et al. In vivo 3-dimensional magnetic resonance wall shear stress estimation in ascending aortic dilatation. J Magn Reson Imaging. 2011;33:589–97.PubMedCrossRef Bieging ET, Frydrychowicz A, Wentland A, Landgraf BR, Johnson KM, Wieben O, et al. In vivo 3-dimensional magnetic resonance wall shear stress estimation in ascending aortic dilatation. J Magn Reson Imaging. 2011;33:589–97.PubMedCrossRef
52.•
go back to reference van Ooij P, Potters WV, Guédon A, Schneiders JJ, Marquering HA, Majoie CB, et al. Wall shear stress estimated with phase contrast MRI in an in vitro and in vivo intracranial aneurysm. J Magn Reson Imaging. 2013;38:876–84. This paper shows that volumetric WSS in complex flow geometries are comparable with CFD simulations. van Ooij P, Potters WV, Guédon A, Schneiders JJ, Marquering HA, Majoie CB, et al. Wall shear stress estimated with phase contrast MRI in an in vitro and in vivo intracranial aneurysm. J Magn Reson Imaging. 2013;38:876–84. This paper shows that volumetric WSS in complex flow geometries are comparable with CFD simulations.
53.
go back to reference Frydrychowicz A, Markl M. Letter by frydrychowicz and markl regarding article, “association between aneurysm shoulder stress and abdominal aortic aneurysm expansion: a longitudinal follow-Up study. Circulation. 2011;123:e643.PubMedCrossRef Frydrychowicz A, Markl M. Letter by frydrychowicz and markl regarding article, “association between aneurysm shoulder stress and abdominal aortic aneurysm expansion: a longitudinal follow-Up study. Circulation. 2011;123:e643.PubMedCrossRef
54.
go back to reference Hope MD, Hope TA, Crook SES, Ordovas KG, Urbania TH, Alley MT, et al. Four-D flow CMR in assessment of valve-related ascending aortic disease. JACC Cardiovasc Imaging. 2011;4:781–7.PubMedCrossRef Hope MD, Hope TA, Crook SES, Ordovas KG, Urbania TH, Alley MT, et al. Four-D flow CMR in assessment of valve-related ascending aortic disease. JACC Cardiovasc Imaging. 2011;4:781–7.PubMedCrossRef
55.
go back to reference Strecker C, Harloff A, Wallis W, Markl M. Flow-sensitive 4D MRI of the thoracic aorta: comparison of image quality, quantitative flow, and wall parameters at 1.5T and 3T. J Magn Reson Imaging. 2012;236:1097–103.CrossRef Strecker C, Harloff A, Wallis W, Markl M. Flow-sensitive 4D MRI of the thoracic aorta: comparison of image quality, quantitative flow, and wall parameters at 1.5T and 3T. J Magn Reson Imaging. 2012;236:1097–103.CrossRef
56.
go back to reference Cheng C, Helderman F, Tempel D, Segers D, Hierck B, Poelmann R, et al. Large variations in absolute wall shear stress levels within one species and between species. Atherosclerosis. 2007;195:225–35.PubMedCrossRef Cheng C, Helderman F, Tempel D, Segers D, Hierck B, Poelmann R, et al. Large variations in absolute wall shear stress levels within one species and between species. Atherosclerosis. 2007;195:225–35.PubMedCrossRef
57.
go back to reference Misra S, Fu AA, Misra KD, Glockner JF, Mukhopadhyay D. Wall shear stress measurement using phase contrast magnetic resonance imaging with phase contrast magnetic resonance angiography in arteriovenous polytetrafluoroethylene grafts. Angiology. 2009;60:441–7.PubMedCrossRef Misra S, Fu AA, Misra KD, Glockner JF, Mukhopadhyay D. Wall shear stress measurement using phase contrast magnetic resonance imaging with phase contrast magnetic resonance angiography in arteriovenous polytetrafluoroethylene grafts. Angiology. 2009;60:441–7.PubMedCrossRef
58.
go back to reference van Bochove GS, Straathof R, Krams R, Nicolay K, Strijkers GJ. MRI-determined carotid artery flow velocities and wall shear stress in a mouse model of vulnerable and stable atherosclerotic plaque. Magma. 2010;23:77–84.PubMedCrossRef van Bochove GS, Straathof R, Krams R, Nicolay K, Strijkers GJ. MRI-determined carotid artery flow velocities and wall shear stress in a mouse model of vulnerable and stable atherosclerotic plaque. Magma. 2010;23:77–84.PubMedCrossRef
59.
go back to reference Janiczek RL, Blackman BR, Roy RJ, Meyer CH, Acton ST, Epstein FH. Three-dimensional phase contrast angiography of the mouse aortic arch using spiral MRI. Magn Reson Med. 2011;66:1382–90.PubMedCentralPubMedCrossRef Janiczek RL, Blackman BR, Roy RJ, Meyer CH, Acton ST, Epstein FH. Three-dimensional phase contrast angiography of the mouse aortic arch using spiral MRI. Magn Reson Med. 2011;66:1382–90.PubMedCentralPubMedCrossRef
60.
go back to reference Geiger J, Arnold R, Herzer L, Hirtler D, Stankovic Z, Russe M, et al. Aortic wall shear stress in Marfan syndrome. Magn Reson Med. 2012;70:1137–44. Geiger J, Arnold R, Herzer L, Hirtler D, Stankovic Z, Russe M, et al. Aortic wall shear stress in Marfan syndrome. Magn Reson Med. 2012;70:1137–44.
61.••
go back to reference Barker AJ, Markl M, Bürk J, Lorenz R, Bock J, Bauer S, et al. Bicuspid aortic valve is associated with altered wall shear stress in the ascending aorta. Circ: Cardiovasc Imaging. 2012;5:457–66. This paper shows significantly elevated WSS patterns in the ascending aorta of patients, independent of stenosis severity. Barker AJ, Markl M, Bürk J, Lorenz R, Bock J, Bauer S, et al. Bicuspid aortic valve is associated with altered wall shear stress in the ascending aorta. Circ: Cardiovasc Imaging. 2012;5:457–66. This paper shows significantly elevated WSS patterns in the ascending aorta of patients, independent of stenosis severity.
62.
go back to reference Bürk J, Blanke P, Stankovic Z, Barker A, Russe M, Geiger J, et al. Evaluation of 3D blood flow patterns and wall shear stress in the normal and dilated thoracic aorta using flow-sensitive 4D CMR. J Cardiovasc Magnet Reson. 2012;14:988–94. Bürk J, Blanke P, Stankovic Z, Barker A, Russe M, Geiger J, et al. Evaluation of 3D blood flow patterns and wall shear stress in the normal and dilated thoracic aorta using flow-sensitive 4D CMR. J Cardiovasc Magnet Reson. 2012;14:988–94.
63.
go back to reference Frydrychowicz A, Markl M, Hirtler D, Harloff A, Schlensak C, Geiger J, et al. Aortic hemodynamics in patients with and without repair of aortic coarctation: in vivo analysis by 4D flow-sensitive magnetic resonance imaging. Invest Radiol. 2011;46:317–25.PubMed Frydrychowicz A, Markl M, Hirtler D, Harloff A, Schlensak C, Geiger J, et al. Aortic hemodynamics in patients with and without repair of aortic coarctation: in vivo analysis by 4D flow-sensitive magnetic resonance imaging. Invest Radiol. 2011;46:317–25.PubMed
64.
go back to reference Hope TA, Kvitting JPE, Hope MD, Miller DC, Markl M, Herfkens RJ. Evaluation of Marfan patients’ status post valve-sparing aortic root replacement with 4D flow. Magn Reson Imaging. 2013;31:1479–84. Hope TA, Kvitting JPE, Hope MD, Miller DC, Markl M, Herfkens RJ. Evaluation of Marfan patients’ status post valve-sparing aortic root replacement with 4D flow. Magn Reson Imaging. 2013;31:1479–84.
65.
go back to reference Markl M, Brendecke SM, Simon J, Barker AJ, Weiller C, Harloff A. Co-registration of the distribution of wall shear stress and 140 complex plaques of the aorta. Magn Reson Imaging. 2013;31:1156–62.PubMedCrossRef Markl M, Brendecke SM, Simon J, Barker AJ, Weiller C, Harloff A. Co-registration of the distribution of wall shear stress and 140 complex plaques of the aorta. Magn Reson Imaging. 2013;31:1156–62.PubMedCrossRef
66.
go back to reference Barker AJ, Lanning C, Shandas R. Quantification of hemodynamic wall shear stress in patients with bicuspid aortic valve using phase-contrast MRI. Ann Biomed Eng. 2010;38:788–800.PubMedCentralPubMedCrossRef Barker AJ, Lanning C, Shandas R. Quantification of hemodynamic wall shear stress in patients with bicuspid aortic valve using phase-contrast MRI. Ann Biomed Eng. 2010;38:788–800.PubMedCentralPubMedCrossRef
67.
go back to reference Cheng CP, Herfkens RJ, Taylor CA. Inferior vena caval hemodynamics quantified in vivo at rest and during cycling exercise using magnetic resonance imaging. Am J Physiol Heart Circ Physiol. 2003;284:H1161–7.PubMed Cheng CP, Herfkens RJ, Taylor CA. Inferior vena caval hemodynamics quantified in vivo at rest and during cycling exercise using magnetic resonance imaging. Am J Physiol Heart Circ Physiol. 2003;284:H1161–7.PubMed
68.
go back to reference Efstathopoulos EP, Patatoukas G, Pantos I, Benekos O, Katritsis D, Kelekis NL. Measurement of systolic and diastolic arterial wall shear stress in the ascending aorta. Phys Med. 2008;24:196–203.PubMedCrossRef Efstathopoulos EP, Patatoukas G, Pantos I, Benekos O, Katritsis D, Kelekis NL. Measurement of systolic and diastolic arterial wall shear stress in the ascending aorta. Phys Med. 2008;24:196–203.PubMedCrossRef
69.
go back to reference Efstathopoulos EP, Patatoukas G, Pantos I, Benekos O, Katritsis D, Kelekis NL. Wall shear stress calculation in ascending aorta using phase contrast magnetic resonance imaging. Investigating effective ways to calculate it in clinical practice. Phys Med. 2008;24:175–81.PubMedCrossRef Efstathopoulos EP, Patatoukas G, Pantos I, Benekos O, Katritsis D, Kelekis NL. Wall shear stress calculation in ascending aorta using phase contrast magnetic resonance imaging. Investigating effective ways to calculate it in clinical practice. Phys Med. 2008;24:175–81.PubMedCrossRef
70.
go back to reference Frydrychowicz A, Arnold R, Hirtler D, Schlensak C, Stalder AF, Hennig J, et al. Multidirectional flow analysis by cardiovascular magnetic resonance in aneurysm development following repair of aortic coarctation. J Cardiovasc Magnet Reson. 2008;10:30.CrossRef Frydrychowicz A, Arnold R, Hirtler D, Schlensak C, Stalder AF, Hennig J, et al. Multidirectional flow analysis by cardiovascular magnetic resonance in aneurysm development following repair of aortic coarctation. J Cardiovasc Magnet Reson. 2008;10:30.CrossRef
71.
go back to reference Wu S, Ringgaard S, Oyre S, Hansen MS, Rasmus S, Pedersen EM. Wall shear rates differ between the normal carotid, femoral, and brachial arteries: an in vivo MRI study. J Magn Reson Imaging. 2004;19:188–93.PubMedCrossRef Wu S, Ringgaard S, Oyre S, Hansen MS, Rasmus S, Pedersen EM. Wall shear rates differ between the normal carotid, femoral, and brachial arteries: an in vivo MRI study. J Magn Reson Imaging. 2004;19:188–93.PubMedCrossRef
72.
go back to reference Sui B, Gao P, Lin Y, Gao B, Liu L, An J. Assessment of wall shear stress in the common carotid artery of healthy subjects using 3.0-Tesla magnetic resonance. Acta Radiol. 2008;49:442–9.PubMedCrossRef Sui B, Gao P, Lin Y, Gao B, Liu L, An J. Assessment of wall shear stress in the common carotid artery of healthy subjects using 3.0-Tesla magnetic resonance. Acta Radiol. 2008;49:442–9.PubMedCrossRef
73.
go back to reference Sui B, Gao P, Lin Y, Qin H, Liu L, Liu G. Noninvasive determination of spatial distribution and temporal gradient of wall shear stress at common carotid artery. J Biomechan. 2008;41:3024–30.CrossRef Sui B, Gao P, Lin Y, Qin H, Liu L, Liu G. Noninvasive determination of spatial distribution and temporal gradient of wall shear stress at common carotid artery. J Biomechan. 2008;41:3024–30.CrossRef
74.
go back to reference Sui B, Gao P, Lin Y, Gao B, Liu L, An J. Blood flow pattern and wall shear stress in the internal carotid arteries of healthy subjects. Acta Radiol. 2008;49:806–14.PubMedCrossRef Sui B, Gao P, Lin Y, Gao B, Liu L, An J. Blood flow pattern and wall shear stress in the internal carotid arteries of healthy subjects. Acta Radiol. 2008;49:806–14.PubMedCrossRef
75.••
go back to reference Harloff A, Berg S, Barker AJ, Schöllhorn J, Schumacher M, Weiller C, et al. Wall shear stress distribution at the carotid bifurcation: influence of eversion carotid endarterectomy. Eur Radiol. 2013;23:3361–9. This paper shows, for the first time, the direct effect of carotid endarterectomy on WSS using 3D cine velocity-encoded MRI. Harloff A, Berg S, Barker AJ, Schöllhorn J, Schumacher M, Weiller C, et al. Wall shear stress distribution at the carotid bifurcation: influence of eversion carotid endarterectomy. Eur Radiol. 2013;23:3361–9. This paper shows, for the first time, the direct effect of carotid endarterectomy on WSS using 3D cine velocity-encoded MRI.
76.
go back to reference Meng H, Tutino VM, Siddiqui XJA. High WSS or Low WSS? Complex interactions of hemodynamics with intracranial aneurysm initiation, growth, and rupture: toward a unifying hypothesis. Am J Neuroradiol. 2013;1–9. doi:10.3174/ajnr.A3558. Meng H, Tutino VM, Siddiqui XJA. High WSS or Low WSS? Complex interactions of hemodynamics with intracranial aneurysm initiation, growth, and rupture: toward a unifying hypothesis. Am J Neuroradiol. 2013;1–9. doi:10.​3174/​ajnr.​A3558.
77.
go back to reference Isoda H, Ohkura Y, Kosugi T, Hirano M, Alley MT, Bammer R, et al. Comparison of hemodynamics of intracranial aneurysms between MR fluid dynamics using 3D cine phase-contrast MRI and MR-based computational fluid dynamics. Neuroradiology. 2010;52:913–20.PubMedCrossRef Isoda H, Ohkura Y, Kosugi T, Hirano M, Alley MT, Bammer R, et al. Comparison of hemodynamics of intracranial aneurysms between MR fluid dynamics using 3D cine phase-contrast MRI and MR-based computational fluid dynamics. Neuroradiology. 2010;52:913–20.PubMedCrossRef
78.
go back to reference Isoda H, Ohkura Y, Kosugi T, Hirano M, Takeda H, Hiramatsu H, 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;52:921–8.PubMedCrossRef Isoda H, Ohkura Y, Kosugi T, Hirano M, Takeda H, Hiramatsu H, 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;52:921–8.PubMedCrossRef
79.
go back to reference Naito T, Miyachi S, Matsubara N, Isoda H, Izumi T, Haraguchi K, et al. Magnetic resonance fluid dynamics for intracranial aneurysms—comparison with computed fluid dynamics. Acta Neurochir (Wien). 2012;154:993–1001.CrossRef Naito T, Miyachi S, Matsubara N, Isoda H, Izumi T, Haraguchi K, et al. Magnetic resonance fluid dynamics for intracranial aneurysms—comparison with computed fluid dynamics. Acta Neurochir (Wien). 2012;154:993–1001.CrossRef
80.
go back to reference Robbers-Visser D, Helderman F, Strengers JL, van Osch-Gevers L, Kapusta L, Pattynama PM, et al. Pulmonary artery size and function after Fontan operation at a young age. J Magn Reson Imaging. 2008;28:1101–7.PubMedCrossRef Robbers-Visser D, Helderman F, Strengers JL, van Osch-Gevers L, Kapusta L, Pattynama PM, et al. Pulmonary artery size and function after Fontan operation at a young age. J Magn Reson Imaging. 2008;28:1101–7.PubMedCrossRef
81.
go back to reference Mano Y, Takehara Y, Sakaguchi T, Alley MT, Isoda H, Shimizu T, et al. Hemodynamic assessment of celiaco-mesenteric anastomosis in patients with pancreaticoduodenal artery aneurysm concomitant with celiac artery occlusion using flow-sensitive four-dimensional magnetic resonance imaging. Eur J Vasc Endovasc Surg. 2013;46:321–8.PubMedCrossRef Mano Y, Takehara Y, Sakaguchi T, Alley MT, Isoda H, Shimizu T, et al. Hemodynamic assessment of celiaco-mesenteric anastomosis in patients with pancreaticoduodenal artery aneurysm concomitant with celiac artery occlusion using flow-sensitive four-dimensional magnetic resonance imaging. Eur J Vasc Endovasc Surg. 2013;46:321–8.PubMedCrossRef
82.
go back to reference Ku DN, Giddens DP, Zarins CK, Glagov S. Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low oscillating shear stress. Arteriosclerosis. 1985;5:293–302.PubMedCrossRef Ku DN, Giddens DP, Zarins CK, Glagov S. Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low oscillating shear stress. Arteriosclerosis. 1985;5:293–302.PubMedCrossRef
83.
go back to reference Hsiao A, Lustig M, Alley MT, Murphy M, Chan FP, Herfkens RJ, et al. Rapid pediatric cardiac assessment of flow and ventricular volume with compressed sensing parallel imaging volumetric cine phase-contrast MRI. Am J Roentgenol. 2012;198:W250–9.CrossRef Hsiao A, Lustig M, Alley MT, Murphy M, Chan FP, Herfkens RJ, et al. Rapid pediatric cardiac assessment of flow and ventricular volume with compressed sensing parallel imaging volumetric cine phase-contrast MRI. Am J Roentgenol. 2012;198:W250–9.CrossRef
Metadata
Title
Measuring Wall Shear Stress Using Velocity-Encoded MRI
Authors
Wouter V. Potters
Henk A. Marquering
Ed VanBavel
Aart J. Nederveen
Publication date
01-04-2014
Publisher
Springer US
Published in
Current Cardiovascular Imaging Reports / Issue 4/2014
Print ISSN: 1941-9066
Electronic ISSN: 1941-9074
DOI
https://doi.org/10.1007/s12410-014-9257-1

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