Abstract
Purpose
Arterial stiffness has predictive value for cardiovascular disease (CVD). Local artery stiffness can provide insight on CVD pathology and may be useful for diagnosis and prognosis. However, current methods are invasive, require real-time expertise for measurement, or are limited by arterial region. 4D Flow MRI can non-invasively measure local stiffness by estimating local pulse wave velocity (PWV). This technique can be applied to vascular regions, previously accessible only by invasive stiffness measurement methods. MRI PWV data can also be analyzed post-exam. However, 4D Flow MRI requires validation before it is used in vivo to measure local PWV.
Methods
PWV, calculated from 4D Flow MRI and a benchtop experiment, was compared with petersons elastic modulus (PEM) of in vitro models. PEM was calculated using high-speed camera images and pressure transducers. Three transit-time algorithms were analyzed for PWV measurement accuracy and precision.
Results
PWV from 4D Flow MRI and reference benchtop experiments show strong correlation with PEM (R2 = 0.99). The cross correlation transit-time algorithm showed the lowest percent difference between 4D Flow MRI and benchtop experiments (4–7%), and the point to point of 50% upstroke algorithm had the highest transit-time vs. distance data average R2 (0.845).
Conclusion
4D Flow MRI is a feasible method for estimating local PWV in simple in vitro models and is a viable tool for clinical analysis. In addition, choice in transit-time algorithm depends on flow waveform shape and arterial region. This study strengthens the validity of 4D Flow MRI local PWV measurement in simple models. However, this technique requires validation in more complex models before it is used in vivo.
Similar content being viewed by others
References
Blacher, J., A. P. Guerin, B. Pannier, S. J. Marchais, M. E. Safar, and G. M. London. Impact of aortic stiffness on survival in end-stage renal disease. Circulation. 99(18):2434–2439, 1999.
Bolster, B. D., E. Atalar, C. J. Hardy, and E. R. McVeigh. Accuracy of arterial pulse-wave velocity measurement using MR. J. Magn. Reson. Imaging. 8:878–888, 1998.
Boutouyrie, P., M. Briet, C. Collin, S. Vermeersch, and B. Pannier. Assessment of pulse wave velocity. Artery Res. 3:3–8, 2009.
Boutouyrie, P., D. Fliser, D. Goldsmith, A. Covic, A. Wiecek, A. Ortiz, et al. Assessment of arterial stiffness for clinical and epidemiological studies: methodological considerations for validation and entry into the European Renal and Cardiovascular Medicine registry. Nephrol. Dial. Transplant. 29:232–239, 2014.
Boutouyrie, P., A. I. Tropeano, R. Asmar, I. Gautier, A. Benetos, P. Lacolley, et al. Aortic stiffness is an independent predictor of primary coronary events in hypertensive patients: a longitudinal study. Hypertension. 39:10–15, 2002.
Chiu, Y. C., P. W. Arand, S. G. Shroff, T. Feldman, and J. D. Carroll. Determination of pulse wave velocities with computerized algorithms. Am. Heart J. 121:1460–1470, 1991.
Cruickshank, K., L. Riste, S. G. Anderson, J. S. Wright, G. Dunn, and R. G. Gosling. Aortic pulse-wave velocity and its relationship to mortality in diabetes and glucose intolerance: an integrated index of vascular function? Circulation. 106:2085–2090, 2002.
Dogui, A., N. Kachenoura, F. Frouin, M. Lefort, A. De Cesare, E. Mousseaux, et al. Consistency of aortic distensibility and pulse wave velocity estimates with respect to the Bramwell-Hill theoretical model: a cardiovascular magnetic resonance study. J. Cardiovasc. Magn. Reson. 13(1):11, 2011.
Dogui, A., A. Redheuil, M. Lefort, A. Decesare, N. Kachenoura, A. Herment, et al. Measurement of aortic arch pulse wave velocity in cardiovascular MR: comparison of transit time estimators and description of a new approach. J. Magn. Reson. Imaging. 33:1321–1329, 2011.
Gu, T., F. R. Korosec, W. F. Block, S. B. Fain, Q. Turk, D. Lum, et al. PC VIPR: a high-speed 3D phase-contrast method for flow quantification and high-resolution angiography. Am. J. Neuroradiol. 26:743–749, 2005.
Hermeling, E., K. D. Reesink, R. S. Reneman, and A. P. G. Hoeks. Measurement of local pulse wave velocity: effects of signal processing on precision. Ultrasound Med. Biol. 33:774–781, 2007.
Johnson, K. M., D. P. Lum, P. A. Turski, W. F. Block, C. A. Mistretta, and O. Wieben. Improved 3D phase contrast MRI with off-resonance corrected dual echo VIPR. Magn. Reson. Med. 60:1329–1336, 2008.
Laurent, S., J. Cockcroft, L. Van Bortel, P. Boutouyrie, C. Giannattasio, D. Hayoz, et al. Expert consensus document on arterial stiffness: methodological issues and clinical applications. Eur. Heart J. 27:2588–2605, 2006.
Laurent, S., S. Katsahian, C. Fassot, A. I. Tropeano, I. Gautier, B. Laloux, et al. Aortic stiffness is an independent predictor of fatal stroke in essential hypertension. Stroke. 34:1203–1206, 2003.
London, G. M., and M. E. Safar. Arterial wall remodelling and stiffness in hypertension: heterogeneous aspects. Clin. Exp. Pharmacol. Physiol. 23:S1–S5, 1996.
Lozano, R., M. Naghavi, K. Foreman, S. Lim, K. Shibuya, V. Aboyans, et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet. 380:2095–2128, 2012.
Markl, M., W. Wallis, S. Brendecke, J. Simon, A. Frydrychowicz, and A. Harloff. Estimation of global aortic pulse wave velocity by flow-sensitive 4D MRI. Magn. Reson. Med. 63:1575–1582, 2010.
Markl, M., W. Wallis, C. Strecker, B. P. Gladstone, W. Vach, and A. Harloff. Analysis of pulse wave velocity in the thoracic aorta by flow-sensitive four-dimensional MRI: reproducibility and correlation with characteristics in patients with aortic atherosclerosis. J. Magn. Reson. Imaging. 35:1162–1168, 2012.
Mattace-Raso, F. U. S., T. J. M. Van Der Cammen, A. Hofman, N. M. Van Popele, M. L. Bos, M. A. D. H. Schalekamp, et al. Arterial stiffness and risk of coronary heart disease and stroke: the Rotterdam Study. Circulation. 113:657–663, 2006.
Meinders, J. M., L. Kornet, P. J. Brands, and A. P. Hoeks. Assessment of local pulse wave velocity in arteries using 2D distension waveforms. Ultrason. Imaging. 23:199–215, 2001.
Millasseau, S. C., A. D. Stewart, S. J. Patel, S. R. Redwood, and P. J. Chowienczyk. Evaluation of carotid-femoral pulse wave velocity: influence of timing algorithm and heart rate. Hypertension. 45:222–226, 2005.
Mitchell, G. F., S.-J. Hwang, R. S. Vasan, M. G. Larson, M. J. Pencina, N. M. Hamburg, et al. Arterial stiffness and cardiovascular events: the framingham heart study. Circulation. 121:505–511, 2010.
Nichols, W. W., and D. A. McDonald. Wave-velocity in the proximal aorta. Med. Biol. Eng. 10:327–335, 1972.
Nichols, W., and B. Singh. Augmentation index as a measure of peripheral vascular disease state. Curr. Opin. Cardiol. 17:543–551, 2002.
Papageorgiou, G. L., and N. B. Jones. Physical modelling of the arterial wall. Part 1: testing of tubes of various materials. J. Biomed. Eng. 9:153–156, 1987.
Peterson, L. H., R. E. Jensen, and J. Parnell. Mechanical properties of arteries in vivo. Circ. Res. 8:622–639, 1960.
Quinaglia, T., M. Z. Bensalah, E. Bollache, N. Kachenoura, G. Soulat, P. Boutouyrie, et al. Differential impact of local and regional aortic stiffness on left ventricular remodeling. J. Hypertens. 36:1, 2018.
Swillens, A., L. Taelman, J. Degroote, J. Vierendeels, and P. Segers. Comparison of non-invasive methods for measurement of local pulse wave velocity using fsi-simulations and in vivo data. Ann. Biomed. Eng. 41:1567–1578, 2013.
Taviani, V., A. J. Patterson, M. J. Graves, C. J. Hardy, P. Worters, M. P. F. Sutcliffe, et al. Accuracy and repeatability of fourier velocity encoded M-mode and two-dimensional cine phase contrast for pulse wave velocity measurement in the descending aorta. J. Magn. Reson. Imaging. 31:1185–1194, 2010.
Tijsseling, A., and A. A. Anderson. Isebree Moens and DJ Korteweg: On the Speed of Propagation of Waves in Elastic Tubes. BHR Gr: Conf Press Surges, pp. 1–19, 2012.
Van Bortel, L. M., D. Duprez, M. J. Starmans-Kool, M. E. Safar, C. Giannattasio, J. Cockcroft, et al. Clinical applications of arterial stiffness, task force III: recommendations for user procedures. Am. J. Hypertens. 15:445–452, 2002.
Van Sloten, T. T., M. T. Schram, K. Van Den Hurk, J. M. Dekker, G. Nijpels, R. M. A. Henry, et al. Local stiffness of the carotid and femoral artery is associated with incident cardiovascular events and all-cause mortality: the hoorn study. J. Am. Coll. Cardiol. 63:1739–1747, 2014.
Walker, P. G., G. B. Cranney, M. B. Scheidegger, G. Waseleski, G. M. Pohost, and A. P. Yoganathan. Semiautomated method for noise reduction and background phase error correction in MR phase velocity data. J. Magn. Reson. Imaging. 3:521–530, 1993.
Wang, Z., Y. Yang, L. J. Yuan, J. Liu, Y. Y. Duan, and T. S. Cao. Noninvasive method for measuring local pulse wave velocity by dual pulse wave Doppler: in vitro and in vivo studies. PLoS ONE. 10:1–13, 2015.
Wentland, A. L., T. M. Grist, and O. Wieben. Review of MRI-based measurements of pulse wave velocity: a biomarker of arterial stiffness. Cardiovasc. Diagn. Ther. 4:193–206, 2014.
Wentland, A. L., O. Wieben, C. J. François, C. Boncyk, A. Munoz Del Rio, K. M. Johnson, et al. Aortic pulse wave velocity measurements with undersampled 4D flow-sensitive MRI: comparison with 2D and algorithm determination. J. Magn. Reson. Imaging. 37:853–859, 2013.
Westenberg, J. J. M., E. P. Van Poelgeest, P. Steendijk, H. B. Grotenhuis, J. W. Jukema, and A. De Roos. Bramwell-Hill modeling for local aortic pulse wave velocity estimation: a validation study with velocity-encoded cardiovascular magnetic resonance and invasive pressure assessment. J. Cardiovasc. Magn. Reson. 14:2, 2012.
World Health Organization. Cardiovascular diseases [Internet]. 2017 [cited 2018 Mar 4]. p. 1–6. http://www.who.int/mediacentre/factsheets/fs317/en/.
Yang, E. Y., L. Chambless, A. R. Sharrett, S. S. Virani, X. Liu, Z. Tang, et al. Carotid arterial wall characteristics are associated with incident ischemic stroke but not coronary heart disease in the Atherosclerosis Risk in Communities (ARIC) Study. Stroke. 43:103–108, 2012.
Conflict of interest
Timothy Ruesink, David Rutkowski, Rafael Medero and Alejandro Roldán-Alzate declare that they have no conflict of interest.
Research Involving Human and Animal Participants
No human studies were carried out by the authors for this article. No animal studies were carried out by the authors for this article.
Author information
Authors and Affiliations
Corresponding author
Additional information
Associate Editors David A. Steinman, Francesco Migliavacca, and Ajit P. Yoganathan oversaw the review of this article.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ruesink, T., Medero, R., Rutkowski, D. et al. In Vitro Validation of 4D Flow MRI for Local Pulse Wave Velocity Estimation. Cardiovasc Eng Tech 9, 674–687 (2018). https://doi.org/10.1007/s13239-018-00377-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13239-018-00377-z