Abstract
4D Flow MRI is a diagnostic tool that can visualize and quantify patient-specific hemodynamics and help interventionalists optimize treatment strategies for repairing coarctation of the aorta (COA). Despite recent developments in 4D Flow MRI, shortcomings include phase-offset errors, limited spatiotemporal resolution, aliasing, inaccuracies due to slow aneurysmal flows, and distortion of images due to metallic artifact from vascular stents. To address these limitations, we developed a framework utilizing Computational Fluid Dynamics (CFD) with Adaptive Mesh Refinement (AMR) that enhances 4D Flow MRI visualization/quantification. We applied this framework to five pediatric patients with COA, providing in-vivo and in-silico datasets, pre- and post-intervention. These two data sets were compared and showed that CFD flow rates were within 9.6% of 4D Flow MRI, which is within a clinically acceptable range. CFD simulated slow aneurysmal flow, which MRI failed to capture due to high relative velocity encoding (Venc). CFD successfully predicted in-stent blood flow, which was not visible in the in-vivo data due to susceptibility artifact. AMR improved spatial resolution by factors of 101 to 103 and temporal resolution four-fold. This computational framework has strong potential to optimize visualization/quantification of aneurysmal and in-stent flows, improve spatiotemporal resolution, and assess hemodynamic efficiency post-COA treatment.
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Abbreviations
- COA:
-
Coarctation of the aorta
- CFD:
-
Computational fluid dynamics
- AMR:
-
Adaptive mesh refinement
- Venc :
-
Velocity encoding
- PC-MRA:
-
Phase-contrast magnetic resonance angiography
- CE-MRA:
-
Contrast-enhanced magnetic resonance angiography
- CTA:
-
Computed tomography angiography
- BC:
-
Boundary condition
- \({q}^{\text{BCA}}\) :
-
Fractional volumetric flow rate in brachiocephalic artery
- \({q}^{\text{LCC}}\) :
-
Fractional volumetric flow rate in left common carotid artery
- \({q}^{\text{LS}}\) :
-
Fractional volumetric flow rate in left subclavian artery
- \({q}^{\text{Desc}}\) :
-
Fractional volumetric flow rate in descending thoracic aorta
- \(\Delta q\) :
-
Maximum absolute difference in fractional volumetric flow rates from 4D flow MRI and CFD among outlets
References
Abbruzzese, P. A., and E. Aidala. Aortic coarctation: an overview. J. Cardiovasc. Med. 8(2):123–128, 2007
Allen, B. D., P. van Ooij, A. J. Barker, M. Carr, M. Gabbour, S. Schnell, K. B. Jarvis, J. C. Carr, M. Markl, C. Rigsby, and J. D. Robinson. Thoracic aorta 3D hemodynamics in pediatric and young adult patients with bicuspid aortic valve. J. Magn. Reson. Imaging. 42:954–963, 2015
Backer, C. L., C. Mavroudis, E. A. Zias, Z. Amin, and T. J. Weigel. Repair of coarctation with resection and extended end-to-end anastomosis. Ann. Thorac. Surg. 66:1365–1370, 1998
Bedford, K. W., and W. K. Yeo. Conjunctive filtering procedures in surface water flow and transport. In: Large Eddy Simulation of Complex Engineering and Geophysical Flows, edited by B. Galperin, and S. A. Orszag. Cambridge: Cambridge University Press, 1993, pp. 513–537
Bock, J., B. W. Kreher, J. Hennig, and M. Markl. Optimized pre-processing of time-resolved 2D and 3D phase contrast MRI data, 2007.
Callahan, S., N. S. Singam, M. Kendrick, M. J. Negahdar, H. Wang, M. F. Stoddard, and A. A. Amini. Dual-Venc acquisition for 4D flow MRI in aortic stenosis with spiral readouts. J Magn Reson Imaging. 2019. https://doi.org/10.1002/jmri.27004
Canniffe, C., P. Ou, K. Walsh, D. Bonnet, and D. Celermajer. Hypertension after repair of aortic coarctation: A systematic review. Int J Cardiol. 167(6):2456–2461, 2013
Desai, L., H. Stefek, H. Berhane, J. Robinson, C. Rigsby, and M. Markl. Four-dimensional flow magnetic resonance imaging for assessment of pediatric coarctation of the aorta. J. Magn. Reson. Imaging. 2021. https://doi.org/10.1002/JMRI.27802
Dyverfeldt, P., M. Bissell, A. J. Barker, A. F. Bolger, C.-J. Carlhäll, T. Ebbers, C. J. Francios, A. Frydrychowicz, J. Geiger, D. Giese, M. D. Hope, P. J. Kilner, S. Kozerke, S. Myerson, S. Neubauer, O. Wieben, and M. Markl. 4D flow cardiovascular magnetic resonance consensus statement. J Cardiovasc Magn Reson. 17:1–19, 2015
Dyverfeldt, P., A. Sigfridsson, J. P. E. Kvitting, and T. Ebbers. Quantification of intravoxel velocity standard deviation and turbulence intensity by generalizing phase-contrast MRI. Magnetic Resonance in Medicine. 56:850–858, 2006
Fathi, M. F., I. Perez-Raya, A. Baghaie, P. Berg, G. Janiga, A. Arzani, and R. M. D’Souza. Super-resolution and denoising of 4D-Flow MRI using physics-Informed deep neural nets. Computer Methods and Programs in Biomedicine.197:105729, 2020
Feltes, T. F., E. Bacha, R. H. Beekman, J. P. Cheatham, J. A. Feinstein, A. S. Gomes, Z. M. Hijazi, F. F. Ing, M. de Moor, W. R. Morrow, C. E. Mullins, K. A. Taubert, and E. M. Zahn. Indications for cardiac catheterization and intervention in pediatric cardiac disease: a scientific statement from the American Heart Association. Circulation. 123:2607–2652, 2011
Figueroa, C. A., I. E. Vignon-Clementel, K. E. Jansen, T. J. R. Hughes, and C. A. Taylor. A coupled momentum method for modeling blood flow in three-dimensional deformable arteries. Computer Methods in Applied Mechanics and Engineering. 195:5685–5706, 2006
Frydrychowicz, A., R. Arnold, D. Hirtler, C. Schlensak, A. F. Stalder, J. Hennig, M. Langer, and M. Markl. Multidirectional flow analysis by cardiovascular magnetic resonance in aneurysm development following repair of aortic coarctation. Journal of Cardiovascular Magnetic Resonance. 10:30, 2008
Frydrychowicz, A., M. Markl, D. Hirtler, A. Harloff, C. Schlensak, J. Geiger, B. Stiller, and R. Arnold. Aortic hemodynamics in patients with and without repair of aortic coarctation: In vivo analysis by 4D Flow-sensitive magnetic resonance imaging. Investigative Radiology. 46:317–325, 2011
Gan, C. T. J., J. W. Lankhaar, N. Westerhof, J. T. Marcus, A. Becker, J. W. R. Twisk, A. Boonstra, P. E. Postmus, and A. Vonk-Noordegraaf. Noninvasively assessed pulmonary artery stiffness predicts mortality in pulmonary arterial hypertension. Chest. 132:1906–1912, 2007
Goubergrits, L., E. Riesenkampff, P. Yevtushenko, J. Schaller, U. Kertzscher, A. Hennemuth, F. Berger, S. Schubert, and T. Kuehne. MRI-based computational fluid dynamics for diagnosis and treatment prediction: Clinical validation study in patients with coarctation of aorta. J. Magn. Reson. Imaging. 41:909–916, 2015
Hope, M. D., A. K. Meadows, T. A. Hope, K. G. Ordovas, D. Saloner, G. P. Reddy, M. T. Alley, and C. B. Higgins. Clinical evaluation of aortic coarctation with 4D flow MR imaging. J. Magn. Reson. Imaging. 31:711–718, 2010
Kaushal, S., C. L. Backer, J. N. Patel, S. K. Patel, B. L. Walker, T. J. Weigel, G. Randolph, D. Wax, and C. Mavroudis. Coarctation of the aorta: Midterm outcomes of resection with extended end-to-end anastomosis. Annals of Thoracic Surgery. 88:1932–1938, 2009
Koivistoinen, T., T. Kööbi, A. Jula, N. Hutri-kähönen, O. T. Raitakari, S. Majahalme, K. Kukkonen-harjula, T. Lehtimäki, A. Reunanen, J. Viikari, V. Turjanmaa, T. Nieminen, and M. Kähönen. Pulse wave velocity reference values in healthy adults aged 26–75 years. Clin. Physiol. Funct. Imaging. 27:191–196, 2007
Levine, G. N., A. S. Gomes, A. E. Arai, D. A. Bluemke, S. D. Flamm, E. Kanal, W. J. Manning, E. T. Martin, J. M. Smith, N. Wilke, and F. S. Shellock. Safety of magnetic resonance imaging in patients with cardiovascular devices: An American heart association scientific statement from the committee on diagnostic and interventional cardiac catheterization, council on clinical cardiology, and the council on cardiovascular radiology and intervention. Circulation. 116:2878–2891, 2007
Markl, M., A. Frydrychowicz, S. Kozerke, M. Hope, and O. Wieben. 4D flow MRI. J. Magn. Reson. Imaging. 36:1015–1036, 2012
Markl, M., P. J. Kilner, and T. Ebbers. Comprehensive 4D velocity mapping of the heart and great vessels by cardiovascular magnetic resonance. J. Cardiovasc. Magn. Reson. 13(1):7, 2011
Marsden, A. L., and M. Esmaily-Moghadam. Multiscale modeling of cardiovascular flows for clinical decision support. Appl. Mech. Rev. 67:030804, 2015
Marsden, A. L., and J. A. Feinstein. Computational modeling and engineering in pediatric and congenital heart disease. Curr. Opin. Pediatr. 27(5):587–596, 2015
Menon, S., P. K. Yeung, and W. W. Kim. Effect of subgrid models on the computed interscale energy transfer in isotropic turbulence. Comput. Fluids. 25:165–180, 1996
Min, J., D. Berman, L. Shaw, L. Mauri, B.-K. Koo, A. Erglis, J. Leipsic, A. Maehara, G. Mintz, B. Witzenbichler, D. C. Metzger, M. Rinaldi, E. Mazzaferri, P. Duffy, G. Weisz, T. Stuckey, B. Brodie, K. Xu, H. Parise, R. Mehran, and G. Stone. Fractional flow reserved derived from computed tomographic angiography (FFRCT) for intermediate severity coronary lesions: Results from the DeFACTO trial (Determination of fractional flow reserve by anatomic computed tomographic angiography) IVUS predictors of stent thrombosis: Results from the prospective, multicenter ADAPT-DES study. J. Am. Coll. Cardiol. 60:B6, 2012
Minderhoud, S. C. S., N. van der Velde, J. J. Wentzel, R. J. van der Geest, M. Attrach, P. A. Wielopolski, R. P. J. Budde, W. A. Helbing, J. W. Roos-Hesselink, and A. Hirsch. The clinical impact of phase offset errors and different correction methods in cardiovascular magnetic resonance phase contrast imaging: a multi-scanner study. J. Cardiovasc. Magn. Reson. 22:1–13, 2020
Mirramezani, M., and S. C. Shadden. A distributed lumped parameter model of blood flow. Annals of Biomedical Engineering. 48:2870–2886, 2020
Miyazaki, S., K. Itatani, T. Furusawa, T. Nishino, M. Sugiyama, Y. Takehara, and S. Yasukochi. Validation of numerical simulation methods in aortic arch using 4D Flow MRI. Heart and Vessels. 32:1032–1044, 2017
Nakazato, R., H. B. Park, D. S. Berman, H. Gransar, B. K. Koo, A. Erglis, F. Y. Lin, A. M. Dunning, M. J. Budoff, J. Malpeso, J. Leipsic, and J. K. Min. Noninvasive fractional flow reserve derived from computed tomography angiography for coronary lesions of intermediate stenosis severity: results from the DeFACTO study. Circ. Cardiovasc. imaging. 6:881–889, 2013
Oliver, J. M., P. Gallego, A. Gonzalez, A. Aroca, M. Bret, and J. M. Mesa. Risk factors for aortic complications in adults with coarctation of the aorta. J. Am. Coll. Cardiol. 44:1641–1647, 2004
Ou, P., D. S. Celermajer, E. Mousseaux, A. Giron, Y. Aggoun, I. Szezepanski, D. Sidi, and D. Bonnet. Vascular remodeling after “successful” repair of coarctation impact of aortic arch geometry. J. Am. Coll. Cardiol. 49:883–890, 2007
Petersson, S., P. Dyverfeldt, R. Gårdhagen, M. Karlsson, and T. Ebbers. Simulation of phase contrast MRI of turbulent flow. Magn. Reson. Med. 64:1039–1046, 2010
Petersson, S., P. Dyverfeldt, A. Sigfridsson, J. Lantz, C. J. Carlhäll, and T. Ebbers. Quantification of turbulence and velocity in stenotic flow using spiral three-dimensional phase-contrast MRI. Magn. Reson. Med. 75:1249, 2016
Pewowaruk, R., L. Lamers, and A. Roldán-Alzate. Accelerated estimation of pulmonary artery stenosis pressure gradients with distributed lumped parameter modeling vs. 3D CFD with instantaneous adaptive mesh refinement: experimental validation in swine. Ann. Biomed. Eng. 2021. https://doi.org/10.1007/s10439-021-02780-5
Pewowaruk, R., Y. Li, D. Rowinski, and A. Roldán-Alzate. Solution adaptive refinement of cut-cell Cartesian meshes can improve FDA nozzle computational fluid dynamics efficiency. Int. J. Numer. Methods Biomed. Eng. 2021. https://doi.org/10.1002/cnm.3432
Pewowaruk, R., and A. Roldán-Alzate. A distributed lumped parameter model of blood flow with fluid-structure interaction. Biomech. Model. Mechanobiol. 20:1659–1674, 2021
Raimund, E., et al. ESC Guidelines on the diagnosis and treatment of aortic diseases: Document covering acute and chronic aortic diseases of the thoracic and abdominal aorta of the adult. The Task Force for the Diagnosis and Treatment of Aortic Diseases of the European Society of Cardiology (ESC). Eur. Heart J. 35(2873–2926):2014, 2014
Rao, P. S. Coarctation of the aorta. Current cardiology reports. 7:425–434, 2005
Richards, K. J., P. K. Senecal, and E. Pomraning. CONVERGE, 2020.
Roldán-Alzate, A., A. Frydrychowicz, E. Niespodzany, B. R. Landgraf, K. M. Johnson, O. Wieben, and S. B. Reeder. In vivo validation of 4D flow MRI for assessing the hemodynamics of portal hypertension. J. Magn. Reson. Imaging. 37:1100–1108, 2013
Sahni, O., K. E. Jansen, C. A. Taylor, and M. S. Shephard. Automated adaptive cardiovascular flow simulations. Engineering with Computers. 25:25–36, 2009
Saxena, A. Recurrent coarctation: interventional techniques and results. World J. Pediatr. Congenit. Heart Surg. 6:257–265, 2015
Stein, P. D., and H. N. Sabbah. Turbulent blood flow in the ascending aorta of humans with normal and diseased aortic valves. Circ. Res. 39:58–65, 1976
Stout, K. K., C. J. Daniels, J. A. Aboulhosn, B. Bozkurt, C. S. Broberg, J. M. Colman, S. R. Crumb, J. A. Dearani, S. Fuller, M. Gurvitz, P. Khairy, M. J. Landzberg, A. Saidi, A. M. Valente, and G. F. van Hare. 2018 AHA/ACC guideline for the management of adults with congenital heart disease: A report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines. Circulation. 139:e698–e800, 2019
Taylor, C. A., T. A. Fonte, and J. K. Min. Computational fluid dynamics applied to cardiac computed tomography for noninvasive quantification of fractional flow reserve: scientific basis. J. Am. Coll. Cardiol. 61:2233–2241, 2013
Torok, R. D. Coarctation of the aorta: Management from infancy to adulthood. World J. Cardiol. 7:765, 2015
Yoshizawa, A., and K. Horiuti. A statistically-derived subgrid-scale kinetic energy model for the large-eddy simulation of turbulent flows. J. Phys. Soc. Jpn. 54:2834–2839, 1985
Zambrano, B. A., N. A. McLean, X. Zhao, J. le Tan, L. Zhong, C. A. Figueroa, L. C. Lee, and S. Baek. Image-based computational assessment of vascular wall mechanics and hemodynamics in pulmonary arterial hypertension patients. J. Biomech. 68:84–92, 2018
Acknowledgments
Funding was provided by the American Heart Association (Grant No. 19TPA34850066). GE Healthcare, which provides research support to the University of Wisconsin. This research was performed using the compute resources and assistance of the UW-Madison Center For High Throughput Computing (CHTC) in the Department of Computer Sciences. The CHTC is supported by UW-Madison, the Advanced Computing Initiative, the Wisconsin Alumni Research Foundation, the Wisconsin Institutes for Discovery, and the National Science Foundation, and is an active member of the OSG Consortium, which is supported by the National Science Foundation and the U.S. Department of Energy's Office of Science.
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Shahid, L., Rice, J., Berhane, H. et al. Enhanced 4D Flow MRI-Based CFD with Adaptive Mesh Refinement for Flow Dynamics Assessment in Coarctation of the Aorta. Ann Biomed Eng 50, 1001–1016 (2022). https://doi.org/10.1007/s10439-022-02980-7
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DOI: https://doi.org/10.1007/s10439-022-02980-7