Abstract
For the left ventricle (LV) to function as an effective pump it must be able to fill from a low left atrial pressure. However, this ability is lost in patients with heart failure. We investigated LV filling by measuring the cardiac blood flow using 2D phase contrast magnetic resonance imaging and quantified the intraventricular pressure gradients and the strength and location of vortices. In normal subjects, blood flows towards the apex prior to the mitral valve opening, and the mitral annulus moves rapidly away after the valve opens, with both effects enhancing the vortex ring at the mitral valve tips. Instead of being a passive by-product of the process as was previously believed, this ring facilitates filling by reducing convective losses and enhancing the function of the LV as a suction pump. The virtual channel thus created by the vortices may help insure efficient mass transfer for the left atrium to the LV apex. Impairment of this mechanism contributes to diastolic dysfunction, with LV filling becoming dependent on left atrial pressure, which can lead to eventual heart failure. Better understanding of the mechanics of this progression may lead to more accurate diagnosis and treatment of this disease.
Similar content being viewed by others
Abbreviations
- DCM:
-
Dilated cardiomyopathy
- FTLE:
-
Finite time Lyapunov exponents
- LA:
-
Left atrium
- LCS:
-
Lagrangian coherent structures
- LV:
-
Left ventricle
- LVDD:
-
Left ventricular diastolic dysfunction
- MV:
-
Mitral valve
- MRI:
-
Magnetic resonance imaging
- pcMRI:
-
Phase contrast MRI
- POD:
-
Proper orthogonal decomposition
- RV:
-
Right ventricle
- SNR:
-
Signal to noise ratio
References
Appleton, C. P. Doppler assessment of left ventricular diastolic function: the refinements continue. J. Am. Coll. Cardiol. 21(7):1697–1700, 1993.
Berkooz, G., P. Holmes, and J. L. Lumley. The proper orthogonal decomposition in the analysis of turbulent flows. Annu. Rev. Fluid Mech. 25:539–575, 1993.
Brucks, S., W. C. Little, T. Chao, D. W. Kitzman, D. Wesley-Farrington, S. Gandhi, and Z. K. Shihabi. Contribution of left ventricular diastolic dysfunction to heart failure regardless of ejection fraction. Am. J. Cardiol. 95(5):603–606, 2005.
Brun, P., C. Tribouilloy, A.-M. Duval, L. Iserin, A. Meguira, G. Pelle, and J.-L. Dubois-Rande. Left ventricular flow propagation during early filling is related to wall relaxation: a color M-mode Doppler analysis. J. Am. Coll. Cardiol. 20(2):420–432, 1992.
Buckberg, G. D., M. Castellá, M. Gharib, and S. Saleh. Active myocyte shortening during the ‘isovolumetric relaxation’ phase of diastole is responsible for ventricular suction; ‘systolic ventricular filling’. Eur. J. Cardiothorac. Surg. 29(Supplement 1):S98–S106, 2006.
Buyens, F., O. Jolivet, A. D. Cesare, J. Bittoun, A. Herment, J.-P. Tasu, and E. Mousseaux. Calculation of left ventricle relative pressure distribution in MRI using acceleration data. Magn. Reson. Med. 53(4):877–884, 2005.
Charonko, J. J., C. V. King, B. L. Smith, and P. P. Vlachos. Assessment of pressure field calculations from particle image velocimetry measurements. Meas. Sci. Technol. 21:105401, 2010.
Cheng, C. P., Y. Igarashi, and W. C. Little. Mechanism of augmented rate of left ventricular filling during exercise. Circ. Res. 70(1):9–19, 1992.
Claessens, T. E., J. De Sutter, D. Vanhercke, P. Segers, and P. R. Verdonck. New echocardiographic applications for assessing global left ventricular diastolic function. Ultrasound Med. Biol. 33(6):823–841, 2007.
Courtois, M., S. J. Kovács, and P. A. Ludbrook. Transmitral pressure–flow velocity relation. Importance of regional pressure gradients in the left ventricle during diastole. Circulation 78(3):661–671, 1988.
Dabiri, J. O., and M. Gharib. Delay of vortex ring pinchoff by an imposed bulk counterflow. Phys. Fluids 16(4):L28–L30, 2004.
Domenichini, F., G. Pedrizzetti, and B. Baccani. Three-dimensional filling flow into a model left ventricle. J. Fluid Mech. 539:179–198, 2005.
Ebbers, T., L. Wigstrom, A. F. Bolger, J. Engvall, and M. Karlsson. Characterization of left ventricular diastolic function in hypertension by use of Doppler tissue imaging and color M-mode techniques. Magn. Reson. Med. 45(5):872–879, 2001.
Garcia, M. J., J. D. Thomas, and A. L. Klein. New Doppler echocardiographic applications for the study of diastolic function. J. Am. Coll. Cardiol. 32(4):865–875, 1998.
Gharib, M., E. Rambod, A. Kheradvar, D. J. Sahn, and J. O. Dabiri. Optimal vortex formation as an index of cardiac health. Proc. Natl. Acad. Sci. U. S. A. 103(16):6305–6308, 2006.
Greenberg, N. L., P. M. Vandervoort, M. S. Firstenberg, M. J. Garcia, and J. D. Thomas. Estimation of diastolic intraventricular pressure gradients by Doppler M-mode echocardiography. Am. J. Physiol. Heart Circ. Physiol. 280(6):H2507–H2515, 2001.
Haller, G. Lagrangian structures and the rate of strain in a partition of two-dimensional turbulence. Phys. Fluids 13(11):3365–3385, 2001.
Haller, G. Lagrangian coherent structures from approximate velocity data. Phys. Fluids 14(6):1851–1861, 2002.
Hasegawa, H., W. C. Little, M. Ohno, S. Brucks, A. Morimoto, H.-J. Cheng, and C.-P. Cheng. Diastolic mitral annular velocityduring the development of heart failure. J. Am. Coll. Cardiol. 41(9):1590–1597, 2003.
Hong, G.-R., G. Pedrizzetti, G. Tonti, P. Li, Z. Wei, J. K. Kim, A. Baweja, S. Liu, N. Chung, H. Houle, J. Narula, and M. A. Vannan. Characterization and quantification of vortex flow in the human left ventricle by contrast echocardiography using vector particle image velocimetry. J. Am. Coll. Cardiol. Imaging 6:705–717, 2008.
Jeong, J., and F. Hussain. On the identification of a vortex. J. Fluid Mech. 285:69–94, 1995.
Katz, L. N. The role played by the ventricular relaxation process in filling the ventricle. Am. J. Physiol. 95(3):542–553, 1930.
Kheradvar, A., and M. Gharib. Influence of ventricular pressure drop on mitral annulus dynamics through the process of vortex ring formation. Ann. Biomed. Eng. 35(12):2050–2064, 2007.
Kheradvar, A., M. Milano, and M. Gharib. Correlation between vortex ring formation and mitral annulus dynamics during ventricular rapid filling. ASAIO J. 53(1):8–16, 2007.
Kilner, P. J., G.-Z. Yang, A. J. Wilkes, R. H. Mohiaddin, D. N. Firmin, and M. H. Yacoub. Asymmetric redirection of flow through the heart. Nature 404:759–761, 2000.
Kumar, R., J. Charonko, W. G. Hundley, C. A. Hamilton, K. C. Stewart, G. R. McNeal, P. P. Vlachos, and W. C. Little. Assessment of left ventricular diastolic function using 4-dimensional phase-contrast cardiac magnetic resonance. J. Comput. Assist. Tomogr. 35(1):108–112, 2011.
Lew, W. Y. W. Evaluation of left-ventricular diastolic function. Circulation 79(6):1393–1397, 1989.
Little, W. C. Diastolic dysfunction beyond distensibility: adverse effects of ventricular dilatation. Circulation 112(19):2888–2890, 2005.
Little, W. C., and J. K. Oh. Echocardiographic evaluation of diastolic function can be used to guide clinical care. Circulation 120(9):802–809, 2009.
Liu, X., and J. Katz. Instantaneous pressure and material acceleration measurements using a four-exposure PIV system. Exp. Fluids 41(2):227–240, 2006.
Nagueh, S. F., C. P. Appleton, T. C. Gillebert, P. N. Marino, J. K. Oh, O. A. Smiseth, A. D. Waggoner, F. A. Flachskampf, P. A. Pellikka, and A. Evangelista. Recommendations for the evaluation of left ventricular diastolic function by echocardiography. J. Am. Soc. Echocardiogr. 22(2):107–133, 2009.
Narula, J., M. A. Vannan, and A. N. DeMaria. Of that waltz in my heart. J. Am. Coll. Cardiol. 49(8):917–920, 2007.
Nishimura, M. D., and M. D. Tajik. Evaluation of diastolic filling of left ventricle in health and disease: Doppler echocardiography is the clinician’s Rosetta stone. J. Am. Coll. Cardiol. 30(1):8–18, 1997.
Ohno, M., C. P. Cheng, and W. C. Little. Mechanism of altered patterns of left ventricular filling during the development of congestive heart failure. Circulation 89(5):2241–2250, 1994.
Ohte, N., H. Narita, S. Akita, K. Kurokawa, J. Hayano, M. Sugawara, and G. Kimura. The mechanism of emergence and clinical significance of apically directed intraventricular flow during isovolumic relaxation. J. Am. Soc. Echocardiogr. 15(7):715–722, 2002.
Pasipoularides, A. Heart’s Vortex: Intracardiac Blood Flow Phenomena. Shelton, CT: PMPH-USA, 2009.
Pasipoularides, A. Diastolic filling vortex forces and cardiac adaptations: probing the epigenetic nexus. Hellenic J. Cardiol. 53:458–469, 2012.
Redfield, M. M., S. J. Jacobsen, J. C. Burnett, D. W. Mahoney, K. R. Bailey, and R. J. Rodeheffer. Burden of systolic and diastolic ventricular dysfunction in the community: appreciating the scope of the heart failure epidemic. JAMA 289(2):194–202, 2003.
Riordan, M. M., and S. J. Kovács. Elucidation of spatially distinct compensatory mechanisms in diastole: radial compensation for impaired longitudinal filling in left ventricular hypertrophy. J. Appl. Physiol. 104(2):513–520, 2008.
Rovner, A., L. de las Fuentes, A. D. Waggoner, N. Memon, R. Chohan, and V. G. Davila-Roman. Characterization of left ventricular diastolic function in hypertension by use of Doppler tissue imaging and color M-mode techniques. J. Am. Soc. Echocardiogr. 19:872–879, 2006.
Sengupta, P. P., B. K. Khandheria, J. Korinek, A. Jahangir, S. Yoshifuku, I. Milosevic, and M. Belohlavek. Left ventricular isovolumic flow sequence during sinus and paced rhythms: new insights from use of high-resolution Doppler and ultrasonic digital particle imaging velocimetry. J. Am. Coll. Cardiol. 49(8):899–908, 2007.
Sengupta, P. P., B. K. Khandheria, J. Korinek, J. Wang, A. Jahangir, J. B. Seward, and M. Belohlavek. Apex-to-base dispersion in regional timing of left ventricular shortening and lengthening. J. Am. Coll. Cardiol. 47:163–172, 2005.
Shortland, A. P., R. A. Black, J. C. Jarvis, F. S. Henry, F. Iudicello, M. W. Collins, and S. Salmons. Formation and travel of vortices in model ventricles: application to the design of skeletal muscle ventricles. J. Biomech. 29(4):503–511, 1996.
Steen, T., and S. Steen. Filling of a model left ventricle studied by colour M mode Doppler. Cardiovasc. Res. 28(12):1821–1827, 1994.
Stewart, K. C., J. C. Charonko, C. L. Niebel, C. Little, and P. P. Vlachos. Left ventricle filling vortex formation is unaffected by diastolic impairment. Am. J. Physiol. Heart Circ. Physiol. 303(10):H1255–H1262, 2012.
Stewart, K. C., R. Kumar, J. J. Charonko, T. Ohara, P. P. Vlachos, and W. C. Little. Evaluation of LV diastolic function from color M-mode echocardiography. J. Am. Coll. Cardiol. Cardiovasc. Imaging 4(1):37–46, 2011.
Stoylen, A., G. Skjelvan, and T. Skjaerpe. Flow propagation velocity is not a simple index of diastolic function in early filling. A comparative study of early diastolic strain rate and strain rate propagation, flow and flow propagation in normal and reduced diastolic function. Cardiovasc. Ultrasound 1(1):3, 2003.
Stugaard, M., U. Brodahl, H. Torp, and H. Ihlen. Abnormalities of left ventricular filling in patients with coronary artery disease: assessment by colour M-mode Doppler technique. Eur. Heart J. 15(3):318–327, 1994.
Thompson, R. B., and E. R. McVeigh. Fast measurement of intracardiac pressure differences with 2D breath-hold phase-contrast MRI. Magn. Reson. Med. 49(6):1056–1066, 2003.
Töger, J., M. Kanski, M. Carlsson, S. Kovács, G. Söderlind, H. Arheden, and E. Heiberg. Vortex ring formation in the left ventricle of the heart: analysis by 4D flow MRI and Lagrangian coherent structures. Ann. Biomed. Eng. 40:2652–2662, 2012.
Tyszka, J. M., D. H. Laidlaw, J. W. Asa, and J. M. Silverman. Three-dimensional, time-resolved (4D) relative pressure mapping using magnetic resonance imaging. J. Magn. Reson. Imaging 12(2):321–329, 2000.
Vierendeels, J. A., E. Dick, and P. R. Verdonck. Hydrodynamics of color M-mode Doppler flow wave propagation velocity V(p): a computer study. J. Am. Soc. Echocardiogr. 15(3):219–224, 2002.
Vierendeels, J. A., K. Riemslagh, E. Dick, and P. R. Verdonck. Computer simulation of intraventricular flow and pressure gradients during diastole. J. Biomech. Eng. 122(6):667–674, 2000.
Westerweel, J., and F. Scarano. Universal outlier detection for PIV data. Exp. Fluids 39(6):1096–1100, 2005.
Zhou, J., R. J. Adrian, S. Balachandar, and T. M. Kendall. Mechanisms for generating coherent packets of hairpin vortices in channel flow. J. Fluid Mech. 387:353–396, 1999.
Acknowledgments
Dr. G. Hundley, MD and Dr. C. Hamilton, PhD are gratefully acknowledged for their help in obtaining the clinical MRI data. The authors would also like to thank Cassie Niebel for her help with image segmentation. This material is based upon work supported under a National Science Foundation Graduate Research Fellowship, National Science Foundation Grant No. 0547434, and a National Institutes of Health R21 Grant No. HL106276-01A1.
Conflict of interest
We confirm that all authors have no conflicts of interest to declare.
Author information
Authors and Affiliations
Corresponding author
Additional information
Associate Editor Aleksander S. Popel oversaw the review of this article.
Electronic supplementary material
Below is the link to the electronic supplementary material.
10439_2013_755_MOESM2_ESM.mpg
Movie S1: Animation of the velocity vectors, relative pressures, and vortical structures for a representative healthy patient. Supplementary material 2 (MPG 645 kb)
10439_2013_755_MOESM3_ESM.mpg
Movie S2: Animation of the velocity vectors, relative pressures, and vortical structures for a representative LVDD patient. Supplementary material 3 (MPG 666 kb)
10439_2013_755_MOESM4_ESM.mpg
Movie S3: Animation of the velocity vectors, relative pressures, and vortical structures for the patient with dilated cardiomyopathy. Supplementary material 4 (MPG 647 kb)
Movie S4: Animation of the FTLE fields for a representative healthy patient, showing LCS and the effect of the vortex pair on the virtual channel. Supplementary material 5 (MPG 349 kb)
Movie S5: Animation of the FTLE fields for a representative LVDD patient, showing LCS and the effect of the vortex pair on the virtual channel. Supplementary material 6 (MPG 372 kb)
Movie S6: Animation of the FTLE fields for the patient with dilated cardiomyopathy, showing LCS and the effect of the vortex pair on the virtual channel. Supplementary material 7 (MPG 350 kb)
Rights and permissions
About this article
Cite this article
Charonko, J.J., Kumar, R., Stewart, K. et al. Vortices Formed on the Mitral Valve Tips Aid Normal Left Ventricular Filling. Ann Biomed Eng 41, 1049–1061 (2013). https://doi.org/10.1007/s10439-013-0755-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10439-013-0755-0