Abstract
Blood motion in the heart features vortices that accompany the redirection of jet flows towards the outlet tracks. Vortices have a crucial role in fluid dynamics. The stability of cardiac vorticity is vital to the dynamic balance between rotating blood and myocardial tissue and to the development of cardiac dysfunction. Moreover, vortex dynamics immediately reflect physiological changes to the surrounding system, and can provide early indications of long-term outcome. However, the pathophysiological relevance of cardiac fluid dynamics is still unknown. We postulate that maladaptive intracardiac vortex dynamics might modulate the progressive remodelling of the left ventricle towards heart failure. The evaluation of blood flow presents a new paradigm in cardiac function analysis, with the potential for sensitive risk identification of cardiac abnormalities. Description of cardiac flow patterns after surgery or device therapy provides an intrinsic qualitative evaluation of therapeutic procedures, and could enable early risk stratification of patients vulnerable to adverse cardiac remodelling.
Similar content being viewed by others
References
Kilner, P. J. et al. Asymmetric redirection of flow through the heart. Nature 404, 759–761 (2000).
Pedrizzetti, G. & Domenichini, F. Nature optimizes the swirling flow in the human left ventricle. Phys. Rev. Lett. 95, 108101 (2005).
Lancellotti, P. et al. Recommendations for the echocardiographic assessment of native valvular regurgitation: an executive summary from the European Association of Cardiovascular Imaging. Eur. Heart J. Cardiovasc. Imaging 14, 611–644 (2013).
Nagueh, S. F. et al. Recommendations for the evaluation of left ventricular diastolic function by echocardiography. J. Am. Soc. Echocardiogr. 22, 107–133 (2009).
Brutsaert, D. L., Rademakers, F. E., Sys, S. U., Gillebert, T. C. & Housmans, P. R. Analysis of relaxation in the evaluation of ventricular function of the heart. Prog. Cardiovasc. Dis. 28, 143–163 (1985).
Sengupta, P. P. et al. Left ventricular structure and function: basic science for cardiac imaging. J. Am. Coll. Cardiol. 48, 1988–2001 (2006).
Buckberg, G., Hoffman, J. I., Mahajan, A., Saleh, S. & Coghlan, C. Cardiac mechanics revisited: the relationship of cardiac architecture to ventricular function. Circulation 118, 2571–2587 (2008).
Vendelin, M., Bovendeerd, P. H., Engelbrecht, J. & Arts, T. Optimizing ventricular fibres: uniform strain or stress, but not ATP consumption, leads to high efficiency. Am. J. Physiol. Heart Circ. Physiol. 283, H1072–H1081 (2002).
Dong, S. J., Hees, P. S., Siu, C. O., Weiss, J. L. & Shapiro, E. P. MRI assessment of LV relaxation by untwisting rate: a new isovolumic phase measure of tau. Am. J. Physiol. Heart Circ. Physiol. 281, H2002–H2009 (2001).
Geerts L., Bovendeerd, P., Nicolay, K. & Arts, T. Characterization of the normal cardiac myofibre field in goat measured with MR-diffusion tensor imaging. Am. J. Physiol. Heart Circ. Physiol. 283, H139–H145 (2002).
Notomi, Y. et al. Ventricular untwisting: a temporal link between left ventricular relaxation and suction. Am. J. Physiol. Heart Circ. Physiol. 294, H505–H513 (2008).
Burns, A. T., La Gerche, A., Prior, D. L. & Macisaac, A. I. Left ventricular untwisting is an important determinant of early diastolic function. JACC Cardiovasc. Imaging 2, 709–716 (2009).
Leite-Moreira, A. F. & Gillebert, T. C. Nonuniform course of left ventricular pressure fall and its regulation by load and contractile state. Circulation 90, 2481–2491 (1994).
Sengupta, P. P. et al. Emerging trends in CV flow visualization. JACC Cardiovasc. Imaging 5, 305–316 (2012).
Courtois, M., Kovacs, S. J. Jr & Ludbrook, P. A. Transmitral pressure-flow velocity relation: Importance of regional pressure gradients in the left ventricle during diastole. Circulation 78, 661–671 (1988).
Vierendeels, J. A., Riemslagh, K., Dick, E. & Verdonck, P. R. Computer simulation of intraventricular flow and pressure gradients during diastole. J. Biomech. Eng. 122, 667–674 (2000).
Ebbers, T., Wigström, L., Bolger, A. F., Wranne, B. & Karlsson, M. Noninvasive measurement of time-varying threedimensional relative pressure fields within the human heart. J. Biomech. Eng. 124, 288–293 (2002).
Domenichini, F., Pedrizzetti, G. & Baccani, B. Three-dimensional filling flow into a model left ventricle. J. Fluid Mech. 539, 179–198 (2005).
Markl, M., Kilner, P. J. & Ebbers, T. Comprehensive 4D velocity mapping of the heart and great vessels by cardiovascular magnetic resonance. J. Cardiovasc. Magn. Reson. 13, 7 (2011).
Bolger, A. F. et al. Transit of blood flow through the human left ventricle mapped by cardiovascular magnetic resonance. J. Cardiovasc. Magn. Reson. 9, 741–747 (2007).
Eriksson, J. et al. Semi-automatic quantification of 4D left ventricular blood flow. J. Cardiovasc. Magn. Reson. 12, 9 (2010).
Carlhäll, C. J. & Bolger, A. Passing strange: flow in the failing ventricle. Circ. Heart Fail. 3, 326–331 (2010).
Adrian, R. J. Twenty years of particle image velocimetry. Exp. Fluids 39, 159–169 (2005).
Kim, H., Hertzberg, J. & Shandas, R. Development and validation of echo PIV. Exp. Fluids 36, 455–462 (2004).
Zhang, F. et al. In vitro and preliminary in vivo validation of echo particle image velocimetry in carotid vascular imaging. Ultrasound Med. Biol. 37, 450–464 (2011).
Kheradvar, A. et al. Echographic particle image velocimetry: a novel technique for quantification of left ventricular blood vorticity pattern. J. Am. Soc. Echocardiogr. 23, 86–94 (2010).
Westerdale, J. et al. Flow velocity vector fields by ultrasound particle imaging velocimetry: in vitro comparison with optical flow velocimetry. J. Ultras. Med. 30, 187–195 (2011).
Sengupta, P. P. et al. 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, 899–908 (2007).
Hong, G. R. et al. Characterization and quantification of vortex flow in the human left ventricle by contrast echocardiography using vector particle image velocimetry. JACC Cardiovasc. Imaging 1, 705–717 (2008).
Sengupta, P. P., Pedrizzetti, G. & Narula, J. Multiplanar visualization of blood flow using echocardiographic particle imaging velocimetry. JACC Cardiovasc. Imaging 5, 566–569 (2012).
Wallace, J. M. Twenty years of experimental and direct numerical simulation access to the velocity gradient tensor: what have we learned about turbulence? Phys. Fluids 21, 021301 (2009).
Wallace, J. M. & Vukoslavcevic, P. V. Measurement of the velocity gradient tensor in turbulent flows. Ann. Rev. Fluid Mech. 42, 157–181 (2010).
Cimino, S. et al. In vivo analysis of intraventricular fluid dynamics in healthy hearts. Eur. J. Mech. B-Fluids 35, 40–46 (2012).
Gharib, M., Rambod, E., Kheradvar, A., Sahn, D. J. & Dabiri, J. O. Optimal vortex formation as an index of cardiac health. Proc. Natl Acad. Sci. USA 103, 6305–6308 (2006).
Son, J. W. et al. Abnormal left ventricular vortex flow patterns in association with left ventricular apical thrombus formation in patients with anterior myocardial infarction: a quantitative analysis by contrast echocardiography. Circ. J. 76, 2640–2646 (2012).
Mangual, J. O. et al. Comparative numerical study on left ventricular fluid dynamics after dilated cardiomyopathy. J. Biomech. 46, 1611–1617 (2013).
Abe, H. et al. Contrast echocardiography for assessing left ventricular vortex strength in heart failure: a prospective cohort study. Eur. Heart J. Cardiovasc. Imaging 14, 1049–1060 (2013).
Goliasch, G. et al. CRT improves LV filling dynamics: insights from echocardiographic particle imaging velocimetry. JACC Cardiovasc. Imaging 6, 704–713 (2013).
Cohn, J. N., Ferrari, R. & Sharpe, N. Cardiac remodeling—concepts and clinical implications: a consensus paper from an International Forum on Cardiac Remodeling. J. Am. Coll. Cardiol. 35, 569–582 (2000).
Kehat, I. & Molkentin, J. D. Molecular pathways underlying cardiac remodeling during pathophysiological stimulation. Circulation 122, 2727–2735 (2010).
Steenman, M. et al. Transcriptomal analysis of failing and nonfailing human hearts. Physiol. Genomics 12, 97–112 (2003).
Asakura, M. & Kitakaze, M. Global gene expression profiling in the failing myocardium. Circ. J. 73, 1568–1576 (2009).
Hill, J. A. & Olson, E. N. Cardiac plasticity. N. Engl. J. Med. 358, 1370–1380 (2008).
Verma, A. et al. Prognostic implication of left ventricular mass and geometry following myocardial infarction: the VALIANT (VALsartan In Acute myocardial iNfarcTion) Echocardiographic Study. JACC Cardiovasc. Imaging 1, 582–591 (2008).
Sengupta, P. P. & Narula, J. Reclassifying heart failure: predominantly subendocardial, subepicardial, and transmural. Heart Fail. Clin. 4, 379–382 (2008).
Wu, E. et al. Infarct size by contrast enhanced cardiac magnetic resonance is a stronger predictor of outcomes than left ventricular ejection fraction or end-systolic volume index: prospective cohort study. Heart 94, 730–736 (2008).
Nijveldt, R. et al. Assessment of microvascular obstruction and prediction of short-term remodeling after acute myocardial infarction: cardiac MR imaging study. Radiology 250, 363–370 (2009).
Hein, S., Kostin, S., Heling, A., Maeno, Y. & Schaper, J. The role of the cytoskeleton in heart failure. Cardiovasc. Res. 45, 273–278 (2000).
Baccarelli, A., Rienstra, M. & Benjamin, E. J. Cardiovascular epigenetic basic concepts and results from animal and human studies. Circ. Cardiovasc. Genet. 3, 567–573 (2010).
Chaturvedi, P. & Tyagi, S. C. Epigenetic mechanisms underlying cardiac degeneration and regeneration. Int. J. Cardiol. 173, 1–11 (2014).
Hove, J. R. et al. Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis. Nature 421, 172–177 (2003).
Liew, C. C. & Dzau, V. J. Molecular genetics and genomics of heart failure. Nat. Rev. Genet. 5, 811–825 (2004).
Pasipoularides, A. Diastolic filling vortex forces and cardiac adaptations: probing the epigenetic nexus. Hellenic J. Cardiol. 53, 458–469 (2012).
Zhang, J. & Friedman, M. H. Adaptive response of vascular endothelial cells to an acute increase in shear stress magnitude. Am. J. Physiol. Heart Circ. Physiol. 302, H983–H991 (2012).
Eriksson, J., Bolger, A. F., Ebbers, T. & Carlhäll, C. J. Four-dimensional blood flow-specific markers of LV dysfunction in dilated cardiomyopathy. Eur. Heart J. Cardiovasc. Imaging 14, 417–424 (2013).
Ross, J. Jr. Afterload mismatch in aortic and mitral valve disease: implications for surgical therapy. J. Am. Coll. Cardiol. 5, 811–826 (1985).
Vahanian, A. et al. Guidelines on the management of valvular heart disease (version 2012). Eur. Heart J. 33, 2451–2496 (2012).
Nishimura, R. A. et al. 2014 AHA/ACC guideline for the management of patients with valvular heart disease: executive summary: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. Circulation http://dx.doi.org/10.1161/CIR.0000000000000029.
Faludi, R. et al. Left ventricular flow patterns in healthy subjects and patients with prosthetic mitral valves: an in vivo study using echocardiographic particle image velocimetry. J. Thorac. Cardiovasc. Surg. 139, 1501–1510 (2010).
Pedrizzetti, G., Domenichini, F. & Tonti, G. On the left ventricular vortex reversal after mitral valve replacement. Ann. Biomed. Eng. 38, 769–773 (2010).
Adhyapak, S. M. & Parachuri, R. V. Architecture of the left ventricle: insights for optimal surgical ventricular restoration. Heart Fail. Rev. 15, 73–83 (2010).
George, T. J., Arnaoutakis, G. J. & Shah, A. S. Surgical treatment of advanced heart failure: alternatives to heart transplantation and mechanical circulatory assist devices. Prog. Cardiovasc. Dis. 54, 115–131 (2011).
Buckberg, G., Athanasuleas, C. & Conte, J. Surgical ventricular restoration for the treatment of heart failure. Nat. Rev. Cardiol. 9, 703–716 (2012).
Doenst, T. et al. Fluid-dynamic modeling of the human left ventricle: methodology and application to surgical ventricular reconstruction. Ann. Thorac. Surg. 87, 1187–1195 (2009).
Liakopoulos, O. J. et al. Sequential deformation and physiological considerations in unipolar right or left ventricular pacing. Eur. J. Cardiothorac. Surg. 29 (Suppl. 1), S188–S197 (2006).
Guerra, M., Amorim, M. J., Brás-Silva, C. & Leite-Moreira, A. F. Intraventricular pressure gradients throughout the cardiac cycle: effects of ischaemia and modulation by afterload. Exp. Physiol. 98, 149–160 (2013).
D'Ascia, C., Cittadini, A., Monti, M. G., Riccio, G. & Saccà, L. Effects of biventricular pacing on interstitial remodelling, tumour necrosis factor alpha expression, and apoptotic death in failing human myocardium. Eur. Heart J. 27, 201–206 (2006).
Orrego, C. M. et al. Cellular evidence of reverse cardiac remodeling induced by cardiac resynchronization therapy. Congest. Heart Fail. 17, 140–146 (2011).
McGarvey, J. R. et al. Directed epicardial assistance in ischemic cardiomyopathy: flow and function using cardiac magnetic resonance imaging. Ann. Thorac. Surg. 96, 577–585 (2013).
Peura, J. L. et al. Recommendations for the use of mechanical circulatory support: device strategies and patient selection: a scientific statement from the American Heart Association. Circulation 126, 2648–2667 (2012).
Birks, E. J. & George, R. S. Molecular changes occurring during reverse remodelling following left ventricular assist device support. J. Cardiovasc. Transl. Res. 3, 635–642 (2010).
Malliaras, K. G., Terrovitis, J. V., Drakos, S. G. & Nanas J. N. Reverse cardiac remodeling enabled by mechanical unloading of left ventricle. J. Cardiovasc. Transl. Res. 2, 114–125 (2009).
Felkin, L. E., Lara-Pezzi, E. A., Hall, J. L., Birks, E. J. & Barton, P. J. Reverse remodelling and recovery from heart failure are associated with complex patterns of gene expression. J. Cardiovasc. Transl. Res. 4, 321–331 (2011).
Acknowledgements
The authors thank Michael John of the Vita-Salute San Raffaele University in Milan, Italy for his support in the preparation of this paper.
Author information
Authors and Affiliations
Contributions
All the authors researched data for the article, discussed its content, wrote the manuscript, and reviewed/edited it before submission.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Rights and permissions
About this article
Cite this article
Pedrizzetti, G., La Canna, G., Alfieri, O. et al. The vortex—an early predictor of cardiovascular outcome?. Nat Rev Cardiol 11, 545–553 (2014). https://doi.org/10.1038/nrcardio.2014.75
Published:
Issue Date:
DOI: https://doi.org/10.1038/nrcardio.2014.75
- Springer Nature Limited
This article is cited by
-
Inter-study reproducibility of cardiovascular magnetic resonance-derived hemodynamic force assessments
Scientific Reports (2024)
-
Enhancement of intra-cardiac flow-field data using adaptive Kernel filtering
Scientific Reports (2023)
-
Evaluation of left ventricular blood flow kinetic energy in patients with hypertension by four-dimensional flow cardiovascular magnetic resonance imaging: a preliminary study
European Radiology (2023)
-
Hemodynamic force analysis is not ready for clinical trials on HFpEF
Scientific Reports (2022)
-
Surrogate models provide new insights on metrics based on blood flow for the assessment of left ventricular function
Scientific Reports (2022)