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      Vortex ring behavior provides the epigenetic blueprint for the human heart

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          Abstract

          The laws of fluid dynamics govern vortex ring formation and precede cardiac development by billions of years, suggesting that diastolic vortex ring formation is instrumental in defining the shape of the heart. Using novel and validated magnetic resonance imaging measurements, we show that the healthy left ventricle moves in tandem with the expanding vortex ring, indicating that cardiac form and function is epigenetically optimized to accommodate vortex ring formation for volume pumping. Healthy hearts demonstrate a strong coupling between vortex and cardiac volumes (R 2 = 0.83), but this optimized phenotype is lost in heart failure, suggesting restoration of normal vortex ring dynamics as a new, and possibly important consideration for individualized heart failure treatment. Vortex ring volume was unrelated to early rapid filling (E-wave) velocity in patients and controls. Characteristics of vortex-wall interaction provide unique physiologic and mechanistic information about cardiac diastolic function that may be applied to guide the design and implantation of prosthetic valves, and have potential clinical utility as therapeutic targets for tailored medicine or measures of cardiac health.

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          Most cited references25

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          Fish exploiting vortices decrease muscle activity.

          Fishes moving through turbulent flows or in formation are regularly exposed to vortices. Although animals living in fluid environments commonly capture energy from vortices, experimental data on the hydrodynamics and neural control of interactions between fish and vortices are lacking. We used quantitative flow visualization and electromyography to show that trout will adopt a novel mode of locomotion to slalom in between experimentally generated vortices by activating only their anterior axial muscles. Reduced muscle activity during vortex exploitation compared with the activity of fishes engaged in undulatory swimming suggests a decrease in the cost of locomotion and provides a mechanism to understand the patterns of fish distributions in schools and riverine environments.
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            Mechanotransduction and flow across the endothelial glycocalyx.

            In this inaugural paper, we shall provide an overview of the endothelial surface layer or glycocalyx in several roles: as a transport barrier, as a porous hydrodynamic interface in the motion of red and white cells in microvessels, and as a mechanotransducer of fluid shearing stresses to the actin cortical cytoskeleton of the endothelial cell. These functions will be examined from a new perspective, the quasiperiodic ultrastructural model proposed in Squire et al. [Squire, J. M., Chew, M., Nneji, G., Neal, C., Barry, J. & Michel, C. (2001) J. Struct. Biol. 136, 239-255] for the 3D organization of the endothelial surface layer and its linkage to the submembranous scaffold. We shall show that the core proteins in the bush-like structures comprising the matrix have a flexural rigidity, EI, that is sufficiently stiff to serve as a molecular filter for plasma proteins and as an exquisitely designed transducer of fluid shearing stresses. However, EI is inadequate to prevent the buckling of these protein structures during the intermittent motion of red cells or the penetration of white cell microvilli. In these cellular interactions, the viscous draining resistance of the matrix is essential for preventing adhesive molecular interactions between proteins in the endothelial membrane and circulating cellular components.
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              The vortex--an early predictor of cardiovascular outcome?

              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.
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                Author and article information

                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group
                2045-2322
                26 February 2016
                2016
                : 6
                : 22021
                Affiliations
                [1 ]Lund University, Department of Clinical Sciences Lund, Clinical Physiology, Skane University Hospital , Lund, Sweden
                [2 ]Cardiovascular Biophysics Laboratory, Cardiovascular Division, Washington University School of Medicine , Box 8086, 660 St Euclid Avenue, St. Louis, MO 63110 USA
                [3 ]Dept. of Cardiology, Arrhythmia Clinic, Lund University Hospital, Lund University , 22185 Lund, Sweden
                [4 ]Dept. of Biomedical Engineering, Faculty of Engineering, Lund University , 221 85 Lund, Sweden
                Author notes
                Article
                srep22021
                10.1038/srep22021
                4768103
                26915473
                e9e6f398-007a-43cb-8bca-8e8c250a9504
                Copyright © 2016, Macmillan Publishers Limited

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 30 September 2015
                : 05 February 2016
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