Three-dimensional macro-scale assessment of regional and temporal wall shear stress characteristics on aortic valve leaflets

The aortic valve (AV) achieves unidirectional blood flow between the left ventricle and the aorta. Although hemodynamic stresses have been shown to regulate valvular biology, the native wall shear stress (WSS) experienced by AV leaflets remains largely unknown. The objective of this study was to quantify computationally the macro-scale leaflet WSS environment using fluid–structure interaction modeling. An arbitrary Lagrangian–Eulerian approach was implemented to predict valvular flow and leaflet dynamics in a three-dimensional AV geometry subjected to physiologic transvalvular pressure. Local WSS characteristics were quantified in terms of temporal shear magnitude (TSM), oscillatory shear index (OSI) and temporal shear gradient (TSG). The dominant radial WSS predicted on the leaflets exhibited high amplitude and unidirectionality on the ventricularis (TSM>7.50 dyn/cm2, OSI < 0.17, TSG>325.54 dyn/cm2 s) but low amplitude and bidirectionality on the fibrosa (TSM < 2.73 dyn/cm2, OSI>0.38, TSG < 191.17 dyn/cm2 s). The radial WSS component computed in the leaflet base, belly and tip demonstrated strong regional variability (ventricularis TSM: 7.50–22.32 dyn/cm2, fibrosa TSM: 1.26–2.73 dyn/cm2). While the circumferential WSS exhibited similar spatially dependent magnitude (ventricularis TSM: 1.41–3.40 dyn/cm2, fibrosa TSM: 0.42–0.76 dyn/cm2) and side-specific amplitude (ventricularis TSG: 101.73–184.43 dyn/cm2 s, fibrosa TSG: 41.92–54.10 dyn/cm2 s), its temporal variations were consistently bidirectional (OSI>0.25). This study provides new insights into the role played by leaflet–blood flow interactions in valvular function and critical hemodynamic stress data for the assessment of the hemodynamic theory of AV disease.

[1]  B J Bellhouse,et al.  Fluid mechanics of the aortic valve. , 1969, British heart journal.

[2]  Y. Missirlis,et al.  Aortic valve mechanics--Part I: material properties of natural porcine aortic valves. , 1978, Journal of bioengineering.

[3]  J. Halleux,et al.  An arbitrary lagrangian-eulerian finite element method for transient dynamic fluid-structure interactions , 1982 .

[4]  I. Shbeeb,et al.  The aortic valve , 1984, Diseases of the colon and rectum.

[5]  K. Matre,et al.  Velocity distributions in the left ventricular outflow tract and the aortic anulus measured with Doppler colour flow mapping in normal subjects. , 1993, European heart journal.

[6]  D. Ku BLOOD FLOW IN ARTERIES , 1997 .

[7]  M. Yacoub,et al.  Asymmetric redirection of flow through the heart , 2000, Nature.

[8]  M. Sacks,et al.  Biaxial mechanical properties of the natural and glutaraldehyde treated aortic valve cusp--Part I: Experimental results. , 2000, Journal of biomechanical engineering.

[9]  G. G. Peters,et al.  A two-dimensional fluid–structure interaction model of the aortic value , 2000 .

[10]  F P T Baaijens,et al.  A three-dimensional computational analysis of fluid-structure interaction in the aortic valve. , 2003, Journal of biomechanics.

[11]  Karyn S Kunzelman,et al.  A coupled fluid-structure finite element model of the aortic valve and root. , 2003, The Journal of heart valve disease.

[12]  F P T Baaijens,et al.  A computational fluid-structure interaction analysis of a fiber-reinforced stentless aortic valve. , 2003, Journal of biomechanics.

[13]  Ajit P Yoganathan,et al.  Fluid mechanics of heart valves. , 2004, Annual review of biomedical engineering.

[14]  Ajit P. Yoganathan,et al.  Estimation of the Shear Stress on the Surface of an Aortic Valve Leaflet , 1999, Annals of Biomedical Engineering.

[15]  K. J. Grande,et al.  Stress Variations in the Human Aortic Root and Valve: The Role of Anatomic Asymmetry , 1998, Annals of Biomedical Engineering.

[16]  A. Yoganathan,et al.  Biofluid Mechanics: The Human Circulation , 2006 .

[17]  Hwa Liang Leo,et al.  Fluid Dynamic Assessment of Three Polymeric Heart Valves Using Particle Image Velocimetry , 2006, Annals of Biomedical Engineering.

[18]  Eli J Weinberg,et al.  Transient, Three-dimensional, Multiscale Simulations of the Human Aortic Valve , 2007, Cardiovascular engineering.

[19]  A. Yoganathan,et al.  Heart valve function: a biomechanical perspective , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[20]  C. Simmons,et al.  Mechanobiology of the aortic heart valve. , 2008, The Journal of heart valve disease.

[21]  Ajit P Yoganathan,et al.  Altered Shear Stress Stimulates Upregulation of Endothelial VCAM-1 and ICAM-1 in a BMP-4– and TGF-&bgr;1–Dependent Pathway , 2009, Arteriosclerosis, thrombosis, and vascular biology.

[22]  Ajit P. Yoganathan,et al.  Altered Shear Stress Stimulates Upregulation of Endothelial VCAM-1 and ICAM-1 in a BMP-4- and TGF-β1-Dependent Pathway , 2009 .

[23]  Ajit P Yoganathan,et al.  Advances in Cardiovascular Fluid Mechanics: Bench to Bedside , 2009, Annals of the New York Academy of Sciences.

[24]  G. Woodruff,et al.  BLOOD FLOW IN ARTERIES , 2009 .

[25]  Eli J. Weinberg,et al.  A Computational Model of Aging and Calcification in the Aortic Heart Valve , 2009, PloS one.

[26]  W. David Merryman Mechano-potential etiologies of aortic valve disease. , 2010, Journal of biomechanics.

[27]  Philippe Sucosky,et al.  Role of Pathologic Shear Stress Alterations in Aortic Valve Endothelial Activation , 2010 .

[28]  W. D. Merryman Mechano-potential etiologies of aortic valve disease. , 2010 .

[29]  Fotis Sotiropoulos,et al.  Direction and magnitude of blood flow shear stresses on the leaflets of aortic valves: is there a link with valve calcification? , 2010, Journal of biomechanical engineering.

[30]  Jia Lu,et al.  Fluid–structure interaction methods in biological flows with special emphasis on heart valve dynamics , 2010 .

[31]  Jürgen Hennig,et al.  Assessment of flow instabilities in the healthy aorta using flow‐sensitive MRI , 2011, Journal of magnetic resonance imaging : JMRI.

[32]  Ajit P. Yoganathan,et al.  Hemodynamics and Mechanobiology of Aortic Valve Inflammation and Calcification , 2011, International journal of inflammation.

[33]  Matts Karlsson,et al.  WALL SHEAR STRESS IN A SUBJECT SPECIFIC HUMAN AORTA - INFLUENCE OF FLUID-STRUCTURE INTERACTION , 2011 .

[34]  Michael Markl,et al.  Bicuspid Aortic Valve Is Associated With Altered Wall Shear Stress in the Ascending Aorta , 2012, Circulation. Cardiovascular imaging.

[35]  A. Yoganathan,et al.  Experimental measurement of dynamic fluid shear stress on the aortic surface of the aortic valve leaflet , 2011, Biomechanics and Modeling in Mechanobiology.

[36]  Santanu Chandra,et al.  Ex Vivo Evidence for the Contribution of Hemodynamic Shear Stress Abnormalities to the Early Pathogenesis of Calcific Bicuspid Aortic Valve Disease , 2012, PloS one.

[37]  Santanu Chandra,et al.  Computational assessment of bicuspid aortic valve wall-shear stress: implications for calcific aortic valve disease , 2012, Biomechanics and modeling in mechanobiology.

[38]  A. Yoganathan,et al.  Experimental measurement of dynamic fluid shear stress on the ventricular surface of the aortic valve leaflet , 2011, Biomechanics and Modeling in Mechanobiology.

[39]  Mor Peleg,et al.  Fluid-structure interaction model of aortic valve with porcine-specific collagen fiber alignment in the cusps. , 2013, Journal of biomechanical engineering.

[40]  Emiliano Votta,et al.  Impact of modeling fluid-structure interaction in the computational analysis of aortic root biomechanics. , 2013, Medical engineering & physics.

[41]  N. Rajamannan,et al.  Bicuspid Aortic Valve Disease: From Bench to Bedside , 2013 .

[42]  N. Rajamannan,et al.  Defining the Role of Fluid Shear Stress in the Expression of Early Signaling Markers for Calcific Aortic Valve Disease , 2013, PloS one.

[43]  N. Rajamannan,et al.  Bicuspid aortic valve hemodynamics induces abnormal medial remodeling in the convexity of porcine ascending aortas , 2014, Biomechanics and Modeling in Mechanobiology.

[44]  Clara Seaman,et al.  Steady flow hemodynamic and energy loss measurements in normal and simulated calcified tricuspid and bicuspid aortic valves. , 2014, Journal of biomechanical engineering.

[45]  Brandon L. Moore,et al.  Spatiotemporal complexity of the aortic sinus vortex , 2014, Experiments in Fluids.

[46]  P. Sucosky Hemodynamic Mechanisms of Bicuspid Aortic Valve Calcification and Aortopathy , 2014 .

[47]  Akihiko Ikeda,et al.  The Konno Procedure in Redo Aortic Valve Replacement after the Nicks Procedure. , 2015, The Journal of heart valve disease.

[48]  Clara Seaman,et al.  Generation of Simulated Calcific Lesions in Valve Leaflets for Flow Studies. , 2015, The Journal of heart valve disease.