Wall Shear Stress Directional Abnormalities in BAV Aortas: Toward a New Hemodynamic Predictor of Aortopathy?

The bicuspid aortic valve (BAV) generates wall shear stress (WSS) abnormalities in the ascending aorta (AA) that may be responsible for the high prevalence of aortopathy in BAV patients. While previous studies have analyzed the magnitude and oscillatory characteristics of the total or streamwise WSS in BAV AAs, the assessment of the circumferential component is lacking despite its expected significance in this highly helical flow environment. This gap may have hampered the identification of a robust hemodynamic predictor of BAV aortopathy. The objective of this study was to perform a global and component-specific assessment of WSS magnitude, oscillatory and directional characteristics in BAV AAs. The WSS environments were computed in the proximal and middle convexity of tricuspid aortic valve (TAV) and BAV AAs using our previous valve-aorta fluid-structure interaction (FSI) models. Component-specific WSS characteristics were investigated in terms of temporal shear magnitude (TSM) and oscillatory shear index (OSI). WSS directionality was quantified in terms of mean WSS vector magnitude and angle, and angular dispersion index (Dα). Local WSS magnitude and multidirectionality were captured in a new shear magnitude and directionality index (SMDI) calculated as the product of the mean WSS magnitude and Dα. BAVs subjected the AA to circumferential TSM overloads (2.4-fold increase vs. TAV). TAV and BAV AAs exhibited a unidirectional circumferential WSS (OSI < 0.04) and an increasingly unidirectional longitudinal WSS between the proximal (OSI > 0.21) and middle (OSI < 0.07) sections. BAVs generated mean WSS vectors skewed toward the anterior wall and WSS angular distributions exhibiting decreased uniformity in the proximal AA (0.27-point increase in Dα vs. TAV). SMDI was elevated in all BAV AAs but peaked in the proximal LR-BAV AA (3.6-fold increase vs. TAV) and in the middle RN-BAV AA (1.6-fold increase vs. TAV). This analysis demonstrates the significance of the circumferential WSS component and the existence of substantial WSS directional abnormalities in BAV AAs. SMDI abnormality distributions in BAV AAs follow the morphotype-dependent occurrence of dilation in BAV AAs, suggesting the predictive potential of this metric for BAV aortopathy.

[1]  R. Goodman,et al.  Bicuspid Aortic Valve Disease and Ascending Aortic Aneurysms: Gaps in Knowledge , 2012, Cardiology research and practice.

[2]  Y. Bossé,et al.  The pathology and pathobiology of bicuspid aortic valve: State of the art and novel research perspectives† , 2015, The journal of pathology. Clinical research.

[3]  P. Sucosky,et al.  Effect of Bicuspid Aortic Valve Cusp Fusion on Aorta Wall Shear Stress: Preliminary Computational Assessment and Implication for Aortic Dilation , 2015 .

[4]  M. Markl,et al.  Aortic Valve Stenosis Alters Expression of Regional Aortic Wall Shear Stress: New Insights From a 4‐Dimensional Flow Magnetic Resonance Imaging Study of 571 Subjects , 2017, Journal of the American Heart Association.

[5]  A. Quarteroni,et al.  Fluid―structure interaction simulation of aortic blood flow , 2011 .

[6]  P. Sucosky,et al.  Three-dimensional macro-scale assessment of regional and temporal wall shear stress characteristics on aortic valve leaflets , 2016, Computer methods in biomechanics and biomedical engineering.

[7]  Janet Liu.  Design of a Novel Tissue Culture System to Subject Aortic Tissue to Multidirectional Bicuspid Aortic Valve Wall Shear Stress , 2018 .

[8]  Stefan Neubauer,et al.  Aortic Dilation in Bicuspid Aortic Valve Disease: Flow Pattern Is a Major Contributor and Differs With Valve Fusion Type , 2013, Circulation. Cardiovascular imaging.

[9]  R. Hetzer,et al.  Configuration of the ascending aorta in patients with bicuspid and tricuspid aortic valve disease undergoing aortic valve replacement with or without reduction aortoplasty. , 2006, The Journal of heart valve disease.

[10]  A. Barker,et al.  Quantification of Hemodynamic Wall Shear Stress in Patients with Bicuspid Aortic Valve Using Phase-Contrast MRI , 2010, Annals of Biomedical Engineering.

[11]  M. Moon,et al.  The bicuspid aortic valve. , 2005, Current problems in cardiology.

[12]  H. Sievers,et al.  A classification system for the bicuspid aortic valve from 304 surgical specimens. , 2007, The Journal of thoracic and cardiovascular surgery.

[13]  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.

[14]  Nicholas I. Fisher,et al.  Statistical Analysis of Circular Data , 1993 .

[15]  A. Ranga,et al.  A Compliant Dynamic FEA Model of the Aortic Valve , 2007 .

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

[17]  L. Trombley,et al.  Matrix metalloproteinase activity in thoracic aortic aneurysms associated with bicuspid and tricuspid aortic valves. , 2004, The Journal of thoracic and cardiovascular surgery.

[18]  B. Strauss,et al.  Vascular matrix remodeling in patients with bicuspid aortic valve malformations: implications for aortic dilatation. , 2003, The Journal of thoracic and cardiovascular surgery.

[19]  J. Jue,et al.  Patterns of aortic dilatation in bicuspid aortic valve-associated aortopathy. , 2013, Journal of the American Society of Echocardiography : official publication of the American Society of Echocardiography.

[20]  Alfio Quarteroni,et al.  Helical flows and asymmetry of blood jet in dilated ascending aorta with normally functioning bicuspid valve , 2012, Biomechanics and Modeling in Mechanobiology.

[21]  H. Nagaraja,et al.  The aortic stenosis complex: aortic valve, atherosclerosis, aortopathy. , 2015, Journal of cardiology.

[22]  A. Della Corte,et al.  Different patterns of extracellular matrix protein expression in the convexity and the concavity of the dilated aorta with bicuspid aortic valve: preliminary results. , 2005, The Journal of thoracic and cardiovascular surgery.

[23]  Y. Bossé,et al.  Bicuspid aortic valve: identifying knowledge gaps and rising to the challenge from the International Bicuspid Aortic Valve Consortium (BAVCon). , 2014, Circulation.

[24]  S. Siu,et al.  Outcomes in adults with bicuspid aortic valves. , 2008, JAMA.

[25]  Simon C Watkins,et al.  Mechanism of aortic medial matrix remodeling is distinct in patients with bicuspid aortic valve. , 2014, The Journal of thoracic and cardiovascular surgery.

[26]  Samantha K. Atkins,et al.  Bicuspid aortic valve hemodynamics does not promote remodeling in porcine aortic wall concavity. , 2016, World journal of cardiology.

[27]  Ajit P Yoganathan,et al.  Design of an ex vivo culture system to investigate the effects of shear stress on cardiovascular tissue. , 2008, Journal of biomechanical engineering.

[28]  A. Della Corte,et al.  Spatiotemporal patterns of smooth muscle cell changes in ascending aortic dilatation with bicuspid and tricuspid aortic valve stenosis: focus on cell-matrix signaling. , 2008, The Journal of thoracic and cardiovascular surgery.

[29]  Samantha K. Atkins,et al.  Etiology of bicuspid aortic valve disease: Focus on hemodynamics. , 2014, World journal of cardiology.

[30]  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.

[31]  H. Baumgartner,et al.  Mechanisms underlying aortic dilatation in congenital aortic valve malformation. , 1999, Circulation.

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

[33]  Jianwen Luo,et al.  In vivo characterization of the aortic wall stress-strain relationship. , 2010, Ultrasonics.

[34]  Michael Markl,et al.  Bicuspid Aortic Cusp Fusion Morphology Alters Aortic Three-Dimensional Outflow Patterns, Wall Shear Stress, and Expression of Aortopathy , 2014, Circulation.

[35]  T. Tadros,et al.  Ascending aortic dilatation associated with bicuspid aortic valve: pathophysiology, molecular biology, and clinical implications. , 2009, Circulation.

[36]  Janet Liu,et al.  Simulations of morphotype-dependent hemodynamics in non-dilated bicuspid aortic valve aortas. , 2017, Journal of biomechanics.

[37]  P. Walker,et al.  Abnormal Extracellular Matrix Protein Transport Associated With Increased Apoptosis of Vascular Smooth Muscle Cells in Marfan Syndrome and Bicuspid Aortic Valve Thoracic Aortic Aneurysm , 2003, Circulation.

[38]  Michael Markl,et al.  Wall shear stress and flow patterns in the ascending aorta in patients with bicuspid aortic valves differ significantly from tricuspid aortic valves: a prospective study. , 2013, European heart journal cardiovascular Imaging.

[39]  Masanori Nakamura,et al.  Patient‐specific assessment of hemodynamics by computational fluid dynamics in patients with bicuspid aortopathy , 2017, The Journal of thoracic and cardiovascular surgery.

[40]  B. Prendergast,et al.  Aortic Dilation in Bicuspid Aortic Valve DiseaseClinical Perspective , 2013 .

[41]  A. Yoganathan,et al.  Bicuspid aortic valves are associated with increased wall and turbulence shear stress levels compared to trileaflet aortic valves , 2014, Biomechanics and Modeling in Mechanobiology.

[42]  Jong-Min Song,et al.  Association between bicuspid aortic valve phenotype and patterns of valvular dysfunction and bicuspid aortopathy: comprehensive evaluation using MDCT and echocardiography. , 2013, JACC. Cardiovascular imaging.

[43]  Jeffery A. Jones,et al.  xpression of matrix metalloproteinases and endogenous nhibitors within ascending aortic aneurysms of patients ith bicuspid or tricuspid aortic valves , 2007 .

[44]  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.

[45]  Michael D Hope,et al.  4D flow CMR in assessment of valve-related ascending aortic disease. , 2011, JACC. Cardiovascular imaging.

[46]  A. Redaelli,et al.  4D Flow Analysis of BAV-Related Fluid-Dynamic Alterations: Evidences of Wall Shear Stress Alterations in Absence of Clinically-Relevant Aortic Anatomical Remodeling , 2017, Front. Physiol..

[47]  S. Body,et al.  Pathogenic Mechanisms of Bicuspid Aortic Valve Aortopathy , 2017, Front. Physiol..

[48]  Andrew McNally,et al.  Morphotype-Dependent Flow Characteristics in Bicuspid Aortic Valve Ascending Aortas: A Benchtop Particle Image Velocimetry Study , 2017, Front. Physiol..