Computational assessment of bicuspid aortic valve wall-shear stress: implications for calcific aortic valve disease
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Abstract
The bicuspid aortic valve (BAV) is associated with a high prevalence of calcific aortic valve disease (CAVD). Although abnormal hemodynamics has been proposed as a potential pathogenic contributor, the native BAV hemodynamic stresses remain largely unknown. Fluid-structure interaction models were designed to quantify the regional BAV leaflet wall-shear stress over the course of CAVD. Systolic flow and leaflet dynamics were computed in two-dimensional tricuspid aortic valve (TAV) and type-1 BAV geometries with different degree of asymmetry (10 and 16% eccentricity) using an arbitrary Lagrangian–Eulerian approach. Valvular performance and regional leaflet wall-shear stress were quantified in terms of valve effective orifice area (EOA), oscillatory shear index (OSI) and temporal shear magnitude (TSM). The dependence of those characteristics on the degree of leaflet calcification was also investigated. The models predicted an average reduction of 49% in BAV peak-systolic EOA relative to the TAV. Regardless of the anatomy, the leaflet wall-shear stress was side-specific and characterized by high magnitude and pulsatility on the ventricularis and low magnitude and oscillations on the fibrosa. While the TAV and non-coronary BAV leaflets shared similar shear stress characteristics, the base of the fused BAV leaflet fibrosa exhibited strong abnormalities, which were modulated by the degree of calcification (6-fold, 10-fold and 16-fold TSM increase in the normal, mildly and severely calcified BAV, respectively, relative to the normal TAV). This study reveals the existence of major differences in wall-shear stress pulsatility and magnitude on TAV and BAV leaflets. Given the ability of abnormal fluid shear stress to trigger valvular inflammation, the results support the existence of a mechano-etiology of CAVD in the BAV.
Keywords
Bicuspid aortic valve Calcification Fluid-structure interaction modeling Shear stress Blood flow Arbitrary Lagrangian–Eulerian methodPreview
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- Balachandran K, Sucosky P, Yoganathan AP (2011) Hemodynamics and mechanobiology of aortic valve inflammation and calcification. Int J Inflam 2011:15Google Scholar
- Barker AJ, Markl M (2011) The role of hemodynamics in bicuspid aortic valve disease. Eur J Cardiothorac Surg 39: 805–806. doi: 10.1016/j.ejcts.2011.01.006 CrossRefGoogle Scholar
- Barker AJ, Lanning C, Shandas R (2010) Quantification of hemodynamic wall shear stress in patients with bicuspid aortic valve using phase-contrast MRI. Ann Biomed Eng 38: 788–800. doi: 10.1007/s10439-009-9854-3 CrossRefGoogle Scholar
- Bellhouse BJ (1969) Velocity and pressure distributions in aortic valve. J Fluid Mech 37: 587–600CrossRefGoogle Scholar
- Bellhouse BJ, Talbot L (1969) The fluid mechanics of the aortic valve. J Fluid Mech 35: 721–735CrossRefGoogle Scholar
- Bellhouse BJ, Bellhouse FH (1968) Mechanism of closure of the aortic valve. Nature 217: 86–87CrossRefGoogle Scholar
- Butcher JT, Penrod AM, Garcia AJ, Nerem RM (2004) Unique morphology and focal adhesion development of valvular endothelial cells in static and fluid flow environments. Arterioscler Thromb Vasc Biol 24: 1429–1434CrossRefGoogle Scholar
- Caro CG (1978) The mechanics of the circulation. Oxford University Press, OxfordMATHGoogle Scholar
- Chandran KB, Yoganathan AP, Rittgers SE (2007) Hemodynamic theories of atherosclerosis. In: Taylor, Francis (eds) Anonymous biofluid mechanics: the human circulation. CRC Press, Boca Raton, pp 227–228Google Scholar
- Conti CA, Della Corte A, Votta E, Del Viscovo L, Bancone C, De Santo LS, Redaelli A (2010) Biomechanical implications of the congenital bicuspid aortic valve: a finite element study of aortic root function from in vivo data. J Thorac Cardiovasc Surg 140:890-6, 896.e1-2. doi: 10.1016/j.jtcvs.2010.01.016 Google Scholar
- De Hart J, Baaijens FP, Peters GW, Schreurs PJ (2003) A computational fluid-structure interaction analysis of a fiber-reinforced stentless aortic valve. J Biomech 36: 699–712CrossRefGoogle Scholar
- Deck JD (1986) Endothelial cell orientation on aortic valve leaflets. Cardiovasc Res 20: 760–767CrossRefGoogle Scholar
- Donea J, Guiliani S, Halleux JP (1982) An arbitrary Lagrangian-Eulerian finite-element method for transient dynamic fluid structure interactions. Comput Methods Appl Mech Eng 33: 689–723CrossRefMATHGoogle Scholar
- Fowles RE, Martin RP, Abrams JM, Schapira JN, French JW, Popp RL (1979) Two-dimensional echocardiographic features of bicuspid aortic valve. Chest 75: 434–440CrossRefGoogle Scholar
- Ge L, Sotiropoulos F (2010) Direction and magnitude of blood flow shear stresses on the leaflets of aortic valves: is there a link with valve calcification. J Biomech Eng 132: 014505. doi: 10.1115/1.4000162 CrossRefGoogle Scholar
- Grande KJ, Cochran RP, Reinhall PG, Kunzelman KS (1998) Stress variations in the human aortic root and valve: the role of anatomic asymmetry. Ann Biomed Eng 26: 534–545CrossRefGoogle Scholar
- Hoehn D, Sun L, Sucosky P (2010) Role of pathologic shear stress alterations in aortic valve endothelial activation. Cardiovasc Eng Technol 1: 165–178. doi: 10.1007/s13239-010-0015-5 CrossRefGoogle Scholar
- Hope MD, Hope TA, Meadows AK, Ordovas KG, Urbania TH, Alley MT, Higgins CB (2010) Bicuspid aortic valve: four-dimensional MR evaluation of ascending aortic systolic flow patterns. Radiology 255: 53–61. doi: 10.1148/radiol.09091437 CrossRefGoogle Scholar
- Hope MD, Meadows AK, Hope TA, Ordovas KG, Reddy GP, Alley MT, Higgins CB (2008) Images in cardiovascular medicine. Evaluation of bicuspid aortic valve and aortic coarctation with 4D flow magnetic resonance imaging. Circulation 4(117): 2818–2819. doi: 10.1161/CIRCULATIONAHA.107.760124 CrossRefGoogle Scholar
- Hughes TJR, Liu WK, Zimmermann TK (1981) Lagrangian-Eulerian finite element formulation for incompressible viscous flows. Comput Methods Appl Mech Eng 29: 329–349. doi: 10.1016/0045-7825(81)90049-9 MathSciNetCrossRefMATHGoogle Scholar
- Jermihov P, Jia L, Sacks MS, Gorman R, Gorman J, Chandran K (2011) Effect of geometry on the leaflet stresses in simulated models of congenital bicuspid aortic valves. Cardiovasc Eng Technol 48–56. doi: 10.1007/s13239-011-0035-9
- Kilner PJ, Yang GZ, Wilkes AJ, Mohiaddin RH, Firmin DN, Yacoub MH (2000) Asymmetric redirection of flow through the heart. Nature 404: 759–761. doi: 10.1038/35008075 CrossRefGoogle Scholar
- Ku DN (1997) Blood flow in arteries. Annu Rev Fluid Mech 29: 399–434MathSciNetCrossRefGoogle Scholar
- Lewin MB, Otto CM (2005) The bicuspid aortic valve: adverse outcomes from infancy to old age. Circulation 111: 832–834. doi: 10.1161/01.CIR.0000157137.59691.0B CrossRefGoogle Scholar
- Merryman WD (2010) Mechano-potential etiologies of aortic valve disease. J Biomech 43: 87–92. doi: 10.1016/j.jbiomech.2009.09.013 CrossRefGoogle Scholar
- Nanda NC, Gramiak R, Manning J, Mahoney EB, Lipchik EO, DeWeese JA (1974) Echocardiographic recognition of the congenital bicuspid aortic valve. Circulation 49: 870–875CrossRefGoogle Scholar
- O’Brien KD (2006) Pathogenesis of calcific aortic valve disease: a disease process comes of age (and a good deal more). Arterioscler Thromb Vasc Biol 26: 1721–1728. doi: 10.1161/01.ATV.0000227513.13697.ac CrossRefGoogle Scholar
- Olson LJ, Subramanian R, Edwards WD (1984) Surgical pathology of pure aortic insufficiency: a study of 225 cases. Mayo Clin Proc 59: 835–841Google Scholar
- Otto CM (1999) Valvular heart disease. Saunders, LondonGoogle Scholar
- Otto CM, Kuusisto J, Reichenbach DD (1994) Characterization of the early lesion of ‘degenerative’ valvular aortic stenosis. Histological and immunohistochemical studies. Circulation 90: 844–853CrossRefGoogle Scholar
- Richards KE, Deserranno D, Donal E, Greenberg NL, Thomas JD, Garcia MJ (2004) Influence of structural geometry on the severity of bicuspid aortic stenosis. Am J Physiol Heart Circ Physiol 287: H1410–6. doi: 10.1152/ajpheart.00264.2003 CrossRefGoogle Scholar
- Roberts WC, Ko JM (2005) Frequency by decades of unicuspid, bicuspid, and tricuspid aortic valves in adults having isolated aortic valve replacement for aortic stenosis, with or without associated aortic regurgitation. Circulation 111: 920–925. doi: 10.1161/01.CIR.0000155623.48408.C5 CrossRefGoogle Scholar
- Roberts WC (1970) The congenitally bicuspid aortic valve. A study of 85 autopsy cases. Am J Cardiol 85(26): 72–83CrossRefGoogle Scholar
- Robicsek F, Thubrikar MJ, Cook JW, Fowler B (2004) The congenitally bicuspid aortic valve: how does it function? Why does it fail?. Ann Thorac Surg 77: 177–185CrossRefGoogle Scholar
- Sabet HY, Edwards WD, Tazelaar HD, Daly RC (1999) Congenitally bicuspid aortic valves: a surgical pathology study of 542 cases (1991 through 1996) and a literature review of 2,715 additional cases. Mayo Clin Proc 74: 14–26CrossRefGoogle Scholar
- Sievers HH, Schmidtke C (2007) A classification system for the bicuspid aortic valve from 304 surgical specimens. J Thorac Cardiovasc Surg 133: 1226–1233. doi: 10.1016/j.jtcvs.2007.01.039 CrossRefGoogle Scholar
- Sucosky P, Balachandran K, Elhammali A, Jo H, Yoganathan AP (2009) Altered shear stress stimulates upregulation of endothelial VCAM-1 and ICAM-1 in a BMP-4- and TGF-beta1-dependent pathway. Arterioscler Thromb Vasc Biol 29: 254–260. doi: 10.1161/ATVBAHA.108.176347 CrossRefGoogle Scholar
- Sun L, Rajamannan NM, Sucosky P (2011) Design and validation of a novel bioreactor to subject aortic valve leaflets to side-specific shear stress. Ann Biomed Eng 39: 2174–2185. doi: 10.1007/s10439-011-0305-6 CrossRefGoogle Scholar
- Thubrikar M (1990) The aortic valve. CRC Press, Boca Raton, FLGoogle Scholar
- Thubrikar MJ, Aouad J, Nolan SP (1986) Comparison of the in vivo and in vitro mechanical properties of aortic valve leaflets. J Thorac Cardiovasc Surg 92: 29–36Google Scholar
- Ward C (2000) Clinical significance of the bicuspid aortic valve. Heart 83: 81–85CrossRefGoogle Scholar
- Weinberg EJ, Kaazempur Mofrad MR (2008) A multiscale computational comparison of the bicuspid and tricuspid aortic valves in relation to calcific aortic stenosis. J Biomech 41: 3482–3487. doi: 10.1016/j.jbiomech.2008.08.006 CrossRefGoogle Scholar
- Weston MW, LaBorde DV, Yoganathan AP (1999) Estimation of the shear stress on the surface of an aortic valve leaflet. Ann Biomed Eng 27: 572–579CrossRefGoogle Scholar
- Yap CH, Saikrishnan N, Tamilselvan G, Yoganathan AP (2011a) Experimental measurement of dynamic fluid shear stress on the aortic surface of the aortic valve leaflet. Biomech Model Mechanobiol. doi: 10.1007/s10237-011-0301-7
- Yap CH, Saikrishnan N, Yoganathan AP (2011b) Experimental measurement of dynamic fluid shear stress on the ventricular surface of the aortic valve leaflet. Biomech Model Mechanobiol. doi: 10.1007/s10237-011-0306-2