Abstract
A matrix-fibril shear stress transfer approach is devised and developed in this paper to analyse the primary biomechanical factors which initiate the structural degeneration of the bioprosthetic heart valves (BHVs). Using this approach, the critical length of the collagen fibrils l c and the interface shear acting on the fibrils in both BHV and natural aortic valve (AV) tissues under physiological loading conditions are calculated and presented. It is shown that the required critical fibril length to provide effective reinforcement to the natural AV and the BHV tissue is l c = 25.36 µm and l c = 66.81 µm, respectively. Furthermore, the magnitude of the required shear force acting on fibril interface to break a cross-linked fibril in the BHV tissue is shown to be 38 µN, while the required interfacial force to break the bonds between the fibril and the surrounding extracellular matrix is 31 µN. Direct correlations are underpinned between these values and the ultimate failure strength and the failure mode of the BHV tissue compared with the natural AV, and are verified against the existing experimental data. The analyses presented in this paper explain the role of fibril interface shear and critical length in regulating the biomechanics of the structural failure of the BHVs, for the first time. This insight facilitates further understanding into the underlying causes of the structural degeneration of the BHVs in vivo.
Similar content being viewed by others
References
Broom ND. The stress/strain and fatigue behaviour of glutaraldehyde preserved heart-valve tissue. J Biomech. 1977;10(11):707–24.
Thubrikar M, Piepgrass WC, Deck JD, Nolan SP. Stresses of natural versus prosthetic aortic valve leaflets in vivo. Ann Thorac Surg. 1980;30(3):230–9.
Billiar KL, Sacks MS. Biaxial mechanical properties of the natural and glutaraldehyde treated aortic valve cusp—part I: experimental results. J Biomech Eng. 2000;122(1):23–30.
Lee JM, Boughner DR, Courtman DW. The glutaraldehyde-stabilized porcine aortic valve xenograft. II. Effect of fixation with or without pressure on the tensile viscoelastic properties of the leaflet material. J Biomed Mater Res. 1984;18(1):79–98.
Purinya B, Kasyanov V, Volkolakov J, Latsis R, Tetere G. Biomechanical and structural properties of the explanted bioprosthetic valve leaflets. J Biomech. 1994;27(1):1–11.
Vesely I, Barber JE, Ratliff NB. Tissue damage and calcification may be indeoendent mechanisms of bioprosthetic heart valve failure. J Heart Valve Dis. 2001;10(4):471–7.
Sacks MS. The biomechanical effects of fatigue on the porcine bioprosthetic heart valve. J Long Term Eff Med Implant. 2001;11(3–4):231–47.
Schoen FJ, Levy RJ. Calcification of tissue heart valve substitutes: progress toward understanding and prevention. Ann Thorac Surg. 2005;79(3):1072–80.
Pibarot P, Dumesnil JG. Valvular heart disease: changing concepts in disease management. Circulation. 2009;119:1034–48.
Sacks MS, Schoen FJ. Collagen fiber disruption occurs independent of calcification in clinically explanted bioprosthetic heart valves. J Biomed Mater Res. 2002;62(3):359–71.
Wells SM, Sacks MS. Effects of pressure on the biaxial mechanical behaviour of porcine bioprosthetic heart valves with long-term cyclic loading. Biomaterials. 2002;23(11):2389–99.
Mirnajafi A, Zubiate B, Sacks MS. Effects of cyclic flexural fatigue on porcine bioprosthetic heart valve heterograft biomaterials. J Biomed Mater Res A. 2010;94(1):205–13.
Sacks MS, Merryman WD, Schmidt DE. On the biomechanics of heart valve function. J Biomech. 2009;42(12):1804–24.
Lewinsohn AD, Anssari-Benham A, Lee DA, Taylor PM, Chester AH, Yacoub MH, Screen HRC. Anisotropic strain transfer through the aortic valve and its relevance to the cellular mechanical environment. Proc Inst Mech Eng H. 2011;225(8):821–30.
Vesely I. Heart valve tissue engineering. Circ Res. 2005;97(8):743–55.
Stella JA, Sacks MS. On the biaxial mechanical properties of the layers of the aortic valve leaflet. J Biomech Eng. 2007;129(5):757–66.
Anssari-Benam A, Bader DL, Screen HRC. A combined experimental and modelling approach to aortic valve viscoelasticity in tensile deformation. J Mater Sci Mater Med. 2011;22(2):253–62.
Billiar KL, Sacks MS. Biaxial mechanical properties of the natural and glutaraldehyde treated aortic valve cusp—part II: a structural constitutive model. J Biomech Eng. 2000;122(4):327–35.
Sacks MS. Incorporation of experimentally derived fiber orientation into a structural constitutive model for planar collagenous tissues. J Biomech Eng. 2003;125(2):280–7.
Aspden RM. Fibre reinforcing by collagen in cartilage and soft connective tissues. Proc Biol Sci. 1994;258(1352):195–200.
Aspden RM. Fibre stress and strain in fibre-reinforced composites. J Mater Sci. 1994;29(5):1310–8.
Goh KL, Aspden RM, Hukins DWL. Critical length of collagen fibrils in extracellular matrix. J Theor Biol. 2003;223(2):259–61.
Kato YP, Christiansen DL, Hahn RA, Shieh S-J, Goldstein JD, Silver FH. Mechanical properties of collagen fibres: a comparison of reconstituted and rat tail tendon fibres. Biomaterials. 1989;10(1):38–42.
Sasaki N, Odajima S. Elongation mechanism of collagen fibrils and force-strain relations of tendon at each level of structural hierarchy. J Biomech. 1996;29(9):1131–6.
Gentleman E, Lay AN, Dickerson DA, Nauman EA, Livesay GA, Dee KC. Mechanical characterization of collagen fibers and scaffolds for tissue engineering. Biomaterials. 2003;24(21):3805–13.
Gautieri A, Vesentini S, Redaelli A, Buehler MJ. Hierarchical structure and nanomechanics of collagen microfibrils from the atomistic scale up. Nano Lett. 2011;11(2):757–66.
Hang F, Barber AH. Nano-mechanical properties of individual mineralized collagen fibrils from bone tissue. J R Soc Interface. 2011;8(57):500–5.
Ahmadzadeh H, Connizzo BK, Freedman BR, Soslowsky LJ, Shenoy VB. Determining the contribution of glycosaminoglycans to tendon mechanical properties with a modified shear-lag model. J Biomech. 2013;46(14):2497–503.
Filon LNG. On the elastic equilibrium of circular cylinders under certain practical systems of load. Philos Trans R Soc Lond A. 1902;198(300):147–233.
Gupta HS, Seto J, Krauss S, Boesecke P, Screen HRC. In situ multi-level analysis of viscoelastic deformation mechanisms in tendon collagen. J Struct Biol. 2010;169(2):183–91.
Anssari-Benam A, Bader DL, Screen HRC. Anisotropic time-dependant behaviour of the aortic valve. J Mech Behav Biomed Mater. 2011;4(8):1603–10.
Leeson-Dietrich J, Boughner D, Vesely I. Porcine pulmonary and aortic valves: a comparison of their tensile viscoelastic properties at physiological strain rates. J Heart Valve Dis. 1995;4(1):88–94.
Thubrikar M, Aouad J, Nolan SP. Comparison of the in vivo and in vitro mechanical properties of aortic valve leaflets. J Thorac Cardiovasc Surg. 1986;92(1):29–36.
Liao J, Yang L, Grashow J, Sacks MS. The relation between collagen fibril kinematics and mechanical properties in the mitral valve anterior leaflet. J Biomech Eng. 2007;129(1):78–87.
Parry DAD, Barnes GRG, Craig AS. A comparison of the size distribution of collagen fibrils in connective tissues as a function of age and a possible relation between fibril size distribution and mechanical properties. Proc R Soc Lond B Biol Sci. 1978;203(1152):305–21.
Taylor PM. Biological matrices and bionanotechnology. Philos Trans R Soc Lond B Biol Sci. 2007;362(1484):1313–20.
Pins GD, Christiansen DL, Patel R, Silver FH. Self-assembly of collagen fibers. Influence of fibrillar alignment and Decorin on mechanical properties. Biophys J. 1997;73(4):2164–72.
Craig AS, Birtles MJ, Conway JF, Parry DA. An estimate of the mean length of collagen fibrils in rat tail-tendon as a function of age. Connect Tissue Res. 1989;19(1):51–62.
Redaelli A, Vesentini S, Soncini M, Vena P, Mantero S, Montevecchi FM. Possible role of decorin glycosaminoglycans in fibril to fibril force transfer in relative mature tendons: a computational study from molecular to microstructural level. J Biomech. 2003;36(10):1555–69.
Balguid A, Rubbens MP, Mol A, Bank RA, Bogers AJ, van Kats JP, de Mol BA, Baaijens FP, Bouten CV. The role of collagen cross-links in biomechanical behavior of human aortic heart valve leaflets: relevance for tissue engineering. Tissue Eng. 2007;13(7):1501–11.
Anssari-Benam A, Gupta HS, Screen HRC. Strain transfer through the aortic valve. J Biomech Eng. 2012;134(6):061003. doi:10.1115/1.4006812.
Hukins DWL, Aspden RM, Yarker YE. Fibre reinforcement and mechanical stability in articular cartilage. Eng Med. 1984;13(3):153–6.
Author information
Authors and Affiliations
Corresponding author
Appendix 1
Appendix 1
Plotting \(\log \dot{\lambda }\) versus log η in Fig. 6 for the three experimentally quantified \(\left( {\dot{\lambda },\eta } \right)\) data points, it may be observed that each two consecutive points have notably different gradients. This implies that at least two exponential terms may be required to adequately describe the behaviour of η versus \(\dot{\lambda }\) via an exponential profile, over the whole range of the three existing points. This function may be mathematically expressed as:
where a, b, c and d are constants to be calculated by fitting this function to the data points.
Setting the first exponential term in equation (A1) to describe the η-\(\dot{\lambda }\) behaviour of the first two points, and accepting fits with R 2 ≥ 0.99 using MATLAB®, domains for a and b over which acceptable fits may be achieved were obtained to be 740 ≤ a ≤ 850 and −200 ≤ b ≤ −140, respectively. These provided the numerical constraints for fitting equation (A1) to all three \(\left( {\dot{\lambda },\eta } \right)\) points:
However, another constraint is derived from the rheological properties of GAG. The yield stress of GAG solutions has been reported to be lower than 105 Pa [42]. Assuming that τ is in the range of 104 Pa ≤ τ ≤ 105 Pa, the model parameters in (A2) should provide the best fit to the three \(\left( {\dot{\lambda },\eta } \right)\) points such that the corresponding value of η at \(\dot{\lambda } = 2.5\) s−1 establishes that \(10^{4} \le 2\eta \frac{{\dot{\lambda }}}{\lambda }\). Therefore equation (A2) is rewritten as:
Fitting equation (A3) to the data points, the set of a, b, c and d that provided R 2 = 1 while satisfying those constraints were calculated to be: a = 778.7, b = −180.3, c = 24.89, and d = −2.97:
where the lower bound for η at \(\dot{\lambda } = 2.5\) was estimated to be η = 0.0145 MPa s.
Rights and permissions
About this article
Cite this article
Anssari-Benam, A., Barber, A.H. & Bucchi, A. Evaluation of bioprosthetic heart valve failure using a matrix-fibril shear stress transfer approach. J Mater Sci: Mater Med 27, 42 (2016). https://doi.org/10.1007/s10856-015-5657-2
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10856-015-5657-2