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Evaluation of bioprosthetic heart valve failure using a matrix-fibril shear stress transfer approach

  • Clinical Applications of Biomaterials
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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.

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References

  1. Broom ND. The stress/strain and fatigue behaviour of glutaraldehyde preserved heart-valve tissue. J Biomech. 1977;10(11):707–24.

    Article  Google Scholar 

  2. 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.

    Article  Google Scholar 

  3. 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.

    Article  Google Scholar 

  4. 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.

    Article  Google Scholar 

  5. 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.

    Article  Google Scholar 

  6. 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.

    Google Scholar 

  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.

    Google Scholar 

  8. Schoen FJ, Levy RJ. Calcification of tissue heart valve substitutes: progress toward understanding and prevention. Ann Thorac Surg. 2005;79(3):1072–80.

    Article  Google Scholar 

  9. Pibarot P, Dumesnil JG. Valvular heart disease: changing concepts in disease management. Circulation. 2009;119:1034–48.

    Article  Google Scholar 

  10. 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.

    Article  Google Scholar 

  11. 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.

    Article  Google Scholar 

  12. 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.

    Article  Google Scholar 

  13. Sacks MS, Merryman WD, Schmidt DE. On the biomechanics of heart valve function. J Biomech. 2009;42(12):1804–24.

    Article  Google Scholar 

  14. 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.

    Article  Google Scholar 

  15. Vesely I. Heart valve tissue engineering. Circ Res. 2005;97(8):743–55.

    Article  Google Scholar 

  16. 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.

    Article  Google Scholar 

  17. 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.

    Article  Google Scholar 

  18. 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.

    Article  Google Scholar 

  19. 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.

    Article  Google Scholar 

  20. Aspden RM. Fibre reinforcing by collagen in cartilage and soft connective tissues. Proc Biol Sci. 1994;258(1352):195–200.

    Article  Google Scholar 

  21. Aspden RM. Fibre stress and strain in fibre-reinforced composites. J Mater Sci. 1994;29(5):1310–8.

    Article  Google Scholar 

  22. Goh KL, Aspden RM, Hukins DWL. Critical length of collagen fibrils in extracellular matrix. J Theor Biol. 2003;223(2):259–61.

    Article  Google Scholar 

  23. 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.

    Article  Google Scholar 

  24. 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.

    Article  Google Scholar 

  25. 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.

    Article  Google Scholar 

  26. 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.

    Article  Google Scholar 

  27. Hang F, Barber AH. Nano-mechanical properties of individual mineralized collagen fibrils from bone tissue. J R Soc Interface. 2011;8(57):500–5.

    Article  Google Scholar 

  28. 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.

    Article  Google Scholar 

  29. 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.

    Article  Google Scholar 

  30. 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.

    Article  Google Scholar 

  31. 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.

    Article  Google Scholar 

  32. 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.

    Google Scholar 

  33. 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.

    Google Scholar 

  34. 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.

    Article  Google Scholar 

  35. 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.

    Article  Google Scholar 

  36. Taylor PM. Biological matrices and bionanotechnology. Philos Trans R Soc Lond B Biol Sci. 2007;362(1484):1313–20.

    Article  Google Scholar 

  37. 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.

    Article  Google Scholar 

  38. 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.

    Article  Google Scholar 

  39. 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.

    Article  Google Scholar 

  40. 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.

    Article  Google Scholar 

  41. 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.

    Article  Google Scholar 

  42. Hukins DWL, Aspden RM, Yarker YE. Fibre reinforcement and mechanical stability in articular cartilage. Eng Med. 1984;13(3):153–6.

    Article  Google Scholar 

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Correspondence to Afshin Anssari-Benam.

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:

$$\eta (\dot{\lambda }) = a\exp b\dot{\lambda } + c\exp d\dot{\lambda }$$
(A1)

where a, b, c and d are constants to be calculated by fitting this function to the data points.

Fig. 6
figure 6

η versus \(\dot{\lambda }\) plotted in logarithmic scale. The connecting dashed lines between each two consecutive points highlight the respective gradients. Note the ~30 % difference in the gradient values

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:

$$\eta (\dot{\lambda }) = a\exp b\dot{\lambda } + c\exp d\dot{\lambda },\;\quad \left\{ \begin{aligned} 740 \le a \le 850 \hfill \\ - 200 \le b \le - 140 \hfill \\ \end{aligned} \right.,$$
(A2)

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:

$$\eta (\dot{\lambda }) = a\exp b\dot{\lambda } + c\exp d\dot{\lambda },\;\quad \left\{ \begin{aligned} &740 \le a \le 850 \\& - 200 \le b \le - 140 \\& 10^{4} \le 2\eta \frac{{\dot{\lambda }}}{\lambda } \\ \end{aligned} \right.,$$
(A3)

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:

$$\eta (\dot{\lambda }) = 778.7\exp \left( { - 180.3\dot{\lambda }} \right) + 24.89\exp \left( { - 2.97\dot{\lambda }} \right)$$
(A4)

where the lower bound for η at \(\dot{\lambda } = 2.5\) was estimated to be η = 0.0145 MPa s.

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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

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