Application of simple biomechanical and biochemical tests to heart valve leaflets: Implications for heart valve characterization and tissue engineering

Abstract

A simple biomechanical test with real-time displacement and strain mapping is reported, which provides displacement vectors and principal strain directions during the mechanical characterization of heart valve tissues. The maps reported in the current study allow us to quickly identify the approximate strain imposed on a location in the samples. The biomechanical results show that the aortic valves exhibit stronger anisotropic mechanical behavior than that of the pulmonary valves before 18% strain equibiaxial stretching. In contrast, the pulmonary valves exhibit stronger anisotropic mechanical behavior than aortic valves beyond 28% strain equibiaxial stretching. Simple biochemical tests are also conducted. Collagens are extracted at different time points (24, 48, 72, and 120 h) at different locations in the samples. The results show that extraction time plays an important role in determining collagen concentration, in which a minimum of 72 h of extraction is required to obtain saturated collagen concentration. This work provides an easy approach for quantifying biomechanical and biochemical properties of semilunar heart valve tissues, and potentially facilitates the development of tissue engineered heart valves.

Keywords

Heart valves real-time maps mechanical property collagen microstructure

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References

Sacks

Merryman

Schmidt

. On the biomechanics of heart valve function. J Biomech 2009; 42(12): 1804–1824.

Schoen

. Mechanisms of function and disease of natural and replacement heart valves. Annu Rev Pathol 2012; 7: 161–183.

Lewinsohn

Anssari-Benham

Lee

. Anisotropic strain transfer through the aortic valve and its relevance to the cellular mechanical environment. Proc. IMechE, Part H: J Engineering in Medicine 2011; 225(8): 821–830.

Koch

Reddy

Zilla

. Aortic valve leaflet mechanical properties facilitate diastolic valve function. Comput Methods Biomech Biomed Engin 2010; 13(2): 225–234.

Stella

Sacks

. On the biaxial mechanical properties of the layers of the aortic valve leaflet. J Biomech Eng 2007; 129(5): 757–766.

Doehring

Kahelin

Vesely

. Mesostructures of the aortic valve. J Heart Valve Dis 2005; 14(5): 679–686.

Joyce

Liao

Schoen

. Functional collagen fiber architecture of the pulmonary heart valve cusp. Ann Thorac Surg 2009; 87(4): 1240–1249.

Latif

Sarathchandra

Taylor

. Molecules mediating cell-ECM and cell-cell communication in human heart valves. Cell Biochem Biophys 2005; 43(2): 275–287.

Huang

H-Y

Liao

Sacks

. In-situ deformation of the aortic valve interstitial cell nucleus under diastolic loading. J Biomech Eng 2007; 129: 880–889.

10.

Filip

Radu

Simionescu

. Interstitial-cells of the heart-valves possess characteristics similar to smooth-muscle cells. Circ Res 1986; 59(3): 310–320.

11.

Gross

Kugel

. Topographical anatomy and histology of the valves in the human heart. Am J Pathol 1931; 7: 445–474.

12.

Sacks

Schoen

Mayer

Jr.

Bioengineering challenges for heart valve tissue engineering. Annu Rev Biomed Eng 2009; 11: 289–313.

13.

Langer

Vacanti

. Tissue engineering. Science 1993; 260(5110): 920–926.

14.

Schoen

Levy

. Calcification of tissue heart valve substitutes: progress toward understanding and prevention. Ann Thorac Surg 2005; 79(3): 1072–1080.

15.

Sacks

. The biomechanical effects of fatigue on the porcine bioprosthetic heart valve. J Long Term Eff Med Implants 2001; 11(3–4): 231–247.

16.

Dasi

Simon

Sucosky

. Fluid mechanics of artificial heart valves. Clin Exp Pharmacol Physiol 2009; 36(2): 225–237.

17.

Perron

Moran

Gauvreau

. Valved homograft conduit repair of the right heart in early infancy. Ann Thorac Surg 1999; 68(2): 542–548.

18.

Shinoka

Breuer

Tanel

. Tissue engineering heart valves: valve leaflet replacement study in a lamb model. Ann Thorac Surg 1995; 60(6 Suppl): S513–S516.

19.

Colazzo

Sarathchandra

Smolenski

. Extracellular matrix production by adipose-derived stem cells: implications for heart valve tissue engineering. Biomaterials 2011; 32(1): 119–127.

20.

Berry

Steen

Williams

. Bioreactors for development of tissue engineered heart valves. Ann Biomed Eng 2010; 38(11): 3272–3279.

21.

Sauren

Hout

Steenhaven

. The mechanical properties of porcine aortic valve tissues. J Biomech 1983; 16: 327–337.

22.

Sacks

. Incorporation of experimentally-derived fiber orientation into a structural constitutive model for planar collagenous tissues. J Biomech Eng 2003; 125(2): 280–287.

23.

Sacks

Sun

. Multiaxial mechanical behavior of biological materials. Annu Rev Biomed Eng 2003; 5: 251–284.

24.

Grashow

Sacks

Liao

. Planar biaxial creep and stress relaxation of the mitral valve anterior leaflet. Ann Biomed Eng 2006; 34(10): 1509–1518.

25.

Sacks

. Biaxial mechanical evaluation of planar biological materials. J Elast 2000; 61: 199–246.

26.

Eilaghi

Flanagan

Brodland

. Strain uniformity in biaxial specimens is highly sensitive to attachment details. J Biomech Eng 2009; 131(9): 091003.

27.

Eilaghi

Flanagan

Tertinegg

. Biaxial mechanical testing of human sclera. J Biomech 2010; 43(9): 1696–1701.

28.

Gregory

Veldhuis

Horst

Brodland

Callaghan

, Novel lap test determines the mechanics of delamination between annular lamellae of the intervertebral disc. Journal of Biomechanics 2011; 44:97–102.

29.

Sun

Sacks

Scott

. Effects of boundary conditions on the estimation of the planar biaxial mechanical properties of soft tissues. J Biomech Eng 2005; 127(4): 709–715.

30.

Brown

Kim

Alsberg

. Combining chondrocytes and smooth muscle cells to engineer hybrid soft tissue constructs. Tissue eng 2000; 6(4): 297–305.

31.

Engelmayr

Jr. Rabkin

Sutherland

. The independent role of cyclic flexure in the early in vitro development of an engineered heart valve tissue. Biomaterials 2005; 26(2): 175–187.

32.

Engelmayr

Jr. Papworth

Watkins

. Guidance of engineered tissue collagen orientation by large-scale scaffold microstructures. J Biomech 2005; 39: 1819–1831.

33.

Balguid

Mol

Van Vlimmeren

MAA

. Hypoxia induces near-native mechanical properties in engineered heart valve tissue. Circulation 2009; 119(2): 290–297.

34.

Christie

Barratt-Boyes

. Mechanical properties of porcine pulmonary valve leaflets: how do they differ from aortic leaflets? Ann Thorac Surg 1995; 60(0003–4975): S195–S199.

35.

Sacks

Smith

Hiester

. The aortic valve microstructure: effects of transvalvular pressure. J Biomed Mater Res 1998; 41(1): 131–141.

36.

Billiar

Sacks

. Biaxial mechanical properties of the natural and glutaraldehyde treated aortic valve cusp—part I: experimental results. J Biomech Eng 2000; 122(1): 23–30.

37.

Stradins

Lacis

Ozolanta

. Comparison of biomechanical and structural properties between human aortic and pulmonary valve. Eur J Cardiothorac Surg 2004; 26(3): 634–639.

38.

Balguid

Rubbens

Mol

. The role of collagen cross-links in biomechanical behavior of human aortic heart valve leaflets—relevance for tissue engineering. Tissue Eng 2007; 13(7): 1501–1511.