A mathematical model for analyzing the elasticity, viscosity, and failure of soft tissue: Comparison of native and decellularized porcine cardiac extracellular matrix for tissue engineering

Tissue Engineering - Part C: Methods

Volumn 19, Issue 8, 2013, Pages 620-630

  Bronshtein, Tomer ^a   Au Yeung, Gigi Chi Ting ^a   Sarig, Udi ^a,b   Nguyen, Evelyne Bao Vi ^a,b   Mhaisalkar, Priyadarshini S ^a   Boey, Freddy Yin Chiang ^a   Venkatraman, Subbu S ^a   MacHluf, Marcelle ^a,b  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ALGORITHMS; BIOMECHANICS; CELL CULTURE; ELASTIC MODULI; ELASTICITY; MATHEMATICAL MODELS; TENSILE TESTING; TISSUE; VISCOELASTICITY; VISCOSITY;

ACCURATE MEASUREMENT; APPARENT VISCOSITY; CARDIAC TISSUE ENGINEERING; EXTRACELLULAR MATRICES; MESENCHYMAL STEM CELL; SCAFFOLD MATERIALS; TISSUE-ENGINEERED CONSTRUCTS; VISCOELASTIC PROPERTIES;

SCAFFOLDS (BIOLOGY);

SUS;

ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; EXTRACELLULAR MATRIX; HEART MUSCLE; HUMAN; PROCEDURES; SWINE; TISSUE ENGINEERING; TISSUE SCAFFOLD; VISCOSITY; YOUNG MODULUS; ARTICLE; METHODOLOGY;

ANIMALS; ELASTIC MODULUS; EXTRACELLULAR MATRIX; HUMANS; MODELS, BIOLOGICAL; MYOCARDIUM; SWINE; TISSUE ENGINEERING; TISSUE SCAFFOLDS; VISCOSITY;

TISSUE SCAFFOLD;

EID: 84879409007     PISSN: 19373384     EISSN: 19373392     Source Type: Journal    
DOI: 10.1089/ten.tec.2012.0387     Document Type: Article

References (59)

1. Sarig, U., and Machluf, M. Engineering cell platforms for myocardial regeneration. Expert Opin Biol Ther 11, 1055, 2011.
2. Eitan, Y., Sarig, U., Dahan, N., and Machluf, M. Acellular cardiac extracellular matrix as a scaffold for tissue engineering: in vitro cell support, remodeling, and biocompati-bility. Tissue Eng Part C Methods 16, 671, 2010.
3. Sarig, U., Au-Yeung, G.C., Wang, Y., Bronshtein, T., Dahan, N., Boey, Y.C., et al. Thick acellular heart extracellular matrix with inherent vasculature: potential platform for myocardial tissue regeneration. Tissue Eng Part A 18, 2125, 2012.
4. Wang, Y., Bronshtein, T., Sarig, U., Boey, Y.C., Venkatra-man, S.S., and Machluf, M. Endothelialization of acellular porcine ECM with chemical modification. Int J Biosci Bio-chem Bioinform 2, 363, 2012.
5. Wang, Y., Bronshtein, T., Sarig, U., Nguyen, B.E., Boey, F.Y., Venkatraman, S.S., et al. A mathematical model predicting the co-culture dynamics of endothelial and mesenchymal stem cells for tissue regeneration. Tissue Eng Part A DOI:10.1089/ten.TEA.2012.0507. 2012 [ahead of print].
6. Badylak, S.F., Freytes, D.O., and Gilbert, T.W. Extracellular matrix as a biological scaffold material: structure and function. Acta Biomater 5, 1, 2009.
7. Ott, H.C., Matthiesen, T.S., Goh, S.K., Black, L.D., Kren, S.M., Netoff, T.I., et al. Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart. Nat Med 14, 213, 2008.
8. Witzenburg, C., Raghupathy, R., Kren, S.M., Taylor, D.A., and Barocas, V.H. Mechanical changes in the rat right ventricle with decellularization. J Biomech 45, 842, 2012.
9. Wainwright, J.M., Czajka, C.A., Patel, U.B., Freytes, D.O., Tobita, K., Gilbert, T.W., et al. Preparation of cardiac extracellular matrix from an intact porcine heart. Tissue Eng Part C Methods 16, 525, 2010.
10. Wang, B., Borazjani, A., Tahai, M., Curry, A.L., Simionescu, D.T., Guan, J., et al. Fabrication of cardiac patch with de-cellularized porcine myocardial scaffold and bone marrow mononuclear cells. J Biomed Mater Res A 94, 1100, 2010.
11. Weymann, A., Loganathan, S., Takahashi, H., Schies, C., Claus, B., Hirschberg, K., et al. Development and evaluation of a perfusion decellularization porcine heart model-generation of 3-dimensional myocardial neoscaffolds. Circ J 75, 852, 2011.
12. Wang, F., and Guan, J. Cellular cardiomyoplasty and cardiac tissue engineering for myocardial therapy. Adv Drug Deliv Rev 62, 784, 2010.
13. Vunjak-Novakovic, G., Tandon, N., Godier, A., Maidhof, R., Marsano, A., Martens, T.P., et al. Challenges in cardiac tissue engineering. Tissue Eng Part B Rev 16, 169, 2010.
14. Freed, L.E., Guilak, F., Guo, X.E., Gray, M.L., Tranquillo, R., Holmes, J.W., et al. Advanced tools for tissue engineering: scaffolds, bioreactors, and signaling. Tissue Eng 12, 3285, 2006.
15. Ikada, Y. Tissue Engineering: Fundamentals and Applications. 1st edition. Amsterdam, Boston: Academic Press/Elsevier, 2006.
16. Engler, A.J., Sen, S., Sweeney, H.L., and Discher, D.E. Matrix elasticity directs stem cell lineage specification. Cell 126, 677, 2006.
17. Reilly, G.C., and Engler, A.J. Intrinsic extracellular matrix properties regulate stem cell differentiation. J Biomech 43, 55, 2010.
18. Dahan, N., Zarbiv, G., Sarig, U., Karram, T., Hoffman, A., and Machluf, M. Porcine small diameter arterial extracellular matrix supports endothelium formation and media remodeling forming a promising vascular engineered biograft. Tissue Eng Part A 18, 411, 2012.
19. Neuenschwander, S., and Hoerstrup, SP. Heart valve tissue engineering. Transpl Immunol 12, 359, 2004.
20. Gilbert, T.W., Sellaro, T.L., and Badylak, S.F. Decellulariza-tion of tissues and organs. Biomaterials 27, 3675, 2006.
21. Schaner, P.J., Martin, N.D., Tulenko, T.N., Shapiro, I.M., Tarola, N.A., Leichter, R.F., et al. Decellularized vein as a potential scaffold for vascular tissue engineering. J Vasc Surg 40, 146, 2004.
22. Badylak, S.F. Xenogeneic extracellular matrix as a scaffold for tissue reconstruction. Transpl Immunol 12, 367, 2004.
23. Walles, T., Herden, T., Haverich, A., and Mertsching, H. Influence of scaffold thickness and scaffold composition on bioartificial graft survival. Biomaterials 24, 1233, 2003.
24. Wong, J.Y., and Bronzino, J.D. Biomaterials. Boca Raton: CRC Press, 2007, pp. 7-9.
25. Edwards, M.-B., Draper, E., Hand, J., Taylor, K., and Young, I. Mechanical testing of human cardiac tissue: some implications for MRI safety. J Cardiov Magn Reson 7, 835, 2005.
26. Rigby, B.J., Hirai, N., Spikes, J.D., and Eyring, H. The mechanical propertiesofrat tail tendon. J Gen Physiol 43, 265, 1959.
27. Maganaris, C.N., and Paul, J.P. In vivo human tendon mechanical properties. J Physiol 521 Pt 1, 307, 1999.
28. Venkatraman, S., Boey, F., and Lao, L.L. Implanted cardiovascular polymers: natural, synthetic and bio-inspired. Prog Polym Sci 33, 853, 2008.
29. Saraf, H., Ramesh, K.T., Lennon, A.M., Merkle, A.C., and Roberts, J.C. Mechanical properties of soft human tissues under dynamic loading. J Biomech 40, 1960, 2007.
30. Flynn, C., Taberner, A., and Nielsen, P. Modeling the mechanical response of in vivo human skin under a rich set of deformations. Ann Biomed Eng 39, 1935, 2011.
31. Valdez-Jasso, D., Bia, D., Zocalo, Y., Armentano, R.L., Haider, M.A., and Olufsen, M.S. Linear and nonlinear visco-elastic modeling of aorta and carotid pressure-area dynamics under in vivo and ex vivo conditions. Ann Biomed Eng 39, 1438, 2011.
32. Yang, T., Chui, C.K., Yu, R.Q., Qin, J., and Chang, S.K. Quasi-linear viscoelastic modeling of arterial wall for surgical simulation. Int J Comput Assist Radiol Surg 6, 829, 2011.
33. Yoo, L., Gupta, V., Lee, C., Kavehpore, P., and Demer, J.L. Viscoelastic properties of bovine orbital connective tissue and fat: constitutive models. Biomech Model Mechanobiol 10, 901, 2011.
34. Gangopadhyay, R. Exploring properties of polyaniline-SDS dispersion: a rheological approach. J Colloid Interface Sci 338, 435, 2009.
35. Smoliuk, L.T., and Protsenko Iu, L. [Mechanical properties of the passive myocardium: experiment and a mathematical model]. Biofizika 55, 905, 2010.
36. Kahn, C.J., Wang, X., and Rahouadj, R. Nonlinear model for viscoelastic behavior of Achilles tendon. J Biomech Eng 132, 111002, 2010.
37. Kroon, M. A constitutive model for smooth muscle including active tone and passive viscoelastic behaviour. Math Med Biol 27, 129, 2010.
38. Thomas, G.C., Asanbaeva, A., Vena, P., Sah, R.L., and Klisch, S.M. A nonlinear constituent based viscoelastic model for articular cartilage and analysis of tissue remodeling due to altered glycosaminoglycan-collagen interactions. J Biomech Eng 131, 101002, 2009.
39. Atanackovic, T.M. A modified Zener model of a viscoelastic body. Continuum Mech Thermodyn 14, 137, 2002.
40. Haddad, Y.M. Viscoelasticity of Engineering Materials. 1st edition. London: Chapman & Hall, 1995, pp. 378.
41. Feng, Z., Yamato, M., Akutsu, T., Nakamura, T., Okano, T., and Umezu, M. Investigation on the mechanical properties of contracted collagen gels as a scaffold for tissue engineering. Artif Organs 27, 84, 2003.
42. Jordan, P., Kerdok, A.E., Howe, R.D., and Socrate, S. Identifying a minimal rheological configuration: a tool for effective and efficient constitutive modeling of soft tissues. J Biomech Eng 133, 041006, 2011.
43. Anssari-Benam, A., Bader, D.L., and Screen, H.R. A combined experimental and modelling approach to aortic valve viscoelasticity in tensile deformation. J Mater Sci Mater Med 22, 253, 2011.
44. Feng, Z., Seya, D., Kitajima, T., Kosawada, T., Nakamura, T., and Umezu, M. Viscoelastic characteristics of contracted collagen gels populated with rat fibroblasts or cardiomyo-cytes. J Artif Organs 13, 139, 2010.
45. Schmitt, C., Hadj Henni, A., and Cloutier, G. Characterization of blood clot viscoelasticity by dynamic ultrasound elastography and modeling of the rheological behavior. J Biomech 44, 622, 2011.
46. Guan, J., Wang, F., Li, Z., Chen, J., Guo, X., Liao, J., et al. The stimulation of the cardiac differentiation of mesen-chymal stem cells in tissue constructs that mimic myocardium structure and biomechanics. Biomaterials 32, 5568, 2011.
47. Lu, H., Hoshiba, T., Kawazoe, N., Koda, I., Song, M., and Chen, G. Cultured cell-derived extracellular matrix scaffolds for tissue engineering. Biomaterials 32, 9658, 2011.
48. Venugopal, J.R., Prabhakaran, M.P., Mukherjee, S., Ra-vichandran, R., Dan, K., and Ramakrishna, S. Biomaterial strategies for alleviation of myocardial infarction. J R Soc Interface 9, 1, 2012.
49. Caspi, O., Lesman, A., Basevitch, Y., Gepstein, A., Arbel, G., Habib, I.H., et al. Tissue engineering of vascularized cardiac muscle from human embryonic stem cells. Circ Res 100, 263, 2007.
50. Jawad, H., Ali, N.N., Lyon, A.R., Chen, Q.Z., Harding, S.E., and Boccaccini, A.R. Myocardial tissue engineering: a review. J Tissue Eng Regen Med 1, 327, 2007.
51. Ruvinov, E., Dvir, T., Leor, J., and Cohen, S. Myocardial repair: from salvage to tissue reconstruction. Expert Rev Cardiovasc Ther 6, 669, 2008.
52. Meral, F.C., Royston, T.J., and Magin, R.L. Rayleigh-Lamb wave propagation on a fractional order viscoelastic plate. J Acoust Soc Am 129, 1036, 2011.
53. Wilkie, K.P., Drapaca, C.S., and Sivaloganathan, S. Aging impact on brain biomechanics with applications to hydro-cephalus. Math Med Biol 29, 145, 2012.
54. Tezcaner, A., Kose, G., and Hasirci, V. Fundamentals of tissue engineering: tissues and applications. Technol Health Care 10, 203, 2002.
55. Davis, N.F., Callanan, A., McGuire, B.B., Mooney, R., Flood, H.D., and McGloughlin, T.M. Porcine extracellular matrix scaffolds in reconstructive urology: an ex vivo comparative study of their biomechanical properties. J Mech Behav Biomed Mater 4, 375, 2011.
56. Fomovsky, G.M., Thomopoulos, S., and Holmes, J.W. Contribution of extracellular matrix to the mechanical properties of the heart. J Mol Cell Cardiol 48, 490, 2010.
57. Buehler, M.J. Multiscale aspects of mechanical properties of biological materials. J Mech Behav Biomed Mater 4, 125, 2011.
58. Hong, Y., Huber, A., Takanari, K., Amoroso, N.J., Ha-shizume, R., Badylak, S.F., et al. Mechanical properties and in vivo behavior of a biodegradable synthetic polymer mi-crofiber-extracellular matrix hydrogel biohybrid scaffold. Biomaterials 32, 3387, 2011.
59. Chen, Q.Z., Bismarck, A., Hansen, U., Junaid, S., Tran, M.Q., Harding, S.E., et al. Characterisation of a soft elastomer poly(glycerol sebacate) designed to match the mechanical properties of myocardial tissue. Biomaterials 29, 47, 2008.