Abstract
We have used incremental stress-strain curves to study the mechanical behavior of porcine aorta, carotid artery, and vena cava. Elastic and viscous stress-strain curves are composed of low and high strain regions that are approximately linear. Analysis of the low strain behavior is consistent with previous studies that suggest that the behavior is dominated by the behavior of elastic fibers, and that the collagen and elastic fibers are in parallel networks. At high strain, the behavior is different than that of skin where it is dominated by the behavior of the collagen fibers. The high strain behavior is consistent with a series arrangement of the collagen and smooth muscle; however, the arrangement of smooth muscle and collagen may be different in aorta than in the other vessels studied. It is concluded that the mechanical behavior of the vessel wall differs from the behavior of other extracellular matrices that do not contain smooth muscle. Our results indicate that at least some of the collagen fibrils in the media are in series with smooth muscle cells and this collagen-smooth muscle network is in parallel with parallel networks of collagen and elastic tissue in aorta, carotid artery, and vena cava. It is concluded that the series arrangement of collagen and smooth muscle may be important in mechanochemical transduction in vessel walls and that the exact quantity and arrangement of these components may differ in different vessels. © 2003 Biomedical Engineering Society.
PAC2003: 8719Rr, 8715La, 8719Uv, 8719Ff
Similar content being viewed by others
References
Ayer, J. P., G. M. Hass, and D. E. Philpott. Aortic elastic tissue: isolation with use of formic acid and discussion of some of its properties. AMA Arch. Pathol.65:519–544, 1958.
Bank, A. J., H. Wang, J. E. Holte, K. Mullen, R. Shammas, and S. H. Kubo. Contribution of collagen, elastin, and smooth muscle to in vivo human brachial artery wall stress and modulus. Circulation94:3263–3270, 1996.
Chien, S., and Y.-J. Shyy. Effects of mechanical forces on signal transduction and gene expression in endothelial cells. Hypertension31:162–169, 1998.
Clark, J. M., and S. Glagov. Structural integration of the arterial wall: I. Relationship and attachments of medial smooth muscle cells in normally distended and hyperdistended aortas. Lab. Invest.40:587–602, 1979.
Clark, J. M., and S. Glagov. Transmural organization of arterial media: The lamellar unit revisited. Arteriosclerosis (Dallas)5:587–602, 1985.
Cox, R. H.Regional variation of series elasticity in canine arterial smooth muscles. Am. J. Physiol.234:H542–H541, 1978.
Cox, R. H.Basis for the altered arterial wall mechanics in the spontaneously hypertensive rat. Hypertension3:485–495, 1981.
Davies, P. F.Flow mediated endothelial mechanotransduction. Physiol. Rev.75:519–560, 1995.
Dobrin, P. B., and A. A. Rovick. Influence of vascular smooth muscle on contractile mechanics and elasticity of arteries. Am. J. Physiol.217:1644–1652, 1969.
Dobrin, P. B.Influence of initial length on length-tension relationship of vascular smooth muscle. Am. J. Physiol.225:664–670, 1973.
Dobrin, P. B.Mechanical properties of arteries. Physiol. Rev.58:397–460, 1978.
Dunn, M. G., and F. H. Silver. Viscoelastic behavior of human connective tissues: Relative contribution of viscous and elastic components. Connect. Tissue Res.12:59–70, 1983.
Fischer, G. M., and J. G. Lluarado. Collagen and elastin content in canine arteries selected from functionally different vascular beds. Circ. Res.19:394–399, 1966.
Folkman, J., and A. Moscona. Role of cell shape in growth control. Nature (London)273:345–349, 1978.
Herlihy, J. T.Helically cut vascular strip preparation: geometrical considerations. Am. J. Physiol.238:H107–H109, 1980.
Hipper, A., and G. Isenberg. Cyclic mechanical strain decreases the DNA synthesis of vascular smooth muscle cells. Pfluegers Arch.440:19–27, 2000.
Ingber, D.How cells (might) sense microgravity. FASEB J.13:S3–S15, 1999.
Jalali, S., Y. S. Li, M. Sotoudeh, S. Yuan, S. Li, S. Chien, and Y.-L. Shyy. Shear stress activates p60src-RAS-MAPK signaling pathways in vascular endothelial cells. Arterioscler., Thromb., Vasc. Biol.18:227–234, 1998.
Jalali, S., M. A. del Pozo, K.-D. Chen, H. Maio, Y.-I. Li, M. A. Schwartz, J. Y.-J. Shyy, and S. Chien. Integrin-mediated mechanotransduction requires its dynamic interaction with specific extracellular matrix (ECM) ligands. Proc. Natl. Acad. Sci. U.S.A.98:1042–1046, 2001.
Kalath, S., P. Tsipouras, and F. H. Silver. Non-invasive assessment of aortic mechanical properties. Ann. Biomed. Eng.14:513–524, 1986.
Kanda, K., T. Matsuda, and T. Oka. Mechanical stress induced cellular orientation and phenotypic modulation of 3–D cultured smooth muscle cells. American Society of Artificial Internal Organs Journal39:M686–M690, 1993.
Langille, B. L.Arterial remodeling: relation to hemodynamics. Can. J. Physiol. Pharmacol.74:834–841, 1996.
Lehoux, S., B. Esposito, R. Merval, L. Loufrani, and A. Tedgui. Pulsatile stretch-induced extracellular signal-regulated kinase 1/2 activation in organ culture of rabbit aorta involves reactive oxygen species. Arterioscler., Thromb., Vasc. Biol.20:2366–2372, 2000.
Li, S., M. Kim, Y. L. Hu, S. Jalai, D. D. Schlaepfer, T. Hunter, S. Chien, and J. Y. Shyy. Fluid shear stress activation of focal adhesion kinase. Linking to mitogen-activated protein kinases. J. Biol. Chem.272:30455–30462, 1997.
Li, Q., Y. Muragaki, I. Hatamura, H. Ueno, and A. Ooshima. Stretch-induced collagen synthesis in cultured smooth muscle cells from rabbit aortic media and a possible involvement of angiotension II and transforming growth factor-beta. J. Vasc. Res.35:93–103, 1998.
Medynsky, A. O., D. W. Holdsworth, M. M. Sherebran, R. N. Ranken, and M. R. Roach. The effect of storage time and repeated measurements on the elastic properties of isolated porcine aortas using high resolution x-ray CT. Can. J. Physiol. Pharmacol.76:451–456, 1998.
Mosler, E., W. Folkhard, E. Knorzer, H. Nemetschek-Gansler, T. Nemetschek, and M. H. Koch. Stress-induced molecular arrangement in tendon collagen. J. Mol. Biol.182:589–596, 1985.
Numaguchi, K., S. Eguchi, T. Yamakawa, E. D. Motley, and T. Inagami. Mechanotransduction of rat aortic vascular smooth muscle cells requires RhoA and intact actin filaments. Circ. Res.85:5–11, 1999.
O'Callaghan, C. J., and B. Williams. Mechanical strain-induced extracellular matrix production by human vascular smooth muscle cells: role of TGF-beta (1). Hypertension36:319–324, 2000.
Ogle, B. M., and D. L. Mooradian. The role of vascular smooth muscle cell integrins in the compaction and mechanical strengthening of a tissue-engineered blood vessel. Tissue Eng.5:387–402, 1999.
Patel, D. J., J. S. Janicki, and T. E. Carew. Static anistropic elastic properties of the aorta in living dogs. Circ. Res.25:765–775, 1969.
Paterlini, M. G., G. Nemethy, and H. A. Scheraga. The energy of formation of internal loops in triple-helical collagen polypeptides. Biopolymers35:607–619, 1995.
Reusch, P., H. Wagdy, R. Reusch, E. Wilson, and H. E. Ives. Mechanical strain increases smooth muscle and decreases nonmuscle myosin expression in rat vascular smooth muscle cells. Circ. Res.79:1046–1053, 1996.
Roach, M. R., and A. C. Burton. The reason for the shape of the distensibility curves of arteries. Can. J. Biochem. Physiol.35:681–690, 1957.
Silver, F. H. Biological Materials: Structure, Mechanical Properties and Modeling of Soft Tissues. New York: New York University Press, 1987, pp. 7–21, 91–110.
Silver, F. H., D. L. Christiansen, and C. M. Buntin. Mechanical properties of the aorta: A review. Crit. Rev. Biomed. Eng.17:323–258, 1989.
Silver, F. H., Y. P. Kato, M. Ohno, and A. J. Wasserman. Analysis of mammalian connective tissue: Relationship between hierarchical structures and mechanical properties. J. Long-Term Effects of Medical Implants2:165–198, 1992.
Silver, F. H., D. L. Christiansen, P. Snowhill, Y. Chen, and W. J. Landis. Role of mineral in the elastic storage of energy in turkey tendon. Biomacromolecules1:180–185, 2000.
Silver, F. H., I. Horvath, and D. Foran. Viscoelasticity of the vessel wall: Role of collagen and elastic fibers. Crit. Rev. Biomed. Eng.29:279–302, 2001.
Silver, F. H., J. W. Freeman, and D. DeVore. Viscoelastic properties of human skin and processed dermis. Skin Research and Technology7:18–23, 2001.
Silver, F. H., J. W. Freeman, I. Horvath, and W. J. Landis. Molecular basis for elastic energy storage in mineralized tendon. Biomacromolecules2:750–756, 2001.
Silver, F. H., I. Horvath, and D. J. Foran. Mechanical implications of the domain structure of fibril forming collagens: Comparison of the molecular and fibrillar flexibility of α-chains found in types I, II and III collagens. J. Theor. Biol.216:243–254, 2002.
Smith, P. G., R. Garcia, and L. Kogerman. Mechanical strain increases protein tyrosine phosphorylation in airway smooth muscle cells. Exp. Cell Res.239:353–360, 1998.
Takahashi, M., and B. C. Berk. Mitogen activated protein kinase (ERK1/2) activation by shear stress and adhesion in endothelial cells. Essential role for a herbimycin-sensitive kinase. J. Clin. Invest.98:2623–2631, 1996.
Wang, N., J. P. Butler, and D. Ingber. Mechanotransduction across the cell surface and through the cytosskeleton. Science (Washington, DC, U.S.)260:1124–1127, 1993.
Wolinsky, H., and S. Glagov. Structural basis for the static mechanical properties of aortic media. Circ. Res.14:400–413, 1964.
Wolinsky, H., and S. Glagov. Comparison of abdominal and thoracic aortic medial structure in mammals. Deviation of man from usual pattern. Circ. Res.25:677–686, 1969.
Xu, Y., S. Gurusiddappa, R. L. Rich, R. T. Owens, D. R. Keene, R. Mayne, A. Hook, and M. Hook. Multiple binding sites in collagen type I for the integrins α1β1 and α2β1. J. Biol. Chem.275:38981–38989, 2000.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Silver, F.H., Snowhill, P.B. & Foran, D.J. Mechanical Behavior of Vessel Wall: A Comparative Study of Aorta, Vena Cava, and Carotid Artery. Annals of Biomedical Engineering 31, 793–803 (2003). https://doi.org/10.1114/1.1581287
Issue Date:
DOI: https://doi.org/10.1114/1.1581287