Skip to main content

Advertisement

SpringerLink
Log in

Measurement of Mechanical Properties of Soft Tissues In Vitro Under Controlled Tissue Hydration

  • Published:
Experimental Mechanics Aims and scope Submit manuscript

Abstract

Alterations in tissue hydration that accompany inflammation or chronic remodeling of the Extracellular Matrix (ECM) have significant impact on the biomechanics of vascular tissue in health and disease. Examination of tissue behavior under controlled hydration in vitro could be helpful in better understanding the effects of tissue water content on its mechanical properties where in vivo tissue conditioning could not be possible. This study explains a multistage experimental protocol that allows both to prepare the tissue specimens with specific water content and to measure their mechanical behavior while maintaining the water content constant during the laboratory experimentation. Stress relaxation behaviors of the bovine aortic specimens–extracted from native, collagen-denatured and elastin-isolated tissues–were obtained within a water content range of 100–400 %. Using this method, distinct relaxation behaviors were obtained from tissue specimens with changing ECM treatments and hydration levels. The relaxation behavior was found to conform to a 4-parameter linear-viscoelastic macromechanical model consisting of two Maxwell components in parallel. The macromechanical model was able to distinguish between the morphological mechanisms associated with ECM elastin and collagen.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. He CM, Roach MR (1994) Composition mechanical properties abdominal aortic aneurysms. Vascular Surgeries 20:6–13

    Article  Google Scholar 

  2. Sacks MS et al (1999) In vivo three-dimensional surface geometry of abdominal aortic aneurisms. Biomed Eng 27:469–479

    Google Scholar 

  3. Sarraf CE et al (2003) Heart valve and arterial tissue eng. Cell Prolif 36:241–254

    Article  Google Scholar 

  4. Buttafoco L et al (2006) Electrospinning of collagen and elastin for tissue engineering applications. J Biomaterials 27:724–734

    Article  Google Scholar 

  5. Cox MAJ et al (2006) Mechanical Charac anisotropic planar biological soft tissues using large identation: computational feasibility study. Biomech Eng 128:428–436

    Article  Google Scholar 

  6. Tsai BM et al (2004) Hypoxic pulmonary vasoconstriction and pulmonary artery tissue cytokine expression are mediated by protein kinase C. Physiol Lung Cell Mol Physiol 287:L1215–L1219

    Article  Google Scholar 

  7. Zhang W et al (2007) Viscoelasticity reduces dynamic stresses and strains in vessel wall: implications for vessel fatigue. Physiol Heart Circ 293:H2355–H2360

    Article  Google Scholar 

  8. Zamir M et al (2009) Dynamic responsiveness of vascular bed as a regulatory mechanism in vasomotor control. Gen Physiol 134:69–75

    Article  Google Scholar 

  9. Silver FH et al (1989) Mech Prop of Aorta: a review. Crit Rev Biomed Eng 17:323–358

    Google Scholar 

  10. Apter JT et al (1966) Correlation of visco-elastic properties of large arteries with microscopic structure, I., II., III. Circ Res 19:104–121

    Article  Google Scholar 

  11. Apter JT, Marquez E (1968) Correlation of visco-elastic properties large arteries with microscopic structure: V. effects sinusoidal forcings at low and at resonance frequencies. Circ Res 22:393–404

    Article  Google Scholar 

  12. Holzapfel GA, Sommer G, Gasser CT, Regitnig P (2005) Determination of layer-specific mechanical properties of human coronary arteries with nonatherosclerotic intimal thickening and related constitutive modeling. Am J Physiol Heart Circ Physiol 289:H2048–H2058

    Article  Google Scholar 

  13. Lu X, Yang J, Zhao JB, Gregersen H, Kassab GS (2003) Shear modulus of porcine coronary artery: contributions of media and adventitia. Am J Physiol Heart Circ Physiol 285:H1966–H1975

    Google Scholar 

  14. Shadwick RE (1999) Mechanical design in arteries. J Exp Biol 202:3305–3313

    Google Scholar 

  15. Wolinsky H, Glagov S (1964) Structural basis for the static mechanical properties of the aortic media. Circ Res 14:400–413

    Article  Google Scholar 

  16. Jimenez Rios JL, Rabin Y (2007) A new device for mechanical testing of blood vessels at cryogenic temperatures. Exper Mech 47(3):337–346

    Article  Google Scholar 

  17. Xu S, Grande-Allen KJ (2010) The evolution of the field of biomechanics through the lens of experimental mechanics. Exper Mech 50(6):667–682

    Article  Google Scholar 

  18. Saravanan U, Baek S, Rajagopal KR et al (2006) On the deformation of the circumflex coronary artery during inflation tests at constant length. Exper Mech 46(5):647–656

    Article  Google Scholar 

  19. Humphrey JD (2002) Cardiovas solid mechanics: cells, tissues and organs. Springer, Berlin

    Google Scholar 

  20. Koplik J, Levine H (1985) Interface moving thru random background. Phys Rev B 32:280–292

    Article  Google Scholar 

  21. He S et al (1992) Roughness of wetting fluid invasion fronts in porous media. Phys Rev Lett 69:3731–3734

    Article  Google Scholar 

  22. Ravikumar KM, Hwang W (2008) Region-specific role of water collagen unwinding and assembly. Proteins 72:1320–1332

    Article  Google Scholar 

  23. Lillie MA et al (1998) Mechanical role of elastin-associated microfibrils in pig aortic elastic tissue. Connect Tissue Res 37:121–141

    Article  Google Scholar 

  24. Talman EA, Boughner DR (2001) Effect of altered hydration on internal shear prop of porcine aortic valve cusps. Thorac Surg 71:S375–S378

    Article  Google Scholar 

  25. Taylor AM et al (2004) Influence of hydration on tensile and compressive prop of avian keratinous tissues. Mater Sci 39:939–942

    Article  Google Scholar 

  26. Gainaru C et al (2009) Dielectric response of deeply supercooled hydration water the connective tissue proteins collagen and elastin. Phys Chem B 113:12628–12631

    Article  Google Scholar 

  27. Gosline JM, French CJ (1979) Dynamic mechanical propeties elastin. Biopol 18:2091–2103

    Article  Google Scholar 

  28. Maroudas A et al (1985) Studies of hydration and swelling pressure in normal and osteoarthritic cartilage. Biorheology 22:159–169

    Google Scholar 

  29. Wexler HR et al (1985) Quantitation of lung water by nuclear magnetic resonance imaging. Invest Radiol 20:583–590

    Article  Google Scholar 

  30. Han SM et al (2001) Disc hydration measured by magnetic resonance imaging in relation to its compressive stiffness in rat models. Proc Inst Mech Eng H 215:497–501

    Article  Google Scholar 

  31. Rochette LM, Patterson SM (2005) Hydration status and cardiovascular function: effects of hydration enhancement on cardiovascular function at rest and during psychological stress. Psychophysiol 56:81–91

    Article  Google Scholar 

  32. Hertzberg RW, Manson JA (1980) Fatigue of engineering plastics. Academic, New York, p 61

    Google Scholar 

  33. Lillie MA, Gosline JM (1990) Effects of hydration on dynamic mechanical properties of elastin. Biopolymers 29:1147–1160

    Article  Google Scholar 

  34. Lovekamp JJ et al (2006) Stability and function of glycosaminoglycans in porcine bioprosthetic heart valves. Biomaterials 27:1507–1518

    Article  Google Scholar 

  35. Scharnagl C et al (2005) Local compressibilities of proteins: comparison of optical experiments and simulations for horse heart cytochrome-c. Biophys 89:64–75

    Article  Google Scholar 

  36. Orecchini A et al (2009) Collective dynamics of protein hydration water by brillouin neutron spectroscopy. Am Chem Soc 131:4664–4669

    Article  Google Scholar 

  37. Mow VC et al (1980) Biphasic creep and stress relaxation of articular cartilage in compression? Theory and experiments. Biomech Eng 102:73–84

    Article  Google Scholar 

  38. Lu XL, Mow VC (2008) Biomechanics of articular cartilage and determination of material properties. Med Sci Sports Exerc 40:193–199

    Article  Google Scholar 

  39. Garcia JJ, Cortes DH (2006) A nonlinear biphasic viscohyperelastic model for articular cartilage. Biomech 39:2991–2998

    Article  Google Scholar 

  40. Soltz MA, Ateshian GA (1998) Experimental verification and theoretical prediction of cartilage interstitial fluid pressurization at an impermeable contact interface in confined compression. Biomech 31:927–934

    Article  Google Scholar 

  41. Huang CY et al (2003) Experimental verification of roles of intrinsic matrix viscoelasticity and tension-compression nonlinearity in biphasic response of cartilage. Biomech Eng 125:84–93

    Article  Google Scholar 

  42. Staverman AJ, Schwarzl FR (1956) Linear deformation behavior of high polymers. In: Stuart HA (ed) Die Physik der Hochpolymeren IV. Springer, Berlin, pp 1–95

    Google Scholar 

  43. Hodis S, Zamir M (2008) Solutions of Maxwell viscoelastic equations displacement and stress distributions within arterial wall. Phys Rev E Stat Nonlin Soft Matter Phys 78:021914

    Article  Google Scholar 

  44. Zhang W et al (2008) Generalized Maxwell model for creep behavior of artery opening angle. Biomech Eng 130:054502

    Article  Google Scholar 

  45. Holzapfel GA et al (2000) Mechanics of angioplasty: wall, balloon and stent. In: Casey J, Bao G (ed) Mechanics in Biology AMD242/BED 46:141–156

  46. Viidik A (1968) Rheological model uncalcified parallel-fibered collogeneous tissue. Biomechanics 1:3–11

    Article  Google Scholar 

  47. Apter JT (1964) Mathematical development of a physical model of visco-elastic properties of aorta. Math Biophys 26:267–288

    Google Scholar 

  48. Lanir Y (1983) Constitutive equations for fibrous connective tissues. Biomech 16:1–12

    Article  Google Scholar 

  49. Fonck E et al (2006) Mechanical prop of elastase treated arteries. Biomechanics 39:S319

    Article  Google Scholar 

  50. Weinberg EJ, Shahmirzadi D, Mofrad MRK (2010) On the multiscale modeling of heart valve in health and isease. Biomech Model Mechanobiol 9:373–387

    Article  Google Scholar 

  51. Shahmirzadi D, Hsieh AH (2011) Tissue and microstructural deformations in aortic tissue under stretch and after deformation recovery. Mech Time-Dependent Mater 15:105–117

    Article  Google Scholar 

  52. Huijing PA (1999) Muscle as a collagen fiber reinforced composite: a review of force transmission muscle and whole limb. Biomech 32:329–345

    Article  Google Scholar 

  53. Basciano CA, Kleinstreuer C (2009) Invariant-based anisotropic constitutive models of the healthy and aneurysmal abdominal aortic wall. Biomech Eng 131. doi:10.1115/1.3005341

  54. Pezzin G, Scandola M, Gotte L (1976) The low-temperature mechanical relaxation of elastin: I. The dry protein. Biopolymers 15:283–292

    Article  Google Scholar 

  55. Weinberg PD et al (1995) Distribution of water in arterial elastin: effects of mechanical stress, osmotic pressure, and temperature. Biopolymers 35:161–169

    Article  Google Scholar 

  56. Lillie MA et al (1996) Elastin dehydration thru liquid and vapor phase: comparison of osmotic stress models. Biopolymers 39:627–639

    Article  Google Scholar 

  57. Fung YC (1993) Biomechanics: mechanical properties of living tissues, 2nd edn. Springer, NY

    Google Scholar 

  58. Samouillan V (2000) Characterization of elastin and collagen in aortic bioprostheses. Med Biol Eng Comput 38:226–231

    Article  Google Scholar 

  59. Shahmirzadi D, Hsieh AH (2009) Controlling vascular tissue hydration during in-vitro procedures. BMES Annual Meeting, Pittsburgh

    Google Scholar 

  60. Shahmirzadi D, Hsieh AH (2010) An efficient technique adjusting and maintaining specific hydration levels in soft biological tissues in vitro. Med Eng Phys 32:795–801

    Article  Google Scholar 

  61. Shahmirzadi D, Hsieh AH (2010) In vitro mechanical testing of hydration-controlled arterial tissue. BMES Annual Meeting, Austin

    Google Scholar 

  62. Wang DM, Tarbell JM (1995) Modeling interstitial flow in an artery wall allows estimation of wall shear stress on smooth muscle cells. Biomech Eng 117:358–363

    Article  Google Scholar 

  63. Somlyo AP, Somlyo AV (1992) Smooth muscle structure and function. Heart cardiovascular system, 2nd edn. Raven, New York

    Google Scholar 

  64. Shahmirzadi D, Bruck H, Hsieh AH. Characterizing the interfibrillar spacing and fibrillar orientation of extracellular matrix in aortic tissues in vitro using histology images: toward multiscale modeling. IEEE Trans Biomedical Engineering. to appear

  65. Han SM, Lee SY, Cho MH, Lee JK (2001) Disc hydration measured by magnetic resonance imaging in relation to its compressive stiffness in rat models. Proc Inst Mech Eng H 215:497–501

    Article  Google Scholar 

  66. Caracciolo G, Petruccetti M, Caminiti R (2005) A new experimental setup for the study of lipid hydration by energy dispersive X-ray diffraction. Chem Phy Lett 414:456–460

    Article  Google Scholar 

  67. Png GM, Choi JW et al (2008) The impact of hydration changes in fresh bio-tissue on THz spectroscopic measurements. Phys Med Biol 53:3501–3517

    Article  Google Scholar 

  68. Danpinid A, Luo J, Vappou J, Terdtoon P, Konofagou EE (2010) In vivo characterization of the aortic wall stress–strain relationship. Ultrasonics 50:654–665

    Article  Google Scholar 

  69. Shahmirzadi D, Li RX, Konofagou EE (2011) Simulated pulse wave imaging for local stiffness estimation of patient-specific aorta. Int Tissue Elasticity Conference, Oct 12–15, Arlington, TX

  70. Shahmirzadi D, Li RX, Konofagou EE. FSI modeling of aortic pulse wave propagation for stiffness estimation with validation against phantom and in vitro studies. Biomechanical Engineering. in press

  71. Fujikura K, Luo J, Gamarnik V, Pernot M, Fukumoto R, Tilson MD, Konofagou EE (2007) A novel noninvasive technique for pulse-wave imaging and characterization of clinically-significant vascular mechanical properties in vivo. Ultrason Imaging 29:137–154

    Google Scholar 

  72. Vappou J, Luo J, Konofagou EE (2010) Pulse wave imaging for noninvasive and quantitative measurement of arterial stiffness in vivo. Am J Hypertens 23:393–398

    Article  Google Scholar 

  73. Shahmirzadi D, Konofagou EE (2012) Detection of aortic wall inclusion using regional pulse wave propagation and velocity in silico. Artery Research. doi:10.1016/j.artres.2012.05.004.

Download references

Acknowledgments

We are grateful to the Department of Mechanical Engineering at the University of Maryland for providing institutional support. We would also like to thank Hyunchul Kim for his help during the course of experimentation.

Conflict of interest statement

There are no conflicts of interest in this study to disclose.

Author information

Authors and Affiliations

  1. Fischell Department of Bioengineering, University of Maryland, College Park, MD, 20742, USA

    D. Shahmirzadi, H. A. Bruck & A. H. Hsieh

  2. Department of Mechanical Engineering, University of Maryland, College Park, MD, 20742, USA

    D. Shahmirzadi, H. A. Bruck & A. H. Hsieh

Authors
  1. D. Shahmirzadi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. H. A. Bruck
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. H. Hsieh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. Shahmirzadi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Shahmirzadi, D., Bruck, H.A. & Hsieh, A.H. Measurement of Mechanical Properties of Soft Tissues In Vitro Under Controlled Tissue Hydration. Exp Mech 53, 405–414 (2013). https://doi.org/10.1007/s11340-012-9644-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11340-012-9644-y

Keywords

Search

Navigation