Skip to main content
Log in

Experimental investigation and constitutive modeling of the 3D histomechanical properties of vein tissue

  • Original Paper
  • Published:
Biomechanics and Modeling in Mechanobiology Aims and scope Submit manuscript

Abstract

Numerous studies have provided material models of arterial walls, but limited information is available on the pseudo-elastic response of vein walls and their underlying microstructure, and only few constitutive formulations have been proposed heretofore. Accordingly, we identified the histomechanics of healthy porcine jugular veins by applying an integrated approach of inflation/extension tests and histomorphometric evaluation. Several alternate phenomenological and microstructure-based strain-energy functions (SEF) were attempted to mimic the material response. Evaluation of their descriptive/predictive capacities showed that the exponential Fung-type SEF alone or in tandem with the neo-Hookean term did not capture the deformational response at high pressures. This problem was solved to a degree with the neo-Hookean and two-fiber (diagonally arranged) family SEF, but altogether the least reliable fit was generated. Fitting precision was much improved with the four-fiber (diagonally, circumferentially, longitudinally arranged) family model, as the inability of neo-Hookean function with force data was alleviated by use of the longitudinal-fiber family. Implementation of a quadratic term as a descriptor of low-pressure anisotropy facilitated the simulation of low-pressure and force data, and the four-fiber families simulated more faithfully than the two-fiber families the physiologic and high-pressure response. Importantly, this SEF was consistent with vein angioarchitecture, namely the occurrence of extensive elastin fibers along the longitudinal axis and few orthogonal fibers attached to them and of three collagen sets with circumferential, longitudinal, and diagonal arrangement, respectively. Our findings help to establish the relationship between vein microstructure and its biomechanical response, yet additional observations are obligatory prior to endeavoring generalizations to other veins.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alastrué V, Peña E, Martínez M, Doblaré M (2008) Experimental study and constitutive modeling of the passive mechanical properties of the ovine infrarenal vena cava tissue. J Biomech 41: 3038–3045

    Article  Google Scholar 

  • Azuma T, Hasegawa M (1973) Distensibility of the vein: from the architectural point of view. Biorheology 10: 469–479

    Google Scholar 

  • Baek S, Gleason RL, Rajapogal KR, Humphrey JD (2007) Theory of small on large: potential utility in computations of fluid-solid interactions in arteries. Comput Methods Appl Mech Eng 196: 3070–3078

    Article  MATH  Google Scholar 

  • Carboni M, Desch GW, Weizsäcker HW (2007) Passive mechanical properties of porcine left circumflex artery and its mathematical description. Med Eng Phys 29: 8–16

    Article  Google Scholar 

  • Crissman RS (1984) The three-dimensional configuration of the elastic fiber network in canine saphenous vein: A stereo scanning electron microscopic study. Blood Vessel 21: 156–170

    Google Scholar 

  • Crissman RS, Guilford W (1984) The three-dimensional architecture of the elastic-fiber network in canine hepatic portal system. Am J Anat 171: 401–413

    Article  Google Scholar 

  • Demiray H, Weizsäcker HW, Pascale K (1986) A mechanical model for passive behaviour of rats carotid artery. Biomed Tech 31: 46–52

    Article  Google Scholar 

  • Desch GW, Weizsäcker HW (2007) A model for passive elastic properties of rat vena cava. J Biomech 40: 3130–3145

    Article  Google Scholar 

  • Fung YC (1993) Biomechanics: mechanical properties of living tissues. Springer, New York

    Google Scholar 

  • Fung YC, Fronek K, Patitucci P (1979) Pseudoelasticity of arteries and the choice of its mathematical expression. Am J Physiol 237: H620–H631

    Google Scholar 

  • Gasser CT, Ogden RW, Holzapfel GA (2006) Hyperelastic modelling of arterial layers with distributed collagen fibre orientations. J R Soc Interface 3: 15–35

    Article  Google Scholar 

  • Gleason RL, Dye WW, Wilson E, Humphrey JD (2008) Quantification of the mechanical behavior of carotid arteries from wild-type, dystrophin deficient, and sarcoglycan-delta knockout mice. J Biomech 41: 3213–3218

    Article  Google Scholar 

  • Gosline JM (1980) The elastic properties of rubber-like proteins and highly extensible tissues. Cambridge University Press, Cambridge

    Google Scholar 

  • Gundiah N, Ratcliffe MB, Pruitt LA (2007) Determination of strain energy function for arterial elastin: experiments using histology and mechanical tests. J Biomech 40: 586–594

    Article  Google Scholar 

  • Han HC, Zhao L, Huang M, Hou LS, Huang YT, Kuang ZB (1998) Postsurgical changes of the opening angle of canine autogenous vein graft. J Biomech Eng 120: 211–216

    Article  Google Scholar 

  • Hansen L, Wan W, Gleason RL (2009) Microstructurally motivated constitutive modeling of mouse arteries cultured under altered axial stretch. J Biomech Eng 131: 101015

    Article  Google Scholar 

  • Hasegawa M (1983) Rheological properties and wall structures of large veins. Biorheology 20: 531–545

    Google Scholar 

  • Hayashi K, Mori K, Miyazaki H (2003) Biomechanical response of femoral vein to chronic elevation of blood pressure in rabbits. Am J Physiol Heart Circ 284: H511–H518

    Google Scholar 

  • Hollander Y, Durban D, Lu X, Kassab GS, Lanir Y (2011) Experimentally validated microstructural 3d constitutive model of coronary arterial media. J Biomech Eng 133: 031007

    Article  Google Scholar 

  • Hollander Y, Durban D, Lu X, Kassab GS, Lanir Y (2011) Constitutive modeling of coronary arterial media—comparison of three model classes. J Biomech Eng 133: 061008

    Article  Google Scholar 

  • Holzapfel GA, Weizsäcker HW (1998) Biomechanical behavior of the arterial wall and its numerical characterization. Comput Biol Med 28: 377–392

    Article  Google Scholar 

  • Holzapfel GA, Gasser CT, Ogden RW (2000) A new constitutive framework for arterial wall mechanics and a comparative study of material models. J Elast 61: 1–48

    Article  MathSciNet  MATH  Google Scholar 

  • Holzapfel GA, Ogden RW (2010) Constitutive modelling of arteries. Proc R Soc A 466: 1551–1597

    Article  MathSciNet  MATH  Google Scholar 

  • Humphrey JD (2002) Cardiovascular solid mechanics: cells, tissues, and organs. Springer, New York

    Google Scholar 

  • Kitoh T, Kawai Y, Ohhashi T (1993) Effects of collagenase, elastase, and hyaluronidase on mechanical properties of isolated dog jugular veins. Am J Physiol 265: H273–H280

    Google Scholar 

  • Kritharis EP, Kakisis JD, Giagini AT, Manos T, Stergiopulos N, Tsangaris S, Sokolis DP (2010) Biomechanical, morphological and zero-stress state characterization of jugular vein remodeling in arteriovenous fistulas for hemodialysis. Biorheology 47: 297–319

    Google Scholar 

  • Kugelgen AV (1956) Weitere Mitteilungen über den Wandbau der grossen Venen des Menschen unter besonderer Berücksightingung ihrer Kollagenstrukturen. Z Zellforsch Mikrosk Anat 44: 121–174

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Minten J, Verheyen A, Cornelissen F, Rombauts W, Dequeker J, de Geest H (1986) Correlation between mechanical properties and wall composition of the canine superior vena cava. Arch Int Physiol Biochim 94: 349–362

    Article  Google Scholar 

  • Monos E, Berczi V, Nadasy G (1995) Local control of veins: biomechanical, metabolic, and humoral aspects. Physiol Rev 75: 611–666

    Google Scholar 

  • Pasquali-Ronchetti I, Alessandrini A, Baccarani Contri M et al (1998) Study of elastic fiber organization by scanning force microscopy. Matrix Biol 17: 75–83

    Article  Google Scholar 

  • Rezakhaniha R, Stergiopulos N (2008) A structural model of the venous wall considering elastin anisotropy. J Biomech Eng 130: 031017

    Article  Google Scholar 

  • Rhodin JAG (1980) Architecture of the vessel wall. In: Bohr DF, Somlyo AD, Sparks HV (eds) Handbook of physiology, section 2: the cardiovascular system. vol 2: vascular smooth muscle. American Physiological Society, Bethesda, pp 1–31

    Google Scholar 

  • Roach MR, Song SH (1988) Arterial elastin as seen with scanning electron microscopy: a review. Scan Microsc 2: 994–1004

    Google Scholar 

  • Sacks MS, Sun W (2003) Multiaxial mechanical behavior of biological materials. Annu Rev Biomed Eng 5: 251–284

    Article  Google Scholar 

  • Sakanishi A, Hasegawa M, Dobashi T (1988) Distensibility characteristics of caval veins and empirical exponential formulae. Biorheology 25: 165–172

    Google Scholar 

  • Sherebrin MH, Song SH, Roach MR (1982) Mechanical anisotropy of purified elastin from the thoracic aorta of dog and sheep. Can J Biochem Physiol 61: 539–545

    Google Scholar 

  • Sokolis DP, Kefaloyannis EM, Kouloukoussa M, Marinos E, Boudoulas H, Karayannacos PE (2006) A structural basis for the aortic stress–strain relation in uniaxial tension. J Biomech 39: 1651–1662

    Article  Google Scholar 

  • Sokolis DP (2008) Passive mechanical properties and constitutive modeling of blood vessels in relation to microstructure. Med Biol Eng Comput 46: 1187–1199

    Article  Google Scholar 

  • Sokolis DP (2010) A passive strain-energy function for elastic and muscular arteries: correlation of material parameters with histological data. Med Biol Eng Comput 48: 507–518

    Article  Google Scholar 

  • Sokolis DP, Sassani S, Kritharis EP, Tsangaris S (2011) Differential histomechanical response of carotid artery in relation to species and region: mathematical description accounting for elastin and collagen anisotropy. Med Biol Eng Comput 49: 867–879

    Article  Google Scholar 

  • Takamizawa K, Hayashi K (1987) Strain energy density function and uniform strain hypothesis for arterial mechanics. J Biomech 20: 7–17

    Article  Google Scholar 

  • Vito RP, Dixon SA (2003) Blood vessel constitutive models—1995–2002. Ann Rev Biomed Eng 5: 413–439

    Article  Google Scholar 

  • Wang C, Garcia M, Lu X, Lanir Y, Kassab GS (2006) Three-dimensional mechanical properties of porcine coronary arteries: a validated two-layer model. Am J Physiol Heart Circ Physiol 291: H1200–H1209

    Article  Google Scholar 

  • Weizsäcker HW (1988) Passive elastic properties of the rat abdominal vena cava. Pflügers Archiv 412: 147–154

    Google Scholar 

  • Weizsäcker HW, Holzapfel GA, Desch GW, Pascale K (1995) Strain energy density function for arteries from different topographical sites. Biomed Tech 2: 139–141

    Article  Google Scholar 

  • Wesley RLR, Vaishnav RN, Fuchs JCA, Patel DJ, Greenfield JC Jr (1975) Static linear and nonlinear elastic properties of normal and arterialized venous tissue in dog and man. Circ Res 37: 509–520

    Article  Google Scholar 

  • Wicker BK, Hutchens HP, Wu Q, Yeh AT, Humphrey JD (2008) Normal basilar artery structure and biaxial mechanical behaviour. Comput Methods Biomech Biomed Eng 11: 539–551

    Article  Google Scholar 

  • Xie JP, Liu SQ, Yang RF, Fung YC (1991) The zero-stress state of rat veins and vena cava. J Biomech Eng 113: 36–41

    Article  Google Scholar 

  • Zhou J, Fung YC (1996) The degree of nonlinearity and anisotropy of blood vessel elasticity. Proc Natl Acad Sci USA 94: 14255–14260

    Article  Google Scholar 

  • Zou Y, Zhang Y (2009) An experimental and theoretical study on the anisotropy of elastin network. Ann Biomed Eng 37: 1572–1583

    Article  MathSciNet  Google Scholar 

  • Zoumi A, Lu X, Kassab GS, Tromberg BJ (2004) Imaging coronary artery microstructure using second-harmonic and two-photon fluorescence microscopy. Biophys J 87: 2778–2786

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dimitrios P. Sokolis.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sokolis, D.P. Experimental investigation and constitutive modeling of the 3D histomechanical properties of vein tissue. Biomech Model Mechanobiol 12, 431–451 (2013). https://doi.org/10.1007/s10237-012-0410-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10237-012-0410-y

Keywords

Navigation