Structure and Function of the Diastolic Heart: Material Properties of Passive Myocardium

  • Bruce Smaill
  • Peter Hunter
Part of the Institute for Nonlinear Science book series (INLS)


A considerable body of indirect evidence indicates that the characteristics and extent of the extracellular connective tissue matrix in the heart are important determinants of ventricular function. An appropriate constitutive law for passive ventricular myocardium should therefore incorporate the most important features of its microstructure. In the first part of this chapter we outline the current understanding of cardiac microstructure. The organization and classification of the connective tissue hierarchy are reviewed and the contributions of the different collagen types constituting the extracellular tissue matrix are considered. We present recent morphological findings that indicate that ventricular myocardium is a layered composite rather than a uniformly branching continuum, and that the extent of coupling between adjacent layers of cells varies through the wall of the ventricle. In the second part of the chapter we describe the results of biaxial mechanical tests on thin sections of ventricular myocardium. For specimens from the midwall and subepicardium of the left ventricle, stress-extension relations in the fiber direction were nonlinear, with maximum fiber extensions between 15 and 25%. In the cross-fiber direction large extensions were measured in midwall specimens, together with rate dependence and hysteresis. This was not observed in subepicardial specimens. In both cases, however, cross-fiber stress-extension relations were highly nonlinear. The variation in biaxial mechanical behavior in midwall and subepicardial specimens is seen to reflect differences in microstructure at these two sites. Finally, we demonstrate that although the observed mechanical behavior can be accurately reproduced by a simple phenomenological constitutive law, it is difficult to identify unique material parameters with such a constitutive formulation.


Papillary Muscle Fiber Direction Ventricular Myocardium Sarcomere Length Constitutive Formulation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. [1]
    C. Abrahams, J.S. Janicki, and K.T. Weber. Myocardial hypertrophy in macaca fascicularis: Structural remodeling of the collagen matrix. Lab. Invest., 56: 676–683, 1987.Google Scholar
  2. [2]
    A. Benninghoff. Das perimysium internum. Handbuch der mikrosk. Anatomie von v. Mollendorf, 6: 192–196, 1930.Google Scholar
  3. [3]
    T.K. Borg, J. Buggy, I. Sullivan, J. Laks, and L. Terracio. Morphological and chemical characteristics of the connective tissue network during normal development and hypertrophy. J. Mol. Cell. Cardiol., 18 (Suppl): 247, 1986.CrossRefGoogle Scholar
  4. [4]
    T.K. Borg, R.E. Gay, and L.D. Johnson. Changes in the distribution of fibronectin and collagen during development of the neonatal rat heart. Collagen Rel. Res., 2: 211–218, 1982.Google Scholar
  5. [5]
    T.K. Borg, L.M. Klevay, R.E. Gay, R. Siegel, and M.E. Bergin. Alteration of the connective tissue network of striated muscle in copper deficient rats. J. Mol. Cell. Cardiol., 17: 1173–1183, 1985.CrossRefGoogle Scholar
  6. [6]
    T.K. Borg, W.F. Ranson, F.A. Moslehy, and J.B. Caulfield. Structural basis of ventricular stiffness. Lab. Invest., 44: 49–54, 1981.Google Scholar
  7. [7]
    J.B. Caulfield. Alterations in cardiac collagen with hypertrophy. Pers. Cardiovasc. Res., 8: 49–57, 1983.Google Scholar
  8. [8]
    J.B. Caulfield and T.K. Borg. The collagen network of the heart. Lab. Invest., 40: 364–371, 1979.Google Scholar
  9. [9]
    J.B. Caulfield, W. Ranson, J.C. Xuan, and S.B. Tao. Histologic correlates of altered ventricular strain patterns following coronary artery ligation. J. Mol Cell Cardiol., 16 (Suppl 1): 11, 1984.CrossRefGoogle Scholar
  10. [10]
    L.L. Demer and F.C.P. Yin. Passive biaxial mechanical properties of isolated canine myocardium. J. Physiol (London), 339: 615–630, 1983.Google Scholar
  11. [11]
    M. Eghbali, M.J. Czaja, M. Zeydel, et al. Collagen chain mRNAs in isolated heart cells from young and adult rats. J. Mol Cell Cardiol., 20: 267–276, 1988.CrossRefGoogle Scholar
  12. [12]
    M. Eghbali, S. Seifter, T.F. Robinson, and O.O. Blumenfeld. Enzyme-antibody histochemistry. A method for detection of collagens collectively. Histochemistry, 87: 257–262, 1987.CrossRefGoogle Scholar
  13. [13]
    M.S. Forbes and N. Sperelakis. Intercalated disk of of the mammalian heart: A review of structure and function. Tissue Cell, 17: 605–648, 1985.CrossRefGoogle Scholar
  14. [14]
    Y.C. Fung. Biomechanics: Mechanical Properties of Living Tissues. Springer-Verlag, New York, 1981.Google Scholar
  15. [15]
    Y.C. Fung. Biorheology of soft tissues. Biorheology, 10: 139–155, 1973.Google Scholar
  16. [16]
    E. Holmgren. Uber die trophospongien der quergestreiften muskelfasern, nebst bermerkungen uber den allgemeinen bau dieser fasern. Arch. Mikrosk. Anat., 71: 165–247, 1907.CrossRefGoogle Scholar
  17. [17]
    A. Horowitz, I. Sheinman, and Y. Lanir. Nonlinear incompressible finite element for simulating loading of cardiac tissue—part II: Three dimensional formulation for thick ventricular wall segments. ASME J. Biomech. Eng., 110: 62–68, 1988.MATHCrossRefGoogle Scholar
  18. [18]
    R.H. Hoyt, M.L. Cohen, and J.E. Saffitz. Distribution and three-dimensional structure of intercellular junctions in canine myocardium. Circ. Res., 64 (3): 563–574, 1989.Google Scholar
  19. [19]
    J.D. Humphrey and F.C.P. Yin. Biaxial mechanical behavior of excised epicardium. ASME J. Biomech. Eng., 110: 349–351, 1988.CrossRefGoogle Scholar
  20. [20]
    P.J. Hunter and B.H. Smaill. The analysis of cardiac function: A continuum approach. Prog. Biophys. Mol Biol, 52: 101–164, 1989.CrossRefGoogle Scholar
  21. [21]
    J.E. J alii, C.W. Doering, J.S. Janicki, R. Pick, S.G. Shroff, and K.T. Weber. Fibrillar collagen and myocardial stiffness in the intact hypertrophied rat left ventricle. Circ. Res., 64: 1041–1050, 1989.Google Scholar
  22. [22]
    F.J. Julian and M.R. Sollins. Sarcomere length-tension relations in living rat papillary muscle. Circ. Res., 37: 299–308, 1975.Google Scholar
  23. [23]
    Y. Lanir and Y.C. Fung. Two-dimensional mechanical properties of rabbit skin. I. Experimental system. J. Biomech., 7: 29–34, 1974.CrossRefGoogle Scholar
  24. [24]
    N.D. Light and A.E. Champion. Characterization of muscle epimysium, perimysium, and endomysium collagens. Biochem. J., 219: 1017–1026, 1984.Google Scholar
  25. [25]
    A.S.D. Mayne, G.W. Christie, B.H. Smaill, P.J. Hunter, and B.G. Barratt-Boyes. An assessment of the material properties of leaflets from four second generation porcine bioprostheses using biaxial testing techniques. J. Thorac. Cardiovasc. Surg., 98: 170–180, 1989.Google Scholar
  26. [26]
    I. Medugorac and R. Jacob. Characterization of left ventricular collagen in the rat. Cardiovasc. Res., 17: 15–21, 1983.CrossRefGoogle Scholar
  27. [27]
    J.B. Michel, J.L. Salzmann, M.O. Nlom, P. Bruneval, D. Barres, and J.P. Camilleri. Morphometric analysis of collagen network and plasma perfused capillary bed in the myocardium of rats during evolution of cardiac hypertrophy. Basic Res. Cardiol., 81: 142–154, 1986.CrossRefGoogle Scholar
  28. [28]
    L.A. Mulieri, G. Hasenfuss, F. Ittleman, E.M. Blanchard, and N.R. Alpert. Protection of human left ventricle from cutting injury with 2, 3-butanedione monoxime. Circ. Res., 65: 1441–1444, 1989.Google Scholar
  29. [29]
    J. Ohayon and R.S. Chadwick. Effects of collagen microstructure on the mechanics of the left ventricle. Biophys. J., 54: 1077–1088, 1989.CrossRefGoogle Scholar
  30. [30]
    J.G. Pinto. Some mechanical considerations in the selection and testing of papillary muscles. J. Biomech. Eng., 102: 62–66, 1980.CrossRefGoogle Scholar
  31. [31]
    J.G. Pinto and Y.C. Fung. Mechanical properties of the heart muscle in the passive state. J. Biomech., 6: 597–616, 1973.CrossRefGoogle Scholar
  32. [32]
    J.G. Pinto and P.J. Patitucci. Creep in cardiac muscle. Am. J. Physiol., 232: H553-H563, 1977.Google Scholar
  33. [33]
    J.G. Pinto and P.J. Patitucci. Visco-elasticity of passive cardiac muscle. J. Biomech. Eng., 102: 57–61, 1980.CrossRefGoogle Scholar
  34. [34]
    T.F. Robinson, L. Cohen-Gould, and S.M. Factor. Skeletal framework of mammalian heart muscle: Arrangement of inter-and peri-cellular connective tissue structures. Lab. Invest., 49: 482–498, 1983.Google Scholar
  35. [35]
    T.F. Robinson, L. Cohen-Gould, S.M. Factor, M. Eghbali, and O.O. Blumenfeld. Structure and function of connective tissue in cardiac muscle: Collagen types I and III in endomysial struts and pericellular fibers. Scan. Microsc., 2: 1005–1015, 1988.Google Scholar
  36. [36]
    T.F. Robinson, S.M. Factor, J.M. Capasso, B.A. Wittenburg, O.O. Blumenfeld, and S. Seifter. Morphology, composition, and function of struts between cardiac myocytes of rat and hamster. Cell Tissue Res., 249: 247–255, 1987.CrossRefGoogle Scholar
  37. [37]
    T.F. Robinson, S.M. Factor, and E.H. Sonnenblick. The heart as a suction pump. Scientif. Am., 254: 84–91, 1986.ADSCrossRefGoogle Scholar
  38. [38]
    T.F. Robinson, M.A. Geraci, E.H. Sonnenblick, and S.M. Factor. Coiled perimysial fibres in papillary muscle in rat heart: Morphology, distribution and changes in configuration. Circ. Res., 63: 577–592, 1988.Google Scholar
  39. [39]
    S. Sato, M. Ashraf, R.W. Millard, H. Fujiwara, and A. Schwartz. Connective tissue changes in early ischaemia of porcine myocardium: An ultrastructure study. J. Mol. Cell. Cardiol., 15: 261–267, 1983.CrossRefGoogle Scholar
  40. [40]
    A.J. Shacklock. Biaxial Testing of Cardiac Tissue. Master’s thesis, University of Auckland, New Zealand, 1987.Google Scholar
  41. [41]
    D.D. Streeter. Gross morphology and fiber geometry of the heart. In Berne R.M., editor, Handbook of Physiology, American Physiological Society, Bethesda, MD, 1979. Section 2.Google Scholar
  42. [42]
    H.E.D.J, ter Keurs, W.H. Rijnsburger, R. van Heuningen, and M.J. Nagelsmit. Tension development and sarcomere length in rat cardiac trabeculae: Evidence of length-dependent activation. Circ. Res., 46: 703–714, 1980.Google Scholar
  43. [43]
    P. Tong and Y.C. Fung. The stress-strain relationship for skin. J. Biomech., 9: 649–657, 1976.CrossRefGoogle Scholar
  44. [44]
    K.T. Weber, J.S. Janicki, S.G. Shroff, R. Pick, R.M. Chen, and R.I. Bashley. Collagen remodeling of the pressure-overloaded, hypertrophied nonhuman primate myocardium. Circ. Res., 62: 757–765, 1988.Google Scholar
  45. [45]
    F.C.P. Yin, P.H. Chew, and S.L. Zeger. An approach to quantification of biaxial tissue stress-strain data. J. Biomech., 19: 27–37, 1986.CrossRefGoogle Scholar
  46. [46]
    F.C.P. Yin, R.K. Strumpf, P.H. Chew, and S.L. Zeger. Quantification of the mechanical properities of noncontracting canine myocardium under simultaneous biaxial loading. J. Biomech., 20: 577–589, 1987.CrossRefGoogle Scholar
  47. [47]
    M. Zhao, H. Zhang, T.F. Robinson, S.M. Factor, and E.H. Sonnenblick. Profound structural alterations of the extracellular collagen matrix in postischemic dysfunctional (“stunned”) but viable myocardium. J. Am. Coll. Cardiol., 10: 1322–1324, 1987.CrossRefGoogle Scholar

Copyright information

© Springer-Verlag New York, Inc. 1991

Authors and Affiliations

  • Bruce Smaill
    • 1
  • Peter Hunter
    • 2
  1. 1.Department of Physiology, School of MedicineUniversity of AucklandNew Zealand
  2. 2.Department of Engineering Science, School of EngineeringUniversity of AucklandNew Zealand

Personalised recommendations