Biomechanical properties and microstructure of human ventricular myocardium

Acta Biomaterialia

Volumn 24, Issue , 2015, Pages 172-192

  Sommer, Gerhard ^a   Schriefl, Andreas J ^a   Andrä, Michaela ^b,c   Sacherer, Michael ^b   Viertler, Christian ^b   Wolinski, Heimo ^d   Holzapfel, Gerhard A ^a  

^a GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

^b MEDICAL UNIVERSITY OF GRAZ   (Austria)

^c Institute of Diagnostic and Interventional Radiology   (Austria)

^d UNIVERSITY OF GRAZ   (Austria)

Author keywords

Biaxial extension testing; Cardiac mechanics; Human ventricular myocardium; Microstructure; Optical clearing; Passive mechanical behavior; Second harmonic generation; Triaxial shear testing

Indexed keywords

BIOMECHANICS; COLLAGEN; DIGITAL STORAGE; DISEASES; DISPERSIONS; ELASTICITY; HARMONIC GENERATION; HEART; HISTOLOGY; NONLINEAR OPTICS; PARAMETER ESTIMATION; TISSUE;

BIAXIAL EXTENSION; BIAXIAL EXTENSION TESTING; CARDIAC MECHANICS; HUMAN VENTRICULAR MYOCARDIUM; MECHANICAL BEHAVIOR; OPTICAL CLEARING; PASSIVE MECHANICAL BEHAVIOR; SHEAR TESTING; TRIAXIAL SHEAR; TRIAXIAL SHEAR TESTING; VENTRICULAR MYOCARDIUM;

MICROSTRUCTURE;

BIOMATERIAL; COLLAGEN;

ADULT; AGED; ARTICLE; BIOMECHANICS; CLINICAL ARTICLE; DISPERSION; DYNAMICS; FEMALE; HEART DISEASE; HEART MUSCLE; HUMAN; HUMAN TISSUE; MALE; MICROSCOPY; PRIORITY JOURNAL; SECOND HARMONIC GENERATION MICROSCOPY; SHEAR STRESS; SIMULATION; VENTRICULAR MYOCARDIUM; CARDIAC MUSCLE; CHEMISTRY; HEART VENTRICLE; SHEAR STRENGTH;

COLLAGEN; HEART VENTRICLES; HUMANS; MYOCARDIUM; SHEAR STRENGTH;

EID: 84940450552     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2015.06.031     Document Type: Article

References (85)

1. A.S. Go, D. Mozaffarian, V.L. Roger, E.J. Benjamin, J.D. Berry, M.J. Blaha, and et al. Heart disease and stroke statistics - 2014 update: a report from the American Heart Association Circulation 129 2014 e28 e292
2. M. Nichols, N. Townsend, R. Luengo-Fernandez, J. Leal, A. Gray, P. Scarborough, and et al. European Heart Network 2012 European Society of Cardiology, Sophia Antipolis Brussels
3. C. Gutierrez, and D.G. Blanchard Diastolic heart failure: challenges of diagnosis and treatment Am Family Physician 69 2004 2609 2616
4. S.F. Nagueh, G. Shah, Y. Wu, G. Torre-Amione, N.M. King, S. Lahmers, and et al. Altered titin expression, myocardial stiffness, and left ventricular function in patients with dilated cardiomyopathy Circulation 110 2004 155 162
5. J.D. Humphrey Cardiovascular Solid Mechanics. Cells, Tissues, and Organs 2002 Springer-Verlag New York
6. J.W. Holmes, T.K. Borg, and J.W. Covell Structure and mechanics of healing myocardial infarcts Annu. Rev. Biomed. Eng. 27 2005 223 253
7. I.J. LeGrice, B.H. Smaill, L.Z. Chai, S.G. Edgar, J.B. Gavin, and P.J. Hunter Laminar structure of the heart: ventricular myocyte arrangement and connective tissue architecture in the dog Am. J. Physiol. Heart Circ. Physiol. 269 1995 H571 H582
8. H. Ashikaga, J.W. Covell, and J.H. Omens Diastolic dysfunction in volume-overload hypertrophy is associated with abnormal shearing of myolaminar sheets Am. J. Physiol. Heart Circ. Physiol. 288 2005 H2603 H2610
9. T.P. Usyk, J.H. Omens, and A.D. McCulloch Regional septal dysfunction in a three-dimensional computational model of focal myofiber disarray Am. J. Physiol. Heart Circ. Physiol. 281 2001 H506 H514
10. M.P. Nash, and A.V. Panfilov Electromechanical model of excitable tissue to study reentrant cardiac arrhythmias Prog. Biophys. Mol. Biol. 85 2004 501 522
11. S.T. Wall, J.C. Walker, K.E. Healy, M.B. Ratcliffe, and J.M. Guccione Theoretical impact of the injection of material into the myocardium: a finite element model simulation Circulation 114 2006 2627 2635
12. S. Niederer, L. Mitchell, N. Smith, and G. Plank Simulating a human heart beat with near-real time performance Front. Physiol. 2 2011 1 7
13. T.S.E. Eriksson, A.J. Prassl, G. Plank, and G.A. Holzapfel Influence of myocardial fiber/sheet orientations on left ventricular mechanical contraction Math. Mech. Solids 18 2013 592 606
14. T.S.E. Eriksson, A.J. Prassl, G. Plank, and G.A. Holzapfel Modeling the dispersion in electro-mechanically coupled myocardium Int. J. Numer. Method Biomed. Eng. 29 2013 1267 1284
15. S. Dokos, I.J. LeGrice, B.H. Smaill, J. Kar, and A.A. Young A triaxial-measurement shear-test device for soft biological tissues J. Biomech. Eng. 122 2000 471 478
16. G.A. Holzapfel, and R.W. Ogden Constitutive modelling of passive myocardium: a structurally based framework for material characterization Philos. Trans. R. Soc. A. 367 2009 3445 3475
17. B. Wang, A. Borazjani, M. Tahai, A.L. Curry, D.T. Simionescu, J. Guan, and et al. Fabrication of cardiac patch with decellularized porcine myocardial scaffold and bone marrow mononuclear cells J. Biomed. Mater. Res. A 94 2010 1100 1110
18. L. Barandon, T. Couffinhal, P. Dufourcq, P. Alzieu, D. Daret, C. Deville, and et al. Repair of myocardial infarction by epicardial deposition of bone-marrow-cell-coated muscle patch in a murine model Ann. Thoracic Surg. 78 2004 1409 1417
19. R.S. Kellar, B.R. Shepherd, D.F. Larson, G.K. Naughton, and S.K. Williams Cardiac patch constructed from human fibroblasts attenuates reduction in cardiac function after acute infarct Tissue Eng. 11 2005 1678 1687
20. A.J. Engler, S. Sen, H.L. Sweeney, and D.E. Discher Matrix elasticity directs stem cells linage specification Cell 126 2006 677 689
21. J. Guan, F. Wang, Z. Li, J. Chen, X. Guo, J. Liao, and et al. The stimulation of the cardiac differentiation of mesenchymal stem cells in tissue constructs that mimic myocardium structure and biomechanics Biomaterials 32 2011 5568 5580
22. F. Wang, and J. Guan Cellular cardiomyoplasty and cardiac tissue engineering for myocardial therapy Adv. Drug Deliv. Rev. 62 2010 784 797
23. L.L. Demer, and F.C.P. Yin Passive biaxial mechanical properties of isolated canine myocardium J. Physiol. London 339 1983 615 630
24. F.C.P. Yin, R.K. Strumpf, P.H. Chew, and S.L. Zeger Quantification of the mechanical properties of noncontracting canine myocardium under simultaneous biaxial loading J. Biomech. 20 1987 577 589
25. J.D. Humphrey, R.K. Strumpf, and F.C.P. Yin Determination of constitutive relation for passive myocardium - Part I and II J. Biomech. Eng. 112 1990 333 346
26. M.S. Sacks, and C.J. Chuong Biaxial mechanical properties of passive right ventricular free wall myocardium J. Biomech. Eng. 115 1993 202 205
27. V.P. Novak, F.C.P. Yin, and J.D. Humphrey Regional mechanical properties of passive myocardium J. Biomech. Eng. 27 1994 403 412
28. M.R. Hill, M.A. Simon, D. Valdez-Jasso, W. Zhang, H.C. Champion, and M.S. Sacks Structural and mechanical adaptations of right ventricle free wall myocardium to pressure overload Ann. Biomed. Eng. 42 2014 2451 2465
29. G.A. Holzapfel, and R.W. Ogden On planar biaxial tests for anisotropic nonlinearly elastic solids. A continuum mechanical framework Math. Mech. Solids 14 2009 474 489
30. S. Dokos, B.H. Smaill, A.A. Young, and I.J. LeGrice Shear properties of passive ventricular myocardium Am. J. Physiol. 283 2002 H2650 H2659
31. W.J. Karlon, A.D. McCulloch, J.W. Covell, J.J. Hunter, and J.H. Omens Regional dysfunction correlates with myofiber disarray in transgenic mice with ventricular expression of ras Am. J. Physiol. Heart Circ. Physiol. 278 2000 H898 906
32. J. van der Bel-Kahn Muscle fiber disarray in common heart diseases Am. J. Cardiol. 40 1977 355 364
33. T. Ragan, J.D. Sylvan, K.H. Kim, H. Huang, K. Bahlmann, R.T. Lee, and et al. High-resolution whole organ imaging using two-photon tissue cytometry J. Biomed. Opt. 12 2007 014015
34. A.J. Schriefl, A.J. Reinisch, S. Sankaran, D.M. Pierce, and G.A. Holzapfel Quantitative assessment of collagen fiber orientations from 2D images of soft biological tissues J. R. Soc. Interface 9 2012 3081 3093
35. A.J. Schriefl, H. Wolinski, P. Regitnig, S.D. Kohlwein, and G.A. Holzapfel An automated approach for 3D quantification of fibrillar structures in optically cleared soft biological tissues J. R. Soc. Interface 10 2013 20120760
36. L.A. Mulieri, G. Hasenfuss, F. Ittleman, E.M. Blanchard, and N.R. Alpert Protection of human left ventricular myocardium from cutting injury with 2,3-butanedione monoxime Circ. Res. 65 1989 1441 1449
37. G. Sommer, D.C. Haspinger, M. Andrä, M. Sacherer, C. Viertler, P. Regitnig, et al. Quantification of shear deformations and corresponding stresses in the biaxially tested human myocardium. Ann. Biomed. Eng. (in press), http://dx.doi.org/10.1007/s10439-015-1281-z.
38. o, and temperature on the dynamic stiffness of quiescent cardiac trabeculae from rat Am. J. Physiol. Heart Circ. Physiol. 288 2005 H1662 H1667
39. D. Rohmer, A. Sitek, and G.T. Gullberg Reconstruction and visualization of fiber and laminar structure in the normal human heart from ex vivo diffusion tensor magnetic resonance imaging (DTMRI) data Invest. Radiol. 42 2007 777 789
40. G. Sommer, M. Eder, L. Kovacs, H. Pathak, L. Bonitz, C. Mueller, and et al. Multiaxial mechanical properties and constitutive modeling of human adipose tissue: a basis for preoperative simulations in plastic and reconstructive surgery Acta Biomater. 9 2013 9036 9048
41. J.D. Humphrey, R.K. Strumpf, and F.C.P. Yin Biaxial material properties of excised ventricular epicardium Am. J. Physiol. Heart Circ. Physiol. 259 1990 H101 H108
42. T.C. Gasser, R.W. Ogden, and G.A. Holzapfel Hyperelastic modelling of arterial layers with distributed collagen fibre orientations J. R. Soc. Interface 3 2006 15 35
43. R.B. Hickler Aortic and large artery stiffness: current methodology and clinical correlations Clin Cardiol. 13 1990 317 322
44. G.A. Holzapfel, G. Sommer, and P. Regitnig Anisotropic mechanical properties of tissue components in human atherosclerotic plaques J. Biomech. Eng. 126 2004 657 665
45. G.A. Holzapfel, G. Sommer, C.T. Gasser, and P. Regitnig Determination of layer-specific mechanical properties of human coronary arteries with non-atherosclerotic intimal thickening, and related constitutive modeling Am. J. Physiol. Heart Circ. Physiol. 289 2005 H2048 2058
46. G. Sommer, P. Regitnig, L. Költringer, and G.A. Holzapfel Biaxial mechanical properties of intact and layer-dissected human carotid arteries at physiological and supra-physiological loadings Am. J. Physiol. Heart Circ. Physiol. 298 2010 H898 912
47. G. Sommer, A. Schriefl, G. Zeindlinger, A. Katzensteiner, H. Ainödhofer, A. Saxena, and et al. Multiaxial mechanical response and constitutive modeling of esophageal tissues: impact on esophageal tissue engineering Acta Biomater. 9 2013 9379-9091
48. J.D. Humphrey, R.K. Strumpf, and F.C.P. Yin Determination of constitutive relation for passive myocardium: II. Parameter estimation J. Biomech. Eng. 112 1990 340 346
49. D.H. Lin Yin FC.A multiaxial constitutive law for mammalian left ventricular myocardium in steady-state barium contracture or tetanus J. Biomech. Eng. 120 1998 504 517
50. K.B. Gupta, M.B. Ratcliffe, M.A. Fallert, L.H. Edmunds Jr, and D.K. Bogen Changes in passive mechanical stiffness of myocardial tissue with aneurysm formation Circulation 89 1994 2315 2326
51. H. Ghaemi, K. Behdinan, and A.D. Spence In vitro technique in estimation of passive mechanical properties of bovine heart part I. Experimental techniques and data Med. Eng. Phys. 31 2009 76 82
52. P. Wang, F. Zhu, N.H. Lee, and K. Konstantopoulos Shear-induced interleukin-6 synthesis in chondrocytes: roles of E prostanoid (EP) 2 and EP3 in cAMP/protein kinase A- and PI3-K/Akt-dependent NF-κB activation J. Biol. Chem. 285 2010 24793 24804
53. D. Valdez-Jasso, M.A. Simon, H.C. Champion, and M.S. Sacks A murine experimental model for the mechanical behaviour of viable right-ventricular myocardium J. Physiol. 590 2012 4571 4584
54. L. Mullins, and N.R. Tobin Theoretical model for the elastic behavior of filler-reinforced vulcanized rubbers Rubber Chem. Technol. 30 1957 551 571
55. J.L. Emery, J.H. Omens, and A.D. McCulloch Strain softening in rat left ventricular myocardium J. Biomech. Eng. 119 1997 6 12
56. J.L. Emery, J.H. Omens, and A.D. McCulloch Biaxial mechanics of the passively overstretched left ventricle Am. J. Physiol. 272 1997 H2299 H2305
57. J.L. Emery, J.H. Omens, O.A. Mathieu-Costello, and A.D. McCulloch Structural mechanisms of acute ventricular strain softening Int. J. Cardiovasc. Med. Sci. 1 1998 241 250
58. D.A. MacKenna, J.H. Omens, A.D. McCulloch, and J.W. Covell Contributions of collagen matrix to passive left ventricular mechanics in isolated rat hearts Am. J. Physiol. 266 1994 H1007 H1018
59. J.B. Caulfield, and T.K. Borg The collagen network of the heart Lab. Invest. 40 1979 364 372
60. H.L. Granzier, and T.C. Irving Passive tension in cardiac muscle: contribution of collagen, titin, microtubules, and intermediate filaments Biophys. J. 68 1995 1027 1044
61. K. Wang, R. McCarter, J. Wright, J. Beverly, and R. Ramirez-Mitchell Viscoelasticity of the sarcomere matrix of skeletal muscles. The titin-myosin composite filament is a dual-stage molecular spring Biophys. J. 64 1993 1161 1177
62. M.R. Rehorn, A.K. Schroer, and S.S. Blemker The passive properties of muscle fibers are velocity dependent J. Biomech. 47 2014 687 693
63. Y.C. Fung Biomechanics Mechanical Properties of Living Tissues second ed. 1993 Springer-Verlag New York
64. C.A.J. Schulze-Bauer, P. Regitnig, and G.A. Holzapfel Mechanics of the human femoral adventitia including high-pressure response Am. J. Physiol. Heart Circ. Physiol. 282 2002 H2427 H2440
65. K.D. Costa, Y. Takayama, A.D. McCulloch, and J.W. Covell Laminar fiber architecture and three-dimensional systolic mechanics in canine ventricular myocardium Am. J. Physiol. 276 1999 H595 H607
66. Y. Takayama, K.D. Costa, and J.W. Covell Contribution of laminar myofiber architecture to load-dependent changes in mechanics of LV myocardium Am. J. Physiol. Heart Circ. Physiol. 282 2002 H1510 H1520
67. T. Toursel, L. Stevens, H. Granzier, and Y. Mounier Passive tension of rat skeletal soleus muscle fibers: effects of unloading conditions J. Appl. Physiol. 92 2002 1465 1472
68. M.S. Kellermayer, S.B. Smith, C. Bustamante, and H.L. Granzier Complete unfolding of the titin molecule under external force J. Struct. Biol. 122 1998 197 205
69. M.S. Kellermayer, S.B. Smith, C. Bustamante, and H.L. Granzier Mechanical fatigue in repetitively stretched single molecules of titin Biophys. J. 80 2001 852 863
70. D. Labeit, K. Watanabe, C. Witt, H. Fujita, Y. Wu, S. Lahmers, and et al. Calcium-dependent molecular spring elements in the giant protein titin Proc. Nat. Acad. Sci. USA 100 2003 13716 13721
71. J. Nedrud, S. Labeit, M. Gotthardt, and H. Granzier Mechanics on myocardium deficient in the N2B region of titin: the cardiac-unique spring element improves efficiency of the cardiac cycle Biophys. J. 101 2011 1385 1392
72. M. Linari, L. Lucii, M. Reconditi, M.E. Casoni, H. Amenitsch, S. Bernstorff, and et al. A combined mechanical and X-ray diffraction study of stretch potentiation in single frog muscle fibres J. Physiol. 526 2000 589 596
73. D.E. Rassier, and W. Herzog Considerations on the history dependence of muscle contraction J. Appl. Physiol. 96 2004 419 427
74. R.S. Kirton, A.J. Taberner, P.M.F. Nielsen, A.A. Young, and D.S. Loiselle Strain softening behaviour in nonviable rat right-ventricular trabeculae, in the presence and the absence of butanedione monoxime Exp. Physiol. 89 2004 593 604
75. R.S. Kirton, A.J. Taberner, A.A. Young, P.M.F. Nielsen, and D.S. Loiselle Strain softening is not present during axial extensions of rat intact right ventricular trabeculae in the presence or absence of 2,3-butanedione monoxime Am. J. Physiol. Heart Circ. Physiol. 286 2004 H708 H715
76. W.A. Linke, V.I. Popov, and G.H. Pollack Passive and active tension in single cardiac myofibrils Biophys. J. 67 1994 782 792
77. W.A. Linke, M.L. Bartoo, M.A. Ivemeyer, and G.H. Pollack Limits of titin extension in single cardiac myofibrils J. Muscle Res. Cell Motil. 17 1996 425 428
78. M. Helmes, K. Trombitás, T. Centner, M. Kellermayer, S. Labeit, W.A. Linke, and et al. Mechanically driven contour-length adjustment in rat cardiac titin's unique N2B sequence: titin is an adjustable spring Circ. Res. 84 1999 1339 1352
79. P. Campagnola Second harmonic generation imaging microscopy: applications to diseases diagnostics Anal. Chem. 83 2011 3224 3231
80. R.M. Smith, A. Matiukas, C.W. Zemlin, and M. Pertsov Nondestructive optical determination of fiber organization in intact myocardial wall Microsc. Res. Tech. 71 2008 510 516
81. A. Cheng, F. Langer, F. Rodriguez, J.C. Criscione, G.T. Daughters, D.C. Miller, and et al. Transmural sheet strains in the lateral wall of the ovine left ventricle Am. J. Physiol. Heart Circ. Physiol. 289 2005 1234 1241
82. A.J. Pope, G.B. Sands, B.H. Smaill, and I.J. LeGrice Three-dimensional transmural organization of perimysial collagen in the heart Am. J. Physiol. Heart Circ. Physiol. 295 2008 H1243 H1252
83. D.D. Streeter Jr, H.M. Spotnitz, D.P. Patel, J. Ross Jr, and E.H. Sonnenblick Fibre orientation in the canine left ventricle during diastole and systole Circ. Res. 24 1969 339 347
84. D.D. Streeter Jr, and D.L. Basset An engineering analysis of myocardial fiber orientation in pig's left ventricle in systole Anat. Rec. 155 1966 503 511
85. F.J. Vetter, S.B. Simons, S. Mironov, C.J. Hyatt, and A.M. Pertsov Epicardial fiber organization in swine right ventricle and its impact on propagation Circ. Res. 96 2005 244 251