The constitutive law of the material comprising any structure is essential for mechanical analysis since this law enables calculation of the stresses from the deformations and vice versa. To date, there is no constitutive law for actively contracting myocardial tissue. Using 2,3-butanedione monoxime to protect the myocardium from mechanical trauma, we subjected thin midwall slices of rabbit myocardium to multiaxial stretching first in the passive state and then during steady-state barium contracture or during tetani in ryanodine-loaded tissue. Assuming transverse isotropy in both the passive and active conditions, we used our previously described methods (Humphrey et al., 1990a) to obtain both passive and active constitutive laws. The major results of this study are: (1) This is the first multiaxial constitutive law for actively contracting mammalian myocardium. (2) The functional forms of the constitutive law for barium contracture and ryanodine-induced tetani are the same but differ from those in the passive state. Hence, one cannot simply substitute differing values for the coefficients of the passive law to describe the active tissue properties. (3) There are significant stresses developed in the cross-fiber direction (more than 40 percent of those in the fiber direction) that cannot be attributed to either deformation effects or nonparallel muscle fibers. These results provide the foundation for future mechanical analyses of the heart.

1.
Abe
H.
,
Nakamura
T.
,
Motomiya
M.
,
Konno
K.
, and
Arai
S.
,
1978
, “
Stresses in left ventricular wall and biaxial stress-strain relation of the cardiac muscle fiber for the potassium arrested heart
,”
ASME JOURNAL OF BIOMECHANICAL ENGINEERING
,
100
, pp.
116
121
.
2.
Abe
H.
,
1981
, “
Stress–strain relation of cardiac muscle determined from ventricular pressure-time relationships during isovolumic contractions
,”
J. Biomech.
,
14
, pp.
357
360
.
3.
Azhari
H.
,
Weiss
J. L.
,
Rogers
W. L.
,
Siu
C. P.
,
Zerhouni
E. A.
, and
Shapiro
E. P.
,
1993
, “
Noninvasive quantification of principal strains in normal canine hearts using tagged MRI images in 3-D
,”
Am. J. Physiol.
,
264
, pp.
H205–H216
H205–H216
.
4.
Borg
T. K.
, and
Caulfield
J. B.
,
1981
, “
The collagen matrix of the heart
,”
Fed. Proc.
,
40
, pp.
2037
2041
.
5.
Brenner
B.
, and
Yu
L. C.
,
1991
, “
Characterization of radial force and radial stiffness in Ca2+-activated skinned fibres of the rabbit psoas muscle
,”
Journal of Physiology
,
441
, pp.
703
718
.
6.
Capasso
J. M.
,
Strobeck
J. E.
,
Malhotra
A.
,
Scheuer
J.
, and
Sonnenblick
E. H.
,
1982
, “
Contractile behavior of rat myocardium after reversal of hypertensive hypertrophy
,”
Am. J. Physiol.
,
242
, pp.
H882–H889
H882–H889
.
7.
Chadwick, R. S., 1981, “The myocardium as a fluid-fiber continuum: Passive equilibrium configurations,” Advances in Bioengineering, pp. 135–138.
8.
Chew
P. H.
,
Yin
F. C. P.
, and
Zeger
S. L.
,
1986
, “
Biaxial stress-strain properties of canine pericardium
,”
J. Mol. Cell. Cardiol.
,
18
, pp.
567
578
.
9.
Downs
J.
,
Halperin
H. R.
,
Humphrey
J.
, and
Yin
F. C. P.
,
1990
, “
An improved video-based computer tracking system for soft biomaterials testing
,”
IEEE Trans. Biomed. Engr.
,
37
, pp.
903
907
.
10.
Fung
Y. C.
,
Fronek
K.
, and
Patitucci
P.
,
1979
, “
Pseudoelasticity of arteries and the choice of its mathematical expression
,”
Am. J. Physiol.
,
237
(
5
), pp.
H620–H631
H620–H631
.
11.
Fung
Y. C. B.
,
1968
, “
Biomechanics: Its scope, history and some problems of continuum mechanics in physiology
,”
Appl. Mech. Rev.
,
21
, pp.
1
20
.
12.
Gould
P.
,
Ghista
D. N.
,
Brombolich
L.
, and
Mirsky
I.
,
1972
, “
In vivo stresses in the human left ventricular wall: Analysis accounting for the irregular 3-dimensional geometry and comparison with idealised geometry analyses
,”
J. Biomech.
,
5
, pp.
521
539
.
13.
Guccione
J. M.
,
Waldman
L. K.
, and
McCulloch
A. D.
,
1993
, “
Mechanics of active contraction in cardiac muscle: Part 11—Cylindrical models of the systolic left ventricle
,”
ASME JOURNAL OF BIOMECHANICAL ENGINEERING
,
115
, pp.
82
90
.
14.
Guccione
J. M.
, and
McCulloch
A. D.
,
1993
, “
Mechanics of active contraction in cardiac muscle: Part I—constitutive relations for fiber stress that describe deactivation
,”
ASME JOURNAL OF BIOMECHANICAL ENGINEERING
,
115
, pp.
72
81
.
15.
Heethaar, R. M., Robb, R. A., Pao, Y. C., and Ritman, E. L., 1976, Three-dimensional stress and strain in the intact heart. Academic Press, New York, pp. 337–342.
16.
Heng
M. K.
,
Janz
R. F.
, and
Jobin
J.
,
1985
, “
Estimation of regional stress in the left ventricular septum and free wall: An echocardiographic study suggesting a mechanism for asymmetric septal hypertrophy
,”
Am. Heart J.
,
110
, pp.
84
90
.
17.
Horowitz, A., Lanir, Y., Perl, M., Yin, F. C. P., Chew, P., Strumpf, R., and Zeger, S., 1986, “A three-dimensional constitutive law for passive myocardium,” ASME Adv. Bioeng., pp. 144–145.
18.
Huisman
R. M.
,
Elzinga
G.
,
Westerhof
N.
, and
Sipkema
P.
,
1980
, “
Measurement of left ventricular wall stress
,”
Cardiovasc. Res.
,
14
, pp.
142
153
.
19.
Humphrey
J. D.
,
Strumpf
R. K.
, and
Yin
F. C. P.
,
1990
a, “
Determination of a constitutive relation for passive myocardium: I. A new functional form
,”
ASME JOURNAL OF BIOMECHANICAL ENGINEERING
,
112
, pp.
333
339
.
20.
Humphrey
J. D.
,
Strumpf
R. K.
, and
Yin
F. C. P.
,
1990
b, “
Determination of a constitutive relation for passive myocardium: II. Parameter estimation
,”
ASME JOURNAL OF BIOMECHANICAL ENGINEERING
,
112
, pp.
340
346
.
21.
Huyghe
J. M.
,
Arts
T.
,
Van Campen
D. H.
, and
Reneman
R. S.
,
1992
, “
Porous medium finite element model of the beating left ventricle
,”
Am. J. Physiol.
,
262
, pp.
H1256–H1267
H1256–H1267
.
22.
Janz
R. F.
,
1982
, “
Estimation of local myocardial stress
,”
Am. J. Physiol.
,
242
, pp.
H875–H881
H875–H881
.
23.
Janz
R. F.
, and
Grimm
A. F.
,
1972
, “
Finite-element model for the mechanical behavior of the left ventricle
,”
Circ. Res.
,
30
, pp.
244
252
.
24.
Jewell
B. R.
,
1977
, “
A reexamination of the influence of muscle length on myocardial performance
,”
Circ. Res.
,
40
, pp.
221
230
.
25.
Kohlhardt
M.
,
Haastert
H. P.
, and
Krause
H.
,
1973
, “
Evidence of non-specificity of the Ca channel in mammalian myocardial fibre membranes
,”
Pflugers Archives
,
342
, pp.
125
136
.
26.
Lanir
Y.
, and
Fung
Y. C.
,
1974
, “
Two-dimensional mechanical properties of rabbit skin II. Experimental results
,”
J. Biomech.
,
7
, pp.
171
182
.
27.
Lanir
Y.
, and
Nevo
E.
,
1993
, “
The orientation of an intramyocardial vessel affects its mechanical loading by the surrounding myocardium
,”
ASME JOURNAL OF BIOMECHANICAL ENGINEERING
,
115
, pp.
327
328
.
28.
Livingston
J. Z.
,
Resar
J. R.
, and
Yin
F. C. P.
,
1993
, “
Effect of tetanic myocardial contraction on coronary pressure-low relationships
,”
Am. J. Physiol.
,
265
, pp.
H1215–H1226
H1215–H1226
.
29.
Livingston
J. Z.
,
Halperin
H. R.
, and
Yin
F. C. P.
,
1994
, “
Accounting for the Gregg effect in tetanized coronary arterial pressure-flow relationships
,”
Cardiovasc. Res.
,
28
, pp.
228
234
.
30.
Marban
E.
,
Kusuoka
H.
,
Yue
D. T.
,
Weisfeldt
M. L.
, and
Wier
W. G.
,
1986
, “
Maximal Ca2+-activated force elicited by tetanization of ferret papillary muscle and whole heart: Mechanism and characteristics of steady contractile activation in intact myocardium
,”
Circ. Res.
,
59
, pp.
262
269
.
31.
Maughan
D. W.
, and
Godt
R. E.
,
1981
, “
Radial forces within muscle fibers in rigor
,”
J. Gen. Physiol.
,
77
, pp.
49x–64
49x–64
.
32.
McPherson
D. D.
,
Skorton
D. J.
,
Kodiyalam
S.
,
Petre
L.
,
Noel
M. P.
,
Kieso
R.
,
Kerber
R. E.
,
Collins
S. M.
, and
Chandran
K. B.
,
1987
, “
Finite element analysis of myocardial diastolic function using three-dimensional echocardiographic reconstructions: Application of a new method for study of acute ischemia in dogs
,”
Circ. Res.
,
60
, pp.
674
682
.
33.
Mirsky
I.
,
1969
, “
Left ventricular stresses in the intact human heart
,”
Biophys. J.
,
9
, pp.
189
208
.
34.
Mirsky
I.
, and
Parmley
W. W.
,
1973
, “
Assessment of passive elastic stiffness for isolated heart muscle and the intact heart
,”
Circ. Res.
,
33
, pp.
233
243
.
35.
Moriarty
T. F.
,
1980
, “
The law of Laplace: Its limitations as a relation for diastolic pressure, volume, or wall stress of the left ventricle
,”
Circ. Res.
,
46
, pp.
321
331
.
36.
Mulieri
L. A.
,
Hasenfuss
G.
,
Ittleman
F.
,
Blanchard
E. M.
, and
Alpert
N. R.
,
1989
, “
Protection of human left ventricular myocardium from cutting injury with 2,3-butanedione monoxime
,”
Circ. Res.
,
65
, pp.
1441
1444
.
37.
Novak
V. P.
,
Yin
F. C. P.
, and
Humphrey
J. D.
,
1994
, “
Regional mechanical properties of passive myocardium
,”
J. Biomech.
,
27
, pp.
403
412
.
38.
Ohayon
J.
, and
Chadwick
R. S.
,
1988
, “
Effects of collagen microstructure on the mechanics of the left ventricle
,”
Biophys. J.
,
54
, pp.
1077
1088
.
39.
Pao
Y. C.
,
Ritman
E. L.
, and
Wood
E. H.
,
1974
, “
Finite-element analysis of left ventricular myocardial stresses
,”
J. Biomech.
,
7
, pp.
469
477
.
40.
Ritman
E. L.
,
Kinsey
J. H.
,
Robb
R. A.
,
Gilbert
B. K.
,
Harris
L. D.
, and
Wood
E. H.
,
1980
, “
Three-dimensional imaging of heart, lungs and circulation
,”
Science
,
210
, pp.
273
280
.
41.
Robinson
T. F.
,
Cohen-Gould
L.
,
Factor
S. M.
,
Eghbali
M.
, and
Blumenfeld
O. O.
,
1988
, “
Structure and function of connective tissue in cardiac muscle: Collagen types I and III in endomysial struts and pericellular fibers
,”
Scanning Microscopy
,
2
, pp.
1005
1015
.
42.
Saeki
V.
,
Kato
C.
,
Horikoshi
T.
, and
Yanagisawa
K.
,
1984
, “
Effects of Ba2+ on the mechanical properties of glycerinated heart muscle
,”
Pflugers Archives
,
400
, pp.
235
240
.
43.
Saeki
Y.
,
Sagawa
K.
, and
Suga
H.
,
1978
, “
Dynamic stiffness of cat heart muscle in Ba2+-induced contracture
,”
Circ. Res.
,
42
, pp.
324
333
.
44.
Saeki
Y.
,
Sagawa
K.
, and
Suga
H.
,
1980
, “
Transient tension responses of heart muscle in Ba2+ contracture to step length changes
,”
Am. J. Physiol.
,
238
, pp.
H340–H347
H340–H347
.
45.
Schoenberg
M.
,
1980
, “
Geometrical factors influencing muscle force development I. The effect of filament spacing upon axial forces
,”
Biophys. J.
,
30
, pp.
51
68
.
46.
Shibata
T.
,
Hunter
W. C.
,
Yang
A.
, and
Sagawa
K.
,
1987
, “
Dynamic stiffness measured in central segment of excised rabbit papillary muscles during barium contracture
,”
Circ. Res.
,
60
, pp.
756
769
.
47.
Shibata
T.
,
Berman
M. R.
,
Hunter
W. C.
, and
Jacobus
W. E.
,
1990
, “
Metabolic and functional consequences of barium-induced contracture in rabbit myocardium
,”
Am. J. Physiol.
,
259
, pp.
H1566–H1574
H1566–H1574
.
48.
Smaill, B., and Hunter, P., 1991, “Structure and function of the diastolic heart: material properties of passive myocardium,” L. Glass, P. Hunter and A. McCulloch, eds., Theory of Heart, Springer-Verlag, pp. 1–29.
49.
Streeter
D. D.
,
Vaishnav
R. N.
,
Patel
D. J.
,
Spotnitz
H. M.
, and
Sonnenblick
E. H.
,
1970
, “
Stress distribution in the canine ventricle during diastole and systole
,”
Biophys. J.
,
10
, pp.
345
363
.
50.
Strumpf
R. K.
,
Humphrey
J. D.
, and
Yin
F. C. P.
,
1993
, “
Biaxial mechanical properties of passive and tetanized canine diaphragm
,”
Am. J. Physiol.
,
265
, pp.
H469–H475
H469–H475
.
51.
Umazume
Y.
,
Onodera
S.
, and
Higuchi
H.
,
1986
, “
Width and lattice spacing in radially compressed frog skinned muscle fibres at various pH values, magnesium ion concentrations and ionic strengths
,”
J. Muscle Res. Cell Mot.
,
7
, pp.
251
258
.
52.
Urthaler
F.
,
Walker
A. A.
,
Reeves
D. N. S.
, and
Hefner
L. L.
,
1988
, “
Maximal twitch tension in intact length-clamped ferret papillary muscles evoked by modified postextrasystolic potentiation
,”
Circ. Res.
,
62
, pp.
65
74
.
53.
Vinson
C. A.
,
Gibson
D. G.
, and
Yettram
A. L.
,
1979
, “
Analysis of left ventricular behaviour in diastole by means of finite element method
,”
Br. Heart J.
,
41
, pp.
60
67
.
54.
Vis
M. A.
,
Sipkema
P.
, and
Westerhof
N.
,
1995
, “
Modelling the pressure-area relations of coronary blood vessels embedded in cardiac muscle in diastole and systole
,”
Am. J. Physiol.
,
268
, pp.
H2531–H2543
H2531–H2543
.
55.
Wong
A. Y. K.
, and
Rautaharju
P. M.
,
1968
, “
Stress distribution within the left ventricular wall approximated as a thick ellipsoidal shell
,”
Am. Heart J.
,
75
, pp.
649
662
.
56.
Xu
S.
,
Brenner
B.
, and
Yu
L. C.
,
1993
, “
State-dependent radial elasticity of attached cross-bridges in single skinned fibres of rabbit psoas muscle
,”
Journal of Physiology
,
465
, pp.
749
765
.
57.
Yin
F. C. P.
,
1981
, “
Ventricular wall stress
,”
Circ. Res.
,
49
, pp.
829
842
.
58.
Yin
F. C. P.
,
1985
, “
Applications of the finite-element method to ventricular mechanics
,”
Critical Reviews in Bioengineering
,
12
, pp.
311
342
.
59.
Yin
F. C. P.
,
Chew
P. H.
, and
Zeger
S. L.
,
1986
, “
An approach to quantification of biaxial tissue stress-strain data
,”
J. Biomech.
,
19
, pp.
27
37
.
60.
Zahalak
G. I.
,
1996
, “
Non-axial muscle stress and stiffness
,”
Journal of Theoretical Biology
,
182
, pp.
59
84
.
61.
Zinemanas
D.
,
Beyar
R.
, and
Sideman
S.
,
1995
, “
An integrated model of LV muscle mechanics, coronary flow, and fluid and mass transport
,”
Am. J. Physiol.
,
268
, pp.
H633–H645
H633–H645
.
This content is only available via PDF.
You do not currently have access to this content.