Prior multiaxial strength studies on trabecular bone have either not addressed large variations in bone volume fraction and microarchitecture, or have not addressed the full range of multiaxial stress states. Addressing these limitations, we utilized micro-computed tomography (μCT) based nonlinear finite element analysis to investigate the complete 3D multiaxial failure behavior of ten specimens (5 mm cube) of human trabecular bone, taken from three anatomic sites and spanning a wide range of bone volume fraction (0.09–0.36), mechanical anisotropy (range of E3/E1 = 3.0–12.0), and microarchitecture. We found that most of the observed variation in multiaxial strength behavior could be accounted for by normalizing the multiaxial strength by specimen-specific values of uniaxial strength (tension, compression in the longitudinal and transverse directions). Scatter between specimens was reduced further when the normalized multiaxial strength was described in strain space. The resulting multiaxial failure envelope in this normalized-strain space had a rectangular boxlike shape for normal–normal loading and either a rhomboidal boxlike shape or a triangular shape for normal-shear loading, depending on the loading direction. The finite element data were well described by a single quartic yield criterion in the 6D normalized-strain space combined with a piecewise linear yield criterion in two planes for normal-shear loading (mean error ± SD: 4.6 ± 0.8% for the finite element data versus the criterion). This multiaxial yield criterion in normalized-strain space can be used to describe the complete 3D multiaxial failure behavior of human trabecular bone across a wide range of bone volume fraction, mechanical anisotropy, and microarchitecture.

References

1.
Vasu
,
R.
,
Carter
,
D. R.
, and
Harris
,
W. H.
,
1981
, “
Stress Distributions in the Acetabular Region. I. Before and After Total Joint Replacement
,”
J. Biomech.
,
15
(
3
), pp.
155
164
.10.1016/0021-9290(82)90247-0
2.
Carter
,
D. R.
,
Orr
,
T. E.
, and
Fyhrie
,
D. P.
,
1989
, “
Relationships Between Loading History and Femoral Cancellous Bone Architecture
,”
J. Biomech.
,
22
(
3
), pp.
231
244
.10.1016/0021-9290(89)90091-2
3.
Cheal
,
E. J.
,
Spector
,
M.
, and
Hayes
,
W. C.
,
1992
, “
Role of Loads and Prosthesis Material Properties on the Mechanics of the Proximal Femur After Total Hip Arthroplasty
,”
J. Orthop. Res.
,
10
(
3
), pp.
405
422
.10.1002/jor.1100100314
4.
Stone
,
J. L.
,
Beaupre
,
G. S.
, and
Hayes
,
W. C.
,
1983
, “
Multiaxial Strength Characteristics of Trabecular Bone
,”
J. Biomech.
,
16
(
9
), pp.
743
752
.10.1016/0021-9290(83)90083-0
5.
Keaveny
,
T. M.
,
Wachtel
,
E. F.
,
Zadesky
,
S. P.
, and
Arramon
,
Y. P.
,
1999
, “
Application of the Tsai-Wu Quadratic Multiaxial Failure Criterion to Bovine Trabecular Bone
,”
ASME J. Biomech. Eng.
,
121
(
1
), pp.
99
107
.10.1115/1.2798051
6.
Fenech
,
C. M.
, and
Keaveny
,
T. M.
,
1999
, “
A Cellular Solid Criterion for Predicting the Axial-Shear Failure Properties of Trabecular Bone
,”
ASME J. Biomech. Eng.
,
121
(
4
), pp.
414
422
.10.1115/1.2798339
7.
Rincon-Kohli
,
L.
, and
Zysset
,
P. K.
,
2009
, “
Multi-Axial Mechanical Properties of Human Trabecular Bone
,”
Biomech. Model. Mechanobiol.
,
8
(
3
), pp.
195
208
.10.1007/s10237-008-0128-z
8.
Niebur
,
G. L.
,
Feldstein
,
M. J.
, and
Keaveny
,
T. M.
,
2002
, “
Biaxial Failure Behavior of Bovine Tibial Trabecular Bone
,”
ASME J. Biomech. Eng.
,
124
(
6
), pp.
699
705
.10.1115/1.1517566
9.
Bayraktar
,
H. H.
,
Gupta
,
A.
,
Kwon
,
R. Y.
,
Papadopoulos
,
P.
, and
Keaveny
,
T. M.
,
2004
, “
The Modified Super-Ellipsoid Yield Criterion for Human Trabecular Bone
,”
ASME J. Biomech. Eng.
,
126
(
6
), pp.
677
684
.10.1115/1.1763177
10.
Wolfram
,
U.
,
Gross
,
T.
,
Pahr
,
D. H.
,
Schwiedrzik
,
J.
,
Wilke
,
H. J.
, and
Zysset
,
P. K.
,
2012
, “
Fabric-Based Tsai-Wu Yield Criteria for Vertebral Trabecular Bone in Stress and Strain Space
,”
J. Mech. Behav. Biomed. Mater.
,
15
, pp.
218
228
.10.1016/j.jmbbm.2012.07.005
11.
Cowin
,
S. C.
,
1986
, “
Fabric Dependence of an Anisotropic Strength Criterion
,”
Mech. Mater.
,
5
(
3
), pp.
251
260
.10.1016/0167-6636(86)90022-0
12.
Zysset
,
P. K.
, and
Rincon-Kohli
,
L.
,
2006
, “
An Alternative Fabric-Based Yield and Failure Criterion for Trabecular Bone
,”
Mechanics of Biological Tissue
,
G. A.
Holzapfel
and
R. W.
Ogden
, eds., Springer, Berlin, Germany, pp.
457
470
.
13.
Garcia
,
D.
,
Zysset
,
P. K.
,
Charlebois
,
M.
, and
Curnier
,
A.
,
2009
, “
A Three-Dimensional Elastic Plastic Damage Constitutive Law for Bone Tissue
,”
Biomech. Model. Mechanobiol.
,
8
(
2
), pp.
149
165
.10.1007/s10237-008-0125-2
14.
Dall'Ara
,
E.
,
Pahr
,
D.
,
Varga
,
P.
,
Kainberger
,
F.
, and
Zysset
,
P.
,
2012
, “
QCT-Based Finite Element Models Predict Human Vertebral Strength In Vitro Significantly Better Than Simulated DXA
,”
Osteoporosis Int.
,
23
(
2
), pp.
563
572
.10.1007/s00198-011-1568-3
15.
Chevalier
,
Y.
,
Pahr
,
D.
, and
Zysset
,
P. K.
,
2009
, “
The Role of Cortical Shell and Trabecular Fabric in Finite Element Analysis of the Human Vertebral Body
,”
ASME J. Biomech. Eng.
,
131
(
11
), p.
111003
.10.1115/1.3212097
16.
Sanyal
,
A.
, and
Keaveny
,
T. M.
,
2013
, “
Biaxial Normal Strength Behavior in the Axial-Transverse Plane for Human Trabecular Bone–Effects of Bone Volume Fraction, Microarchitecture, and Anisotropy
,”
ASME J. Biomech. Eng.
,
135
(
12
), p.
121010
.10.1115/1.4025679
17.
Deshpande
,
V. S.
, and
Fleck
,
N. A.
,
2001
, “
Multi-Axial Yield Behavior of Polymer Foams
,”
Acta Mater.
,
49
(
10
), pp.
1859
1866
.10.1016/S1359-6454(01)00058-1
18.
Wang
,
D. A.
, and
Pan
,
J.
,
2006
, “
A Non-Quadratic Yield Function for Polymeric Foams
,”
Int. J. Plast.
,
22
(
3
), pp.
434
458
.10.1016/j.ijplas.2005.03.011
19.
Kopperdahl
,
D. L.
, and
Keaveny
,
T. M.
,
1998
, “
Yield Strain Behavior of Trabecular Bone
,”
J. Biomech.
,
31
(
7
), pp.
601
608
.10.1016/S0021-9290(98)00057-8
20.
Morgan
,
E. F.
, and
Keaveny
,
T. M.
,
2001
, “
Dependence of Yield Strain of Human Trabecular Bone on Anatomic Site
,”
J. Biomech.
,
34
(
5
), pp.
569
577
.10.1016/S0021-9290(01)00011-2
21.
Niebur
,
G. L.
,
Yuen
,
J. C.
,
Hsia
,
A. C.
, and
Keaveny
,
T. M.
,
1999
, “
Convergence Behavior of High-Resolution Finite Element Models of Trabecular Bone
,”
ASME J. Biomech. Eng.
,
121
(
6
), pp.
629
635
.10.1115/1.2800865
22.
Charras
,
G. T.
, and
Guldberg
,
R. E.
,
2000
, “
Improving the Local Solution Accuracy of Large-Scale Digital Image-Based Finite Element Analyses
,”
J. Biomech.
,
33
(
2
), pp.
255
259
.10.1016/S0021-9290(99)00141-4
23.
van Rietbergen
,
B.
,
Odgaard
,
A.
,
Kabel
,
J.
, and
Huiskes
,
R.
,
1996
, “
Direct Mechanics Assessment of Elastic Symmetries and Properties of Trabecular Bone Architecture
,”
J. Biomech.
,
29
(
12
), pp.
1653
1657
.10.1016/S0021-9290(96)80021-2
24.
Turner
,
C. H.
, and
Cowin
,
S. C.
,
1988
, “
Errors Introduced by Off-Axis Measurements of the Elastic Properties of Bone
,”
J. Biomech.
,
110
(
3
), pp.
213
214
.10.1115/1.3108433
25.
Papadopoulos
,
P.
, and
Lu
,
J.
,
2001
, “
On the Formulation and Numerical Solution of Problems in Anisotropic Finite Plasticity
,”
Comput. Methods Appl. Mech. Eng
,
190
(
37–38
), pp.
4889
4910
.10.1016/S0045-7825(00)00355-8
26.
Bevill
,
G.
,
Eswaran
,
S. K.
,
Gupta
,
A.
,
Papadopoulos
,
P.
, and
Keaveny
,
T. M.
,
2006
, “
Influence of Bone Volume Fraction and Architecture on Computed Large-Deformation Failure Mechanisms in Human Trabecular Bone
,”
Bone
,
39
(
6
), pp.
1218
1225
.10.1016/j.bone.2006.06.016
27.
Sanyal
,
A.
,
Gupta
,
A.
,
Bayraktar
,
H. H.
,
Kwon
,
R. Y.
, and
Keaveny
,
T. M.
,
2012
, “
Shear Strength Behavior of Human Trabecular Bone
,”
J. Biomech.
,
45
(
15
), pp.
2513
2519
.10.1016/j.jbiomech.2012.07.023
28.
Fields
,
A. J.
,
Nawathe
,
S.
,
Eswaran
,
S. K.
,
Jekir
,
M. G.
,
Adams
,
M. F.
,
Papadopoulos
,
P.
, and
Keaveny
,
T. M.
,
2012
, “
Vertebral Fragility and Structural Redundancy
,”
J. Bone Miner. Res.
,
27
(
10
), pp.
2152
2158
.10.1002/jbmr.1664
29.
Nawathe
,
S.
,
Akhlaghpour
,
H.
,
Bouxsein
,
M. L.
, and
Keaveny
,
T. M.
,
2013
, “
Microstructural Failure Mechanisms in the Human Proximal Femur for Sideways Fall Loading
,”
J. Bone Miner. Res.
,
29
(
2
), pp.
507
515
.10.1002/jbmr.2033
30.
Tsai
,
S.
, and
Wu
,
E.
,
1971
, “
A General Theory for Strength of Anisotropic Materials
,”
J. Compos. Mater.
,
5
(
1
), pp.
58
80
.10.1177/002199837100500106
31.
Chakrabarty
,
J.
,
1987
,
Theory of Plasticity
,
McGraw-Hill, Inc
. New York.
32.
Gibson
,
L. J.
,
Ashby
,
M. F.
,
Zhang
,
J.
, and
Triantafillou
,
T. C.
,
1989
, “
Failure Surfaces for Cellular Materials Under Multiaxial Loads—I. Modelling
,”
Int. J. Mech. Sci.
,
31
(
9
), pp.
635
663
.10.1016/S0020-7403(89)80001-3
33.
Walker
,
J. D.
, and
Thacker
,
B. H.
,
1999
,
Yield Surfaces for Anisotropic Plates
,
American Institute of Physics
,
Snowbird, UT
, pp.
567
570
.
34.
Barlat
,
F.
,
Lege
,
D. J.
, and
Brem
,
J. C.
,
1991
, “
A Six-Component Yield Function for Anisotropic Materials
,”
Int. J. Plast.
,
7
(
7
), pp.
693
712
.10.1016/0749-6419(91)90052-Z
35.
Karafillis
,
A. P.
, and
Boyce
,
M. C.
,
1993
, “
A General Anisotropic Yield Criterion Using Bounds and a Transformation Weighting Tensor
,”
J. Mech. Phys. Solids
,
41
(
12
), pp.
1859
1886
.10.1016/0022-5096(93)90073-O
36.
Gol'denblat
,
I. I.
, and
Kopnov
,
V. A.
,
1965
, “
Strength of Glass-Reinforced Plastics in the Complex Stress State
,”
Polym. Mech.
,
1
(
2
), pp.
54
59
.10.1007/BF00860685
37.
von Mises
,
R.
,
1928
, “
Mechanik der Plastischen Formäenderung von Kristallen
,”
Z. Angew. Math. Mech.
,
8
(
3
), pp.
161
185
.10.1002/zamm.19280080302
38.
Hill
,
R.
,
1983
,
The Mathematical Theory of Plasticity
,
Clarendon, Oxford University
,
Oxford, New York
.
39.
Hoffman
,
O.
,
1967
, “
The Brittle Strength of Orthotropic Materials
,”
J. Compos. Mater.
,
1
(
2
), pp.
200
206
.10.1177/002199836700100210
40.
Schwiedrzik
,
J. J.
,
Wolfram
,
U.
, and
Zysset
,
P. K.
,
2013
, “
A Generalized Anisotropic Quadric Yield Criterion and its Application to Bone Tissue at Multiple Length Scales
,”
Biomech. Model. Mechanobiol.
,
12
(
6
), pp.
1155
1168
.10.1007/s10237-013-0472-5
41.
Bower
,
M. V.
, and
Koedam
,
D. H.
,
1997
, “
Tensor Polynomial Failure Criterion: Coefficient Limits Based on Convexity Requirements
,”
J. Reinf. Plast. Compos.
,
16
(
5
), pp.
435
477
.
42.
Cowin
,
S. C.
, and
He
,
Q.-C.
,
2005
, “
Tensile and Compressive Stress Yield Criteria for Cancellous Bone
,”
J. Biomech.
,
38
(
1
), pp.
141
144
.10.1016/j.jbiomech.2004.03.003
43.
Arramon
,
Y. P.
,
Mehrabadi
,
M. M.
,
Martin
,
D. W.
, and
Cowin
,
S. C.
,
2000
, “
A Multidimensional Anisotropic Strength Criterion Based on Kelvin Modes
,”
Int. J. Solids Struct.
,
37
(
21
), pp.
2915
2935
.10.1016/S0020-7683(98)00338-2
44.
Kelly
,
N.
, and
McGarry
,
J. P.
,
2012
, “
Experimental and Numerical Characterisation of the Elasto-Plastic Properties of Bovine Trabecular Bone and Trabecular Bone Analogue
,”
J. Mech. Behav. Biomed. Mater.
,
9
, pp.
184
197
.10.1016/j.jmbbm.2011.11.013
45.
Troy
,
K. L.
, and
Grabiner
,
M. D.
,
2007
, “
Off-Axis Loads Cause Failure of the Distal Radius at Lower Magnitudes Than Axial Loads: A Finite Element Analysis
,”
J. Biomech.
,
40
(
8
), pp.
1670
1675
.10.1016/j.jbiomech.2007.01.018
46.
Bevill
,
G.
,
Farhamand
,
F.
, and
Keaveny
,
T. M.
,
2009
, “
Heterogeneity of Yield Strain in Low-Density Versus High-Density Human Trabecular Bone
,”
J. Biomech.
,
42
(
13
), pp.
2165
2170
.10.1016/j.jbiomech.2009.05.023
47.
Chang
,
W. C.
,
Christensen
,
T. M.
,
Pinilla
,
T. P.
, and
Keaveny
,
T. M.
,
1999
, “
Uniaxial Yield Strains for Bovine Trabecular Bone are Isotropic and Asymmetric
,”
J. Orthop. Res.
,
17
(
4
), pp.
582
585
.10.1002/jor.1100170418
48.
Nawathe
,
S.
,
Juillard
,
F.
, and
Keaveny
,
T. M.
,
2013
, “
Theoretical Bounds for the Influence of Tissue-Level Ductility on the Apparent-Level Strength of Human Trabecular Bone
,”
J. Biomech.
,
46
(
7
), pp.
1293
1299
.10.1016/j.jbiomech.2013.02.011
49.
Yeh
,
O. C.
, and
Keaveny
,
T. M.
,
2001
,“
Relative Roles of Microdamage and Microfracture in the Mechanical Behavior of Trabecular Bone
,”
J. Orthop. Res.
,
19
(
6
), pp.
1001
1007
.10.1016/S0736-0266(01)00053-5
50.
Guo
,
X. E.
,
McMahon
,
T. A.
,
Keaveny
,
T. M.
,
Hayes
,
W. C.
, and
Gibson
,
L. J.
,
1994
, “
Finite Element Modeling of Damage Accumulation in Trabecular Bone Under Cyclic Loading
,”
J. Biomech.
,
27
(
2
), pp.
145
155
.10.1016/0021-9290(94)90203-8
51.
Silva
,
M. J.
, and
Gibson
,
L. J.
,
1997
, “
The Effects of Non-Periodic Microstructure and Defects on the Compressive Strength of Two-Dimensional Cellular Solids
,”
Intern. J. Mech. Sci.
,
39
(
5
), pp.
549
563
.10.1016/S0020-7403(96)00065-3
You do not currently have access to this content.