A two-level micromechanical model of cortical bone based on a generalized self-consistent method was developed to take into consideration the transversely isotropic elasticity of many microstructural features in cortical bone, including Haversian canals, resorption cavities, and osteonal and interstitial lamellae. In the first level, a single osteon was modeled as a two-phase composite such that Haversian canals were represented by elongated pores while the surrounding osteonal lamellae were considered as matrix. In the second level, osteons and resorption cavities were modeled as multiple inclusions while interstitial lamellae were regarded as matrix. The predictions of cortical bone elasticity from this two-level micromechanical model were mostly in agreement with experimental data for the dependence of transversely isotropic elasticity of human femoral cortical bone on porosity. However, variation in cortical bone elastic constants was greater in experimental data than in model predictions. This could be attributed to variations in the elastic properties of microstructural features in cortical bone. The present micromechanical model of cortical bone will be useful in understanding the contribution of cortical bone porosity to femoral neck fractures.

1.
Katz
,
J. L.
, 1981, “
Composite Material Models for Cortical Bone
,”
Mechanical Properties of Bone
,
S. C.
Cowin
, ed.,
ASME
,
New York
, pp.
171
184
.
2.
Currey
,
J. D.
, 1964, “
Three Analogies to Explain the Mechanical Properties of Bone
,”
Biorheology
0006-355X,
2
, pp.
1
10
.
3.
Katz
,
J. L.
, 1971, “
Hard Tissue as a Composite Material. I. Bounds on the Elastic Behavior
,”
J. Biomech.
0021-9290,
4
, pp.
455
473
.
4.
Piekarski
,
K.
, 1973, “
Analysis of Bone as a Composite Material
,”
Int. J. Eng. Sci.
0020-7225,
11
, pp.
557
565
.
5.
Pidaparti
,
R. M.
, and
Burr
,
D. B.
, 1992, “
Collagen Fiber Orientation and Geometry Effects on the Mechanical Properties of Secondary Osteons
,”
J. Biomech.
0021-9290,
25
, pp.
869
880
.
6.
Wagner
,
H. D.
, and
Weiner
,
S.
, 1992, “
On the Relationship Between the Microstructure of Bone and Its Mechanical Stiffness
,”
J. Biomech.
0021-9290,
25
, pp.
1311
1320
.
7.
Mammone
,
J. F.
, and
Hudson
,
S. M.
, 1993, “
Micromechanics of Bone Strength and Fracture
,”
J. Biomech.
0021-9290,
26
, pp.
439
446
.
8.
Pidaparti
,
R. M.
,
Chandran
,
A.
,
Takano
,
Y.
, and
Turner
,
C. H.
, 1996, “
Bone Mineral Lies Mainly Outside Collagen Fibrils: Predictions of a Composite Model for Osteonal Bone
,”
J. Biomech.
0021-9290,
29
, pp.
909
916
.
9.
Ascenzi
,
A.
, 1988, “
The Micromechanics Versus the Macromechanics of Cortical Bone—A Comprehensive Presentation
,”
ASME J. Biomech. Eng.
0148-0731,
110
, pp.
357
363
.
10.
Hogan
,
H. A.
, 1992, “
Micromechanics Modeling of Haversian Cortical Bone Properties
,”
J. Biomech.
0021-9290,
25
, pp.
549
556
.
11.
Sevostianov
,
I.
, and
Kachanov
,
M.
, 2000, “
Impact of the Porous Microstructure on the Overall Elastic Properties of the Osteonal Cortical Bone
,”
J. Biomech.
0021-9290,
33
, pp.
881
888
.
12.
Aoubiza
,
B.
,
Crolet
,
J. M.
, and
Meunier
,
A.
, 1996, “
On the Mechanical Characterization of Compact Bone Structure Using the Homogenization Theory
,”
J. Biomech.
0021-9290,
29
, pp.
1539
1547
.
13.
Hellmich
,
C.
, and
Ulm
,
F. J.
, 2002, “
Are Mineralized Tissues Open Crystal Foams Reinforced by Crosslinked Collagen? Some Energy Arguments
,”
J. Biomech.
0021-9290,
35
, pp.
1199
1212
.
14.
Takano
,
Y.
,
Turner
,
C. H.
, and
Burr
,
D. B.
, 1996, “
Mineral Anisotropy in Mineralized Tissues Is Similar Among Species and Mineral Growth Occurs Independently of Collagen Orientation in Rats: Results From Acoustic Velocity Measurements
,”
J. Bone Miner. Res.
0884-0431,
11
, pp.
1292
1301
.
15.
Hasegawa
,
K.
,
Turner
,
C. H.
, and
Burr
,
D. B.
, 1994, “
Contribution of Collagen and Mineral to the Elastic Anisotropy of Bone
,”
Calcif. Tissue Int.
0171-967X,
55
, pp.
381
386
.
16.
Zysset
,
P. K.
,
Guo
,
X. E.
,
Hoffler
,
C. E.
,
Moore
,
K. E.
, and
Goldstein
,
S. A.
, 1999, “
Elastic Modulus and Hardness of Cortical and Trabecular Bone Lamellae Measured by Nanoindentation in the Human Femur
,”
J. Biomech.
0021-9290,
32
, pp.
1005
1012
.
17.
Rho
,
J. Y.
,
Roy
,
M. E.
II
,
Tsui
,
T. Y.
, and
Pharr
,
G. M.
, 1999, “
Elastic Properties of Microstructural Components of Human Bone Tissue as Measured by Nanoindentation
,”
J. Biomed. Mater. Res.
0021-9304,
45
, pp.
48
54
.
18.
Fan
,
Z.
,
Swadener
,
J. G.
,
Rho
,
J. Y.
,
Roy
,
M. E.
, and
Pharr
,
G. M.
, 2002, “
Anisotropic Properties of Human Tibial Cortical Bone as Measured by Nanoindentation
,”
J. Orthop. Res.
0736-0266,
20
, pp.
806
810
.
19.
Currey
,
J. D.
, and
Zioupos
,
P.
, 2001, “
The Effect of Porous Microstructure on the Anisotropy of Bone-Like Tissue: A Counterexample
,”
J. Biomech.
0021-9290,
34
, pp.
707
710
.
20.
Kerner
,
E. H.
, 1956, “
The Elastic and Thermoelastic Properties of Composite Media
,”
Proc. Phys. Soc. London, Sect. B
0370-1301,
69
, pp.
807
808
.
21.
Christensen
,
R. M.
, and
Lo
,
K. H.
, 1979, “
Solutions for Effective Shear Properties in Three Phase Sphere and Cylinder Models
,”
J. Mech. Phys. Solids
0022-5096,
27
, pp.
315
330
.
22.
Christensen
,
R. M.
, 1990, “
A Critical Evaluation for a Class of Micro-Mechanics Models
,”
J. Mech. Phys. Solids
0022-5096,
38
, pp.
379
404
.
23.
Huang
,
Y.
,
Hu
,
K. X.
,
Wei
,
X.
, and
Chandra
,
A.
, 1994, “
A Generalized Self-Consistent Mechanics Method for Composite Materials with Multiphase Inclusions
,”
J. Mech. Phys. Solids
0022-5096,
42
, pp.
491
504
.
24.
Black
,
J.
,
Mattson
,
R.
, and
Korostoff
,
E.
, 1974, “
Haversian Osteons: Size, Distribution, Internal Structure, and Orientation
,”
J. Biomed. Mater. Res.
0021-9304,
8
, pp.
299
319
.
25.
Dong
,
X. N.
, 2002, “
Micromechanics of Osteonal Cortical Bone
,” Ph.D. thesis, Columbia University, New York, NY.
26.
Dong
,
X. N.
,
Zhang
,
X.
,
Huang
,
Y. Y.
, and
Guo
,
X. E.
, 2005, “
A Generalized Self-Consistent Estimate for the Effective Elastic Moduli of Fiber-Reinforced Composite Materials with Multiple Transversely Isotropic Inclusions
,”
Int. J. Mech. Sci.
0020-7403,
47
, pp.
922
940
.
27.
Dong
,
X. N.
, and
Guo
,
X. E.
, 2004, “
The Dependence of Transversely Isotropic Elasticity of Human Femoral Cortical Bone on Porosity
,”
J. Biomech.
0021-9290,
37
, pp.
1281
1287
.
28.
Hashin
,
Z.
, and
Rosen
,
B. W.
, 1964, “
The Elastic Moduli of Fiber-Reinforced Materials
,”
ASME Trans. J. Appl. Mech.
0021-8936,
31
, pp.
223
232
.
29.
Hashin
,
Z.
, 1983, “
Analysis of Composite Materials—A Survey
,”
ASME J. Appl. Mech.
0021-8936,
50
, pp.
481
505
.
30.
Budiansky
,
B.
, 1965, “
On the Elastic Moduli of Some Heterogeneous Materials
,”
J. Mech. Phys. Solids
0022-5096,
13
, pp.
223
227
.
31.
Lai
,
W. M.
,
Rubin
,
D.
, and
Krempl
,
E.
, 1993,
Introduction to Continuum Mechanics
,
Pergamon Press
,
New York
.
32.
Huang
,
Y.
,
Hwang
,
K. C.
,
Hu
,
K. X.
, and
Chandra
,
A.
, 1995, “
A Unified Energy Approach to a Class of Micromechanics Models for Composite Materials
,”
Acta Mech. Sin.
0459-1879,
11
, pp.
59
75
.
33.
Martin
,
R. B.
,
Burr
,
D. B.
, and
Sharkey
,
N. A.
, 1998,
Skeletal Tissue Mechanics
,
Springer
,
New York
.
34.
Van Buskirk
,
W. C.
,
Cowin
,
S. C.
, and
Ward
,
R. N.
, 1981, “
Ultrasonic Measurement of Orthotropic Elastic Constants of Bovine Femoral Bone
,”
ASME J. Biomech. Eng.
0148-0731,
103
, pp.
67
72
.
35.
Reilly
,
D. T.
, and
Burstein
,
A. H.
, 1975, “
The Elastic and Ultimate Properties of Compact Bone Tissue
,”
J. Biomech.
0021-9290,
8
, pp.
393
405
.
36.
Knets
,
I. V.
,
Krauya
,
U. E.
, and
Vilks
,
Y. K.
, 1975, “
Acoustic Emission in Human Bone Tissue Subjected to Longitudinal Extension
,”
Mechanika polimerov
,
11
, pp.
685
690
.
37.
Knets
,
I. V.
, 1978, “
Mechanics of Biological Tissues. A Review
,”
Polymer Mechanics (translation of Mekhanika Polimerov)
,
13
, pp.
434
440
.
38.
Wesly
,
R. L.
,
Vaishnav
,
R. N.
,
Fuchs
,
J. C.
,
Patel
,
D. J.
, and
Greenfield
,
J. C.
Jr.
, 1975, “
Static Linear and Nonlinear Elastic Properties of Normal and Arterialized Venous Tissue in Dog and Man
,”
Circ. Res.
0009-7330,
37
, pp.
509
520
.
39.
Beel
,
J. A.
,
Groswald
,
D. E.
, and
Luttges
,
M. W.
, 1984, “
Alterations in the Mechanical Properties of Peripheral Nerve Following Crush Injury
,”
J. Biomech.
0021-9290,
17
, pp.
185
193
.
40.
Hengsberger
,
S.
,
Kulik
,
A.
, and
Zysset
,
P.
, 2001, “
A Combined Atomic Force Microscopy and Nanoindentation Technique to Investigate the Elastic Properties of Bone Structural Units
,”
Eur. Cells Mater
1473-2262,
1
, pp.
12
17
.
41.
Hengsberger
,
S.
,
Kulik
,
A.
, and
Zysset
,
P.
, 2002, “
Nanoindentation Discriminates the Elastic Properties of Individual Human Bone Lamellae under Dry and Physiological Conditions
,”
Bone (N.Y.)
8756-3282,
30
, pp.
178
184
.
42.
Lang
,
S. B.
, 1970, “
Ultrasonic Method for Measuring Elastic Coefficients of Bone and Results on Fresh and Dried Bovine Bones
,”
IEEE Trans. Biomed. Eng.
0018-9294,
17
, pp.
101
105
.
43.
Yoon
,
H. S.
, and
Katz
,
J. L.
, 1976, “
Ultrasonic Wave Propagation in Human Cortical Bone—Ii. Measurements of Elastic Properties and Microhardness
,”
J. Biomech.
0021-9290,
9
, pp.
459
464
.
44.
Bonfield
,
W.
, and
Grynpas
,
M. D.
, 1977, “
Anisotropy of the Young’s Modulus of Bone
,”
Nature (London)
0028-0836,
270
, pp.
453
454
.
45.
Ashman
,
R. B.
,
Cowin
,
S. C.
,
Van Buskirk
,
W. C.
, and
Rice
,
J. C.
, 1984, “
A Continuous Wave Technique for the Measurement of the Elastic Properties of Cortical Bone
,”
J. Biomech.
0021-9290,
17
, pp.
349
361
.
46.
Katz
,
J. L.
, 1980, “
Anisotropy of Young’s Modulus of Bone
,”
Nature (London)
0028-0836,
283
, pp.
106
107
.
47.
Bonfield
,
W.
, and
Tully
,
A. E.
, 1982, “
Ultrasonic Analysis of the Youngs Modulus of Cortical Bone
,”
ASME J. Biomech. Eng.
0148-0731,
4
, pp.
23
27
.
48.
Katz
,
J. L.
,
Yoon
,
H. S.
,
Lipson
,
S.
,
Maharidge
,
R.
,
Meunier
,
A.
, and
Christel
,
P.
, 1984, “
The Effects of Remodeling on the Elastic Properties of Bone
,”
Calcif. Tissue Int.
0171-967X,
36 Suppl 1
, pp.
S31
36
.
49.
Keaveny
,
T. M.
,
Guo
,
X. E.
,
Wachtel
,
E. F.
,
McMahon
,
T. A.
, and
Hayes
,
W. C.
, 1994, “
Trabecular Bone Exhibits Fully Linear Elastic Behavior and Yields at Low Strains
,”
J. Biomech.
0021-9290,
27
, pp.
1127
1136
.
50.
Lekhnitskii
,
S. G.
, 1981,
Theory of Elasticity of an Anisotropic Body
,
Mir
,
Moscow
.
51.
Zar
,
J. H.
, 1999,
Biostatistical Analysis
,
Prentice-Hall
,
Upper Saddle River, NJ
.
52.
Crolet
,
J. M.
,
Aoubiza
,
B.
, and
Meunier
,
A.
, 1993, “
Compact Bone: Numerical Simulation of Mechanical Characteristics
,”
J. Biomech.
0021-9290,
26
, pp.
677
687
.
53.
Schaffler
,
M. B.
,
Burr
,
D. B.
, and
Frederickson
,
R. G.
, 1987, “
Morphology of the Osteonal Cement Line in Human Bone
,”
Anat. Rec.
0003-276X,
217
, pp.
223
228
.
54.
Guo
,
X. E.
,
Liang
,
L. C.
, and
Goldstein
,
S. A.
, 1998, “
Micromechanics of Osteonal Cortical Bone Fracture
,”
ASME J. Biomech. Eng.
0148-0731,
120
, pp.
112
117
.
55.
Yeni
,
Y. N.
, and
Norman
,
T. L.
, 2000, “
Fracture Toughness of Human Femoral Neck: Effect of Microstructure, Composition, and Age
,”
Bone (N.Y.)
8756-3282,
26
, pp.
499
504
.
56.
Dong
,
X. N.
, and
Guo
,
X. E.
, 2004, “
Geometric Determinants to Cement Line Debonding and Osteonal Lamellae Failure in Osteon Pushout Tests
,”
ASME J. Biomech. Eng.
0148-0731,
126
, pp.
387
390
.
57.
Skedros
,
J. G.
,
Holmes
,
J. L.
,
Vajda
,
E. G.
, and
Bloebaum
,
R. D.
, 2005, “
Cement Lines of Secondary Osteons in Human Bone Are Not Mineral-Deficient: New Data in a Historical Perspective
,”
Anat. Rec.
0003-276X,
286
, pp.
781
803
.
58.
Dong
,
X. N.
,
Zhang
,
X.
, and
Guo
,
X. E.
, 2005, “
Interfacial Strength of Cement Lines in Human Cortical Bone
,”
Mech. Chem. Biosyst.
1546-2048,
2
, pp.
63
68
.
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