Bone mechanical properties vary with age; meanwhile, a close relationship exists among bone mechanical properties at different levels. Therefore, conducting multilevel analyses for bone structures with different ages are necessary to elucidate the effects of aging on bone mechanical properties at different levels. In this study, an approach that combined microfinite element (micro-FE) analysis and macrocompressive test was established to simulate the failure of male rat femoral cortical bone. Micro-FE analyses were primarily performed for rat cortical bones with different ages to simulate their failure processes under compressive load. Tissue-level failure strains in tension and compression of these cortical bones were then back-calculated by fitting the experimental stress–strain curves. Thus, tissue-level failure strains of rat femoral cortical bones with different ages were quantified. The tissue-level failure strain exhibited a biphasic behavior with age: in the period of skeletal maturity (1–7 months of age), the failure strain gradually increased; when the rat exceeded 7 months of age, the failure strain sharply decreased. In the period of skeletal maturity, both the macro- and tissue-levels mechanical properties showed a large promotion. In the period of skeletal aging (9–15 months of age), the tissue-level mechanical properties sharply deteriorated; however, the macromechanical properties only slightly deteriorated. The age-related changes in tissue-level failure strain were revealed through the analysis of male rat femoral cortical bones with different ages, which provided a theoretical basis to understand the relationship between rat cortical bone mechanical properties at macro- and tissue-levels and decrease of bone strength with age.

References

References
1.
Chen
,
H.
,
Zhou
,
X.
,
Shoumura
,
S.
,
Emura
,
S.
, and
Bunai
,
Y.
,
2010
, “
Age- and Gender-Dependent Changes in Three-Dimensional Microstructure of Cortical and Trabecular Bone at the Human Femoral Neck
,”
Osteoporosis Int.
,
21
(
4
), pp.
627
636
.
2.
Stein
,
M. S.
,
Thomas
,
C. D. L.
,
Feik
,
S. A.
,
Wark
,
J. D.
, and
Clement
,
J. G.
,
1998
, “
Bone Size and Mechanics at the Femoral Diaphysis Across Age and Sex
,”
J. Biomech.
,
31
(
12
), pp.
1101
1110
.
3.
Wang
,
X.
,
Shen
,
X.
,
Li
,
X.
, and
Agrawal
,
C. M.
,
2002
, “
Age-Related Changes in the Collagen Network and Toughness of Bone
,”
Bone
,
31
(
1
), pp.
1
7
.
4.
Ural
,
A.
, and
Vashishth
,
D.
,
2006
, “
Cohesive Finite Element Modeling of Age-Related Toughness Loss in Human Cortical Bone
,”
J. Biomech.
,
39
(
16
), pp.
2974
2982
.
5.
Vilayphiou
,
N.
,
Boutroy
,
S.
,
Sornay-Rendu
,
E.
,
Van Rietbergen
,
B.
,
Munoz
,
F.
,
Delmas
,
P. D.
, and
Chapurlat
,
R.
,
2010
, “
Finite Element Analysis Performed on Radius and Tibia HR-pQCT Images and Fragility Fractures at All Sites in Postmenopausal Women
,”
Bone
,
46
(
4
), pp.
1030
1037
.
6.
Urano
,
T.
, and
Inoue
,
S.
,
2014
, “
Genetics of Osteoporosis
,”
Biochem. Biophys. Res. Commun.
,
452
(
2
), pp.
287
293
.
7.
Chappard
,
D.
,
Baslé
,
M. F.
,
Legrand
,
E.
, and
Audran
,
M.
,
2011
, “
New Laboratory Tools in the Assessment of Bone Quality
,”
Osteoporosis Int.
,
22
(
8
), pp.
2225
2240
.
8.
Zhang
,
R.
,
Gong
,
H.
,
Zhu
,
D.
,
Gao
,
J. Z.
,
Fang
,
J.
, and
Fan
,
Y. B.
,
2014
, “
Seven Day Insertion Rest in Whole Body Vibration Improves Multi-Level Bone Quality in Tail Suspension Rats
,”
PLoS One
,
9
(
3
), pp.
1
12
.
9.
Gao
,
J. Z.
,
Gong
,
H.
,
Zhang
,
R.
, and
Zhu
,
D.
,
2015
, “
Age-Related Regional Deterioration Patterns and Changes in Nanoscale Characterizations of Trabeculae in the Femoral Head
,”
Exp. Gerontol.
,
62
, pp.
63
72
.
10.
Lloyd
,
A. A.
,
Wang
,
Z. X.
, and
Donnelly
,
E.
,
2015
, “
Multiscale Contribution of Bone Tissue Material Property Heterogeneity to Trabecular Bone Mechanical Behavior
,”
ASME J. Biomech. Eng.
,
137
(
1
), p.
010801
.
11.
Zhang
,
R.
,
Gong
,
H.
,
Zhu
,
D.
,
Ma
,
R. S.
,
Fang
,
J.
, and
Fan
,
Y. B.
,
2015
, “
Multi-Level Femoral Morphology and Mechanical Properties of Rats of Different Ages
,”
Bone
,
76
, pp.
76
87
.
12.
Ferguson
,
V. L.
,
Ayers
,
R. A.
,
Bateman
,
T. A.
, and
Simske
,
S. J.
,
2003
, “
Bone Development and Age-Related Bone Loss in Male C57BL/6J Mice
,”
Bone
,
33
(
3
), pp.
387
398
.
13.
Wang
,
L.
,
Banu
,
J.
,
McMahan
,
C. A.
, and
Kalu
,
D. N.
,
2001
, “
Male Rodent Model of Age-Related Bone Loss in Men
,”
Bone
,
29
(
2
), pp.
141
148
.
14.
Djonic
,
D.
,
Milovanovic
,
P.
,
Nikolic
,
S.
,
Ivovic
,
M.
,
Marinkovic
,
J.
,
Beck
,
T.
, and
Djuric
,
M.
,
2011
, “
Inter-Sex Differences in Structural Properties of Aging Femora: Implications on Differential Bone Fragility: A Cadaver Study
,”
J. Bone Miner. Metab.
,
29
(
4
), pp.
449
457
.
15.
Kapuš
,
O.
,
Gába
,
A.
,
Svoboda
,
Z.
, and
Botek
,
M.
,
2014
, “
Relationship Between Body Composition and Bone Mineral Density of the Lumbar Spine and Proximal Femur: Influence of Years Since Menopause
,”
Mod. Rheumatol.
,
24
(
3
), pp.
505
510
.
16.
DallAra
,
E.
,
Luisier
,
B.
,
Schmidt
,
R.
,
Kainberger
,
F.
,
Zysset
,
P.
, and
Pahr
,
D.
,
2013
, “
A Nonlinear QCT-Based Finite Element Model Validation Study for the Human Femur Tested in Two Configurations In Vitro
,”
Bone
,
52
(
1
), pp.
27
38
.
17.
Nishiyama
,
K. K.
,
Gilchrist
,
S.
,
Guy
,
P.
,
Cripton
,
P.
, and
Boyd
,
S. K.
,
2013
, “
Proximal Femur Bone Strength Estimated by a Computationally Fast Finite Element Analysis in a Sideways Fall Configuration
,”
J. Biomech.
,
46
(
7
), pp.
1231
1236
.
18.
Luisier
,
B.
,
DallAra
,
E.
, and
Pahr
,
D. H.
,
2014
, “
Orthotropic HR-pQCT-Based FE Models Improve Strength Predictions for Stance but Not for Side-Way Fall Loading Compared to Isotropic QCT-Based FE Models of Human Femurs
,”
J. Mech. Behav. Biomed.
,
32
, pp.
287
299
.
19.
Pahr
,
D. H.
,
Schwiedrzik
,
J.
,
DallAra
,
E.
, and
Zysset
,
P. K.
,
2014
, “
Clinical Versus Pre-Clinical FE Models for Vertebral Body Strength Predictions
,”
J. Mech. Behav. Biomed. Mater.
,
33
, pp.
76
83
.
20.
Huang
,
H. L.
,
Tsai
,
M. T.
,
Lin
,
D. J.
,
Chien
,
C. S.
, and
Hsu
,
J. T.
,
2010
, “
A New Method to Evaluate the Elastic Modulus of Cortical Bone by Using a Combined Computed Tomography and Finite Element Approach
,”
Comput. Biol. Med.
,
40
(
4
), pp.
464
468
.
21.
Li
,
S.
,
Demirci
,
E.
, and
Silberschmidt
,
V. V.
,
2013
, “
Variability and Anisotropy of Mechanical Behavior of Cortical Bone in Tension and Compression
,”
J. Mech. Behav. Biomed. Mater.
,
21
, pp.
109
120
.
22.
Carretta
,
R.
,
Luisier
,
B.
,
Bernoulli
,
D.
,
Stüssi
,
E.
,
Müller
,
R.
, and
Lorenzetti
,
S.
,
2013
, “
Novel Method to Analyze Post-Yield Mechanical Properties at Trabecular Bone Tissue Level
,”
J. Mech. Behav. Biomed. Mater.
,
20
, pp.
6
18
.
23.
Cyganik
,
Ł.
,
Binkowski
,
M.
,
Kokot
,
G.
,
Rusin
,
T.
,
Popik
,
P.
,
Bolechała
,
F.
,
Nowak
,
R.
,
Wróbel
,
Z.
, and
John
,
A.
,
2014
, “
Prediction of Young's Modulus of Trabeculae in Microscale Using Macro-Scale's Relationships Between Bone Density and Mechanical Properties
,”
J. Mech. Behav. Biomed. Mater.
,
36
, pp.
120
134
.
24.
MacNeil
,
J. A.
, and
Boyd
,
S. K.
,
2008
, “
Bone Strength at the Distal Radius Can Be Estimated From High-Resolution Peripheral Quantitative Computed Tomography and the Finite Element Method
,”
Bone
,
42
(
6
), pp.
1203
1213
.
25.
Hambli
,
R.
, and
Allaoui
,
S.
,
2013
, “
A Robust 3D Finite Element Simulation of Human Proximal Femur Progressive Fracture Under Stance Load With Experimental Validation
,”
Ann. Biomed. Eng.
,
41
(
12
), pp.
2515
2527
.
26.
Carretta
,
R.
,
Stüssi
,
E.
,
Müller
,
R.
, and
Lorenzetti
,
S.
,
2013
, “
Within Subject Heterogeneity in Tissue-Level Post-Yield Mechanical and Material Properties in Human Trabecular Bone
,”
J. Mech. Behav. Biomed. Mater.
,
24
, pp.
64
73
.
27.
Harrison
,
N. M.
,
McDonnell
,
P.
,
Mullins
,
L.
,
Wilson
,
N.
,
O'Mahoney
,
D.
, and
McHugh
,
P. E.
,
2013
, “
Failure Modelling of Trabecular Bone Using a Non-Linear Combined Damage and Fracture Voxel Finite Element Approach
,”
Biomech. Model. Mechanobiol.
,
12
(
2
), pp.
225
241
.
28.
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
.
29.
Bekas
,
C.
,
Curioni
,
A.
,
Arbenz
,
P.
,
Flaig
,
C.
,
Van Lenthe
,
G. H.
,
Müller
,
R.
, and
Wirth
,
A. J.
,
2010
, “
Extreme Scalability Challenges in Micro-Finite Element Simulations of Human Bone
,”
Concurrency Comput. Pract. Exper.
,
22
(
16
), pp.
2282
2296
.
30.
van Lenthe
,
G. H.
, and
Müller
,
R.
,
2006
, “
Prediction of Failure Load Using Micro-Finite Element Analysis Models: Toward In Vivo Strength Assessment
,”
Drug Discovery Today
,
3
(
2
), pp.
221
229
.
31.
Mueller
,
T. L.
,
Christen
,
D.
,
Sandercott
,
S.
,
Boyd
,
S. K.
,
Rietbergen
,
B. V.
,
Eckstein
,
F.
,
Lochmüller
,
E. M.
,
Müller
,
R.
, and
van Lenthe
,
G. H.
,
2011
, “
Computational Finite Element Bone Mechanics Accurately Predicts Mechanical Competence in the Human Radius of an Elderly Population
,”
Bone
,
48
(
6
), pp.
1232
1238
.
32.
Van Der Linden
,
J. C.
,
Homminga
,
J.
,
Verhaar
,
J. A. N.
, and
Weinans
,
H.
,
2001
, “
Mechanical Consequences of Bone Loss in Cancellous Bone
,”
J. Bone Miner. Res.
,
16
(
3
), pp.
457
465
.
33.
Gong
,
H.
,
Zhang
,
M.
, and
Fan
,
Y. B.
,
2011
, “
Micro-Finite Element Analysis of Trabecular Bone Yield Behavior-Effects of Tissue Nonlinear Material Properties
,”
J. Mech. Med. Biol.
,
11
(
3
), pp.
563
580
.
34.
Koivumäki
,
J. E. M.
,
Thevenot
,
J.
,
Pulkkinen
,
P.
,
Kuhn
,
V.
,
Link
,
T. M.
,
Eckstein
,
F.
, and
Jämsä
,
T.
,
2012
, “
Cortical Bone Finite Element Models in the Estimation of Experimentally Measured Failure Loads in the Proximal Femur
,”
Bone
,
51
(
4
), pp.
737
740
.
35.
Ali
,
A. A.
,
Cristofolini
,
L.
,
Schileo
,
E.
,
Hu
,
H. X.
,
Taddei
,
F.
,
Kim
,
R. H.
,
Rullkoetter
,
P. J.
, and
Laz
,
P. J.
,
2014
, “
Specimen-Specific Modeling of Hip Fracture Pattern and Repair
,”
J. Biomech.
,
47
(
2
), pp.
536
543
.
36.
Qasim
,
M.
,
Natarajan
,
R. N.
,
An
,
H. S.
, and
Andersson
,
G. B. J.
,
2014
, “
Damage Accumulation Location Under Cyclic Loading in the Lumbar Disc Shifts From Inner Annulus Lamellae to Peripheral Annulus With Increasing Disc Degeneration
,”
J. Biomech.
,
47
(
1
), pp.
24
31
.
37.
Bayraktar
,
H. H.
,
Morgan
,
E. F.
,
Niebur
,
G. L.
,
Morris
,
G. E.
,
Wong
,
E. K.
, and
Keaveny
,
T. M.
,
2004
, “
Comparison of the Elastic and Yield Properties of Human Femoral Trabecular and Cortical Bone Tissue
,”
J. Biomech.
,
37
(
1
), pp.
27
35
.
38.
Feerick
,
E. M.
,
Liu
,
X. Y.
, and
McGarry
,
P.
,
2013
, “
Anisotropic Mode-Dependent Damage of Cortical Bone Using the Extended Finite Element Method (XFEM)
,”
J. Mech. Behav. Biomed. Mater.
,
20
, pp.
77
89
.
39.
Ziv
,
V.
,
Wagner
,
H. D.
, and
Weiner
,
S.
,
1996
, “
Microstructure-Microhardness Relations in Parallel-Fibered and Lamellar Bone
,”
Bone
,
18
(
5
), pp.
417
428
.
40.
Milovanovic
,
P.
,
Potocnik
,
J.
,
Djonic
,
D.
,
Nikolic
,
S.
,
Zivkovic
,
V.
,
Djuric
,
M.
, and
Rakocevic
,
Z.
,
2012
, “
Age-Related Deterioration in Trabecular Bone Mechanical Properties at Material Level: Nanoindentation Study of the Femoral Neck in Women by Using AFM
,”
Exp. Gerontol.
,
47
(
2
), pp.
154
159
.
41.
Rasoulian
,
R.
,
Najafi
,
A. R.
,
Chittenden
,
M.
, and
Jasiuk
,
I.
,
2013
, “
Reference Point Indentation Study of Age-Related Changes in Porcine Femoral Cortical Bone
,”
J. Biomech.
,
46
(
10
), pp.
1689
1696
.
42.
Burr
,
D. B.
,
Liu
,
Z. Y.
, and
Allen
,
M. R.
,
2015
, “
Duration-Dependent Effects of Clinically Relevant Oral Alendronate Doses on Cortical Bone Toughness in Beagle Dogs
,”
Bone
,
71
, pp.
58
62
.
43.
Hambli
,
R.
,
2013
, “
Micro-CT Finite Element Model and Experimental Validation of Trabecular Bone Damage and Fracture
,”
Bone
,
56
(
2
), pp.
363
374
.
44.
Hamrick
,
M. W.
,
McPherron
,
A. C.
, and
Lovejoy
,
C. O.
,
2002
, “
Bone Mineral Content and Density in the Humerus of Adult Myostatin-Deficient Mice
,”
Calcif. Tissue Int.
,
71
(
1
), pp.
63
68
.
45.
Augat
,
P.
, and
Schorlemmer
,
S.
,
2006
, “
The Role of Cortical Bone and Its Microstructure in Bone Strength
,”
Age Ageing
,
35
(
S2
), pp.
27
31
.
46.
Allena
,
R.
, and
Cluzel
,
C.
,
2014
, “
Identification of Anisotropic Tensile Strength of Cortical Bone Using Brazilian Test
,”
J. Mech. Behav. Biomed. Mater.
,
38
, pp.
134
142
.
47.
Nalla
,
R. K.
,
Stölken
,
J. S.
,
Kinney
,
J. H.
, and
Ritchie
,
R. O.
,
2005
, “
Fracture in Human Cortical Bone: Local Fracture Criteria and Toughening Mechanisms
,”
J. Biomech.
,
38
(
7
), pp.
1517
1525
.
48.
Pietruszczak
,
S.
,
Gdela
,
K.
,
Webber
,
C. E.
, and
Inglis
,
D.
,
2007
, “
On the Assessment of Brittle-Elastic Cortical Bone Fracture in the Distal Radius
,”
Eng. Fract. Mech.
,
74
(
12
), pp.
1917
1927
.
49.
Pithioux
,
M.
,
Chabrand
,
P.
,
Hochard
,
C.
, and
Champsaur
,
P.
,
2011
, “
Improved Femoral Neck Fracture Predictions Using Anisotropic Failure Criteria Models
,”
J. Mech. Med. Biol.
,
11
(
5
), pp.
1333
1346
.
50.
Tang
,
S. Y.
, and
Vashishth
,
D.
,
2011
, “
The Relative Contributions of Non-Enzymatic Glycation and Cortical Porosity on the Fracture Toughness of Aging Bone
,”
J. Biomech.
,
44
(
2
), pp.
330
336
.
51.
Holguin
,
N.
,
Brodt
,
M. D.
,
Sanchez
,
M. E.
, and
Silva
,
M. J.
,
2014
, “
Aging Diminishes Lamellar and Woven Bone Formation Induced by Tibial Compression in Adult C57BL/6
,”
Bone
,
65
, pp.
83
91
.
52.
Cook
,
R. B.
, and
Zioupos
,
P.
,
2009
, “
The Fracture Toughness of Cancellous Bone
,”
J. Biomech.
,
42
(
13
), pp.
2054
2060
.
53.
McNerny
,
E. M. B.
,
Gong
,
B.
,
Morris
,
M. D.
, and
Kohn
,
D. H.
,
2015
, “
Bone Fracture Toughness and Strength Correlate With Collagen Cross-Link Maturity in a Dose-Controlled Lathyrism Mouse Model
,”
J. Bone Miner. Res.
,
30
(
3
), pp.
455
464
.
54.
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
.
55.
Szabó
,
M. E.
, and
Thurner
,
P. J.
,
2013
, “
Anisotropy of Bovine Cortical Bone Tissue Damage Properties
,”
J. Biomech.
,
46
(
1
), pp.
2
6
.
56.
Macione
,
J.
,
Depaula
,
C. A.
,
Guzelsu
,
N.
, and
Kotha
,
S. P.
,
2010
, “
Correlation Between Longitudinal, Circumferential, and Radial Moduli in Cortical Bone: Effect of Mineral Content
,”
J. Mech. Behav. Biomed. Mater.
,
3
(
5
), pp.
405
413
.
57.
Weiner
,
S.
,
Traub
,
W.
, and
Wagner
,
H. D.
,
1999
, “
Lamellar Bone: Structure-Function Relations
,”
J. Struct. Biol.
,
126
(
3
), pp.
241
255
.
58.
Olszta
,
M. J.
,
Cheng
,
X. G.
,
Jee
,
S. S.
,
Kumar
,
R.
,
Kim
,
Y. Y.
,
Kaufman
,
M. J.
,
Douglas
,
E. P.
, and
Gower
,
L. B.
,
2007
, “
Bone Structure and Formation: A New Perspective
,”
Mater. Sci. Eng. R
,
58
(
3–5
), pp.
77
116
.
59.
Ruff
,
C. B.
, and
Hayes
,
W. C.
,
1988
, “
Sex Differences in Age-Related Remodeling of the Femur and Tibia
,”
J. Orthop. Res.
,
6
(
6
), pp.
886
896
.
60.
Riggs
,
B. L.
,
Melton
,
L. J.
,
Robb
,
R. A.
,
Camp
,
J. J.
,
Atkinson
,
E. J.
,
Peterson
,
J. M.
,
Rouleau
,
P. A.
,
McCollough
,
C. H.
,
Bouxsein
,
M. L.
, and
Khosla
,
S.
,
2004
, “
Population-Based Study of Age and Sex Differences in Bone Volumetric Density, Size, Geometry, and Structure at Different Skeletal Sites
,”
J. Bone Miner. Res.
,
19
(
12
), pp.
1945
1954
.
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