Heterogeneity of material properties is an important potential contributor to bone fracture resistance because of its putative contribution to toughness, but establishing the contribution of heterogeneity to fracture risk is still in an incipient stage. Experimental studies have demonstrated changes in distributions of compositional and nanomechanical properties with fragility fracture history, disease, and pharmacologic treatment. Computational studies have demonstrated that models with heterogeneous material properties predict apparent stiffness moderately better than homogeneous models and show greater energy dissipation. Collectively, these results suggest that microscale material heterogeneity affects not only microscale mechanics but also structural performance at larger length scales.

References

1.
Cefalu
,
C. A.
,
2004
, “
Is Bone Mineral Density Predictive of Fracture Risk Reduction?
,”
Curr. Med. Res. Opin.
,
20
(
3
), pp.
341
349
.10.1185/030079903125003062
2.
Moro
,
M.
,
Hecker
,
A. T.
,
Bouxsein
,
M. L.
, and
Myers
,
E. R.
,
1995
, “
Failure Load of Thoracic Vertebrae Correlates With Lumbar Bone Mineral Density Measured by DXA
,”
Calcif. Tissue Int.
,
56
(
3
), pp.
206
209
.10.1007/BF00298611
3.
Oden
,
Z. M.
,
Selvitelli
,
D. M.
,
Hayes
,
W. C.
, and
Myers
,
E. R.
,
1998
, “
The Effect of Trabecular Structure on DXA-Based Predictions of Bovine Bone Failure
,”
Calcif. Tissue Int.
,
63
(
1
), pp.
67
73
.10.1007/s002239900491
4.
Bjarnason
,
K.
,
Hassager
,
C.
,
Svendsen
,
O. L.
,
Stang
,
H.
, and
Christiansen
,
C.
,
1996
, “
Anteroposterior and Lateral Spinal Dxa for the Assessment of Vertebral Body Strength: Comparison With Hip and Forearm Measurement
,”
Osteoporos. Int.
,
6
(
1
), pp.
37
42
.10.1007/BF01626536
5.
Cheng
,
X. G.
,
Nicholson
,
P. H.
,
Boonen
,
S.
,
Lowet
,
G.
,
Brys
,
P.
,
Aerssens
,
J.
,
Van Der Perre
,
G.
, and
Dequeker
,
J.
,
1997
, “
Prediction of Vertebral Strength In Vitro by Spinal Bone Densitometry and Calcaneal Ultrasound
,”
J. Bone Miner. Res.
,
12
(
10
), pp.
1721
1728
.10.1359/jbmr.1997.12.10.1721
6.
Linde
,
F.
,
Gothgen
,
C. B.
,
Hvid
,
I.
, and
Pongsoipetch
,
B.
,
1988
, “
Mechanical Properties of Trabecular Bone by a Non-Destructive Compression Testing Approach
,”
Eng. Med.
,
17
(
1
), pp.
23
29
.10.1243/EMED_JOUR_1988_017_008_02
7.
Lochmuller
,
E. M.
,
Eckstein
,
F.
,
Kaiser
,
D.
,
Zeller
,
J. B.
,
Landgraf
,
J.
,
Putz
,
R.
, and
Steldinger
,
R.
,
1998
, “
Prediction of Vertebral Failure Loads From Spinal and Femoral Dual-Energy X-Ray Absorptiometry, and Calcaneal Ultrasound: An In Situ Analysis With Intact Soft Tissues
,”
Bone
,
23
(
5
), pp.
417
424
.10.1016/S8756-3282(98)00127-6
8.
Donnelly
,
E.
,
Lane
,
J. M.
, and
Boskey
,
A. L.
,
2014
, “
Research Perspectives: The 2013 AAOS/ORS Research Symposium on Bone Quality and Fracture Prevention
,”
J. Orthop. Res.
,
32
(
7
), pp.
855
864
.10.1002/jor.22626
9.
Gourion-Arsiquaud
,
S.
,
Faibish
,
D.
,
Myers
,
E.
,
Spevak
,
L.
,
Compston
,
J.
,
Hodsman
,
A.
,
Shane
,
E.
,
Recker
,
R. R.
,
Boskey
,
E. R.
, and
Boskey
,
A. L.
,
2009
, “
Use of FTIR Spectroscopic Imaging to Identify Parameters Associated With Fragility Fracture
,”
J. Bone Miner. Res.
,
24
(
9
), pp.
1565
1571
.10.1359/jbmr.090414
10.
Tai
,
K.
,
Dao
,
M.
,
Suresh
,
S.
,
Palazoglu
,
A.
, and
Ortiz
,
C.
,
2007
, “
Nanoscale Heterogeneity Promotes Energy Dissipation in Bone
,”
Nat. Mater.
,
6
(
6
), pp.
454
462
.10.1038/nmat1911
11.
Ritchie
,
R. O.
,
2011
, “
The Conflicts Between Strength and Toughness
,”
Nat. Mater.
,
10
(
11
), pp.
817
822
.10.1038/nmat3115
12.
Gourion-Arsiquaud
,
S.
,
Lukashova
,
L.
,
Power
,
J.
,
Loveridge
,
N.
,
Reeve
,
J.
, and
Boskey
,
A. L.
,
2013
, “
Fourier Transform Infrared Imaging of Femoral Neck Bone: Reduced Heterogeneity of Mineral-to-Matrix and Carbonate-to-Phosphate and More Variable Crystallinity in Treatment-Naive Fracture Cases Compared With Fracture-Free Controls
,”
J. Bone Miner. Res.
,
28
(
1
), pp.
150
161
.10.1002/jbmr.1724
13.
Boskey
,
A. L.
,
Dicarlo
,
E.
,
Paschalis
,
E.
,
West
,
P.
, and
Mendelsohn
,
R.
,
2005
, “
Comparison of Mineral Quality and Quantity in Iliac Crest Biopsies From High- and Low-Turnover Osteoporosis: An FT-IR Microspectroscopic Investigation
,”
Osteoporos. Int.
,
16
(
12
), pp.
2031
2038
.10.1007/s00198-005-1992-3
14.
Roschger
,
P.
,
Rinnerthaler
,
S.
,
Yates
,
J.
,
Rodan
,
G. A.
,
Fratzl
,
P.
, and
Klaushofer
,
K.
,
2001
, “
Alendronate Increases Degree and Uniformity of Mineralization in Cancellous Bone and Decreases the Porosity in Cortical Bone of Osteoporotic Women
,”
Bone
,
29
(
2
), pp.
185
191
.10.1016/S8756-3282(01)00485-9
15.
Roschger
,
P.
,
Lombardi
,
A.
,
Misof
,
B. M.
,
Maier
,
G.
,
Fratzl-Zelman
,
N.
,
Fratzl
,
P.
, and
Klaushofer
,
K.
,
2009
, “
Mineralization Density Distribution of Postmenopausal Osteoporotic Bone is Restored to Normal After Long-Term Alendronate Treatment: QBEI and SSAXS Data From the Fracture Intervention Trial Long-Term Extension (Flex)
,”
J. Bone Miner. Res.
,
25
(
1
), pp.
48
55
.10.1359/jbmr.090702
16.
Van Der Linden
,
J. C.
,
Birkenhager-Frenkel
,
D. H.
,
Verhaar
,
J. A.
, and
Weinans
,
H.
,
2001
, “
Trabecular Bone's Mechanical Properties Are Affected by Its Non-Uniform Mineral Distribution
,”
J. Biomech.
,
34
(
12
), pp.
1573
1580
.10.1016/S0021-9290(01)00146-4
17.
Jaasma
,
M. J.
,
Bayraktar
,
H. H.
,
Niebur
,
G. L.
, and
Keaveny
,
T. M.
,
2002
, “
Biomechanical Effects of Intraspecimen Variations in Tissue Modulus for Trabecular Bone
,”
J. Biomech.
,
35
(
2
), pp.
237
246
.10.1016/S0021-9290(01)00193-2
18.
Bourne
,
B. C.
, and
Van Der Meulen
,
M. C.
,
2004
, “
Finite Element Models Predict Cancellous Apparent Modulus When Tissue Modulus Is Scaled From Specimen CT-Attenuation
,”
J. Biomech.
,
37
(
5
), pp.
613
621
.10.1016/j.jbiomech.2003.10.002
19.
Tai
,
K.
,
Qi
,
H. J.
, and
Ortiz
,
C.
,
2005
, “
Effect of Mineral Content on the Nanoindentation Properties and Nanoscale Deformation Mechanisms of Bovine Tibial Cortical Bone
,”
J. Mater. Sci. Mater. Med.
,
16
(
10
), pp.
947
959
.10.1007/s10856-005-4429-9
20.
Fratzl
,
P.
,
Gupta
,
H. S.
,
Fischer
,
F. D.
, and
Kolednik
,
O.
,
2007
, “
Hindered Crack Propagation in Materials With Periodically Varying Young's Modulus–Lessons From Biological Materials
,”
Adv. Mater.
,
19
(
18
), pp.
2657
2661
.10.1002/adma.200602394
21.
Nalla
,
R. K.
,
Stolken
,
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
.10.1016/j.jbiomech.2004.07.010
22.
Augat
,
P.
, and
Schorlemmer
,
S.
,
2006
, “
The Role of Cortical Bone and Its Microstructure in Bone Strength
,”
Age Ageing,
35
(
Suppl 2
), pp.
ii27
ii31
.10.1093/ageing/afl081
23.
Rho
,
J. Y.
,
Kuhn-Spearing
,
L.
, and
Zioupos
,
P.
,
1998
, “
Mechanical Properties and the Hierarchical Structure of Bone
,”
Med. Eng. Phys.
,
20
(
2
), pp.
92
102
.10.1016/S1350-4533(98)00007-1
24.
Dempster
,
D. W.
,
2000
, “
The Contribution of Trabecular Architecture to Cancellous Bone Quality
,”
J. Bone Miner. Res.
,
15
(
1
), pp.
20
23
.10.1359/jbmr.2000.15.1.20
25.
Keaveny
,
T. M.
,
Morgan
,
E. F.
,
Niebur
,
G. L.
, and
Yeh
,
O. C.
,
2001
, “
Biomechanics of Trabecular Bone
,”
Annu. Rev. Biomed. Eng.
,
3
(1), pp.
307
333
.10.1146/annurev.bioeng.3.1.307
26.
Zysset
,
P. K.
,
2003
, “
A Review of Morphology-Elasticity Relationships in Human Trabecular Bone: Theories and Experiments
,”
J. Biomech.
,
36
(
10
), pp.
1469
1485
.10.1016/S0021-9290(03)00128-3
27.
Rho
,
J. Y.
,
Tsui
,
T. Y.
, and
Pharr
,
G. M.
,
1997
, “
Elastic Properties of Human Cortical and Trabecular Lamellar Bone Measured by Nanoindentation
,”
Biomaterials
,
18
(
20
), pp.
1325
1330
.10.1016/S0142-9612(97)00073-2
28.
Rho
,
J. Y.
,
Zioupos
,
P.
,
Currey
,
J. D.
, and
Pharr
,
G. M.
,
1999
, “
Variations in the Individual Thick Lamellar Properties Within Osteons by Nanoindentation
,”
Bone
,
25
(
3
), pp.
295
300
.10.1016/S8756-3282(99)00163-5
29.
Donnelly
,
E.
,
Williams
,
R. W.
,
Downs
,
S. A.
,
Dickinson
,
M. E.
,
Baker
,
S. P.
, and
van der Meulen
,
M. C. H.
,
2006
, “
Quasistatic and Dynamic Nanomechanical Properties of Cancellous Bone Tissue Relate to Collagen Content and Organization
,”
J. Mater. Res.
,
21
(
8
), pp.
2106
2117
.10.1557/jmr.2006.0259
30.
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 of the Human Femur
,”
J. Biomech.
,
32
, pp.
1005
1012
.10.1016/S0021-9290(99)00111-6
31.
Jepsen
,
K. J.
, and
Schlecht
,
S. H.
,
2014
, “
Biomechanical Mechanisms: Resolving the Apparent Conundrum of Why Individuals With Type II Diabetes Show Increased Fracture Incidence Despite Having Normal Bmd
,”
J. Bone Miner. Res.
,
29
(
4
), pp.
784
786
.10.1002/jbmr.2189
32.
Hansma
,
P.
,
Turner
,
P.
,
Drake
,
B.
,
Yurtsev
,
E.
,
Proctor
,
A.
,
Mathews
,
P.
,
Lulejian
,
J.
,
Randall
,
C.
,
Adams
,
J.
,
Jungmann
,
R.
,
Garza-De-Leon
,
F.
,
Fantner
,
G.
,
Mkrtchyan
,
H.
,
Pontin
,
M.
,
Weaver
,
A.
,
Brown
,
M. B.
,
Sahar
,
N.
,
Rossello
,
R.
, and
Kohn
,
D.
,
2008
, “
The Bone Diagnostic Instrument II: Indentation Distance Increase
,”
Rev. Sci. Instrum.
,
79
(
6
), p.
064303
.10.1063/1.2937199
33.
Choi
,
K.
,
Kuhn
,
J. L.
,
Ciarelli
,
M. J.
, and
Goldstein
,
S. A.
,
1990
, “
The Elastic Moduli of Human Subchondral, Trabecular, and Cortical Bone Tissue and the Size-Dependency of Cortical Bone Modulus
,”
J. Biomech.
,
23
(
11
), pp.
1103
1113
.10.1016/0021-9290(90)90003-L
34.
Kuhn
,
L. T.
,
Grynpas
,
M. D.
,
Rey
,
C. C.
,
Wu
,
Y.
,
Ackerman
,
J. L.
, and
Glimcher
,
M. J.
,
2008
, “
A Comparison of the Physical and Chemical Differences Between Cancellous and Cortical Bovine Bone Mineral at Two Ages
,”
Calcif. Tissue Int.
,
83
(
2
), pp.
146
154
.10.1007/s00223-008-9164-z
35.
Tseng
,
K. F.
,
Bonadio
,
J. F.
,
Stewart
,
T. A.
,
Baker
,
A. R.
, and
Goldstein
,
S. A.
,
1996
, “
Local Expression of Human Growth Hormone in Bone Results in Impaired Mechanical Integrity in the Skeletal Tissue of Transgenic Mice
,”
J. Orthop. Res.
,
14
(
4
), pp.
598
604
.10.1002/jor.1100140414
36.
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
37.
Boskey
,
A.
, and
Mendelsohn
,
R.
,
2005
, “
Infrared Analysis of Bone in Health and Disease
,”
J. Biomed. Opt.
,
10
(
3
), p.
031102
.10.1117/1.1922927
38.
Carden
,
A.
, and
Morris
,
M. D.
,
2000
, “
Application of Vibrational Spectroscopy to the Study of Mineralized Tissues (Review)
,”
J. Biomed. Opt.
,
5
(
3
), pp.
259
268
.10.1117/1.429994
39.
Judex
,
S.
,
Boyd
,
S.
,
Qin
,
Y. X.
,
Miller
,
L.
,
Muller
,
R.
, and
Rubin
,
C.
,
2003
, “
Combining High-Resolution Micro-Computed Tomography With Material Composition to Define the Quality of Bone Tissue
,”
Curr. Osteoporos Rep.
,
1
(
1
), pp.
11
19
.10.1007/s11914-003-0003-x
40.
Donnelly
,
E.
,
2011
, “
Methods for Assessing Bone Quality: A Review
,”
Clin. Orthop. Relat. Res.
,
469
(
8
), pp.
2128
2138
.10.1007/s11999-010-1702-0
41.
Ciarelli
,
T. E.
,
Tjhia
,
C.
,
Rao
,
D. S.
,
Qiu
,
S.
,
Parfitt
,
A. M.
, and
Fyhrie
,
D. P.
,
2009
, “
Trabecular Packet-Level Lamellar Density Patterns Differ by Fracture Status and Bone Formation Rate in White Females
,”
Bone
,
45
(
5
), pp.
903
908
.10.1016/j.bone.2009.07.002
42.
Wang
,
Z. X.
, and
Donnelly
,
E.
, “
Altered Heterogeneity of Tissue Mineral and Collagen Properties in Perimenopausal Women With Fragility Fractures
,” (in review).
43.
Bousson
,
V.
,
Bergot
,
C.
,
Wu
,
Y.
,
Jolivet
,
E.
,
Zhou
,
L. Q.
, and
Laredo
,
J. D.
,
2011
, “
Greater Tissue Mineralization Heterogeneity in Femoral Neck Cortex From Hip-Fractured Females Than Controls. A Microradiographic Study
,”
Bone
,
48
(
6
), pp.
1252
1259
.10.1016/j.bone.2011.03.673
44.
Tamminen
,
I. S.
,
Misof
,
B. M.
,
Roschger
,
P.
,
Mayranpaa
,
M. K.
,
Turunen
,
M. J.
,
Isaksson
,
H.
,
Kroger
,
H.
,
Makitie
,
O.
, and
Klaushofer
,
K.
,
2014
, “
Increased Heterogeneity of Bone Matrix Mineralization in Pediatric Patients Prone to Fractures: A Biopsy Study
,”
J. Bone Miner. Res.
,
29
(
5
), pp.
1110
1117
.10.1002/jbmr.2124
45.
Fratzl-Zelman
,
N.
,
Roschger
,
P.
,
Misof
,
B. M.
,
Pfeffer
,
S.
,
Glorieux
,
F. H.
,
Klaushofer
,
K.
, and
Rauch
,
F.
,
2009
, “
Normative Data on Mineralization Density Distribution in Iliac Bone Biopsies of Children, Adolescents and Young Adults
,”
Bone
,
44
(
6
), pp.
1043
1048
.10.1016/j.bone.2009.02.021
46.
Paschalis
,
E. P.
,
Betts
,
F.
,
Dicarlo
,
E.
,
Mendelsohn
,
R.
, and
Boskey
,
A. L.
,
1997
, “
FTIR Microspectroscopic Analysis of Human Iliac Crest Biopsies From Untreated Osteoporotic Bone
,”
Calcif. Tissue Int.
,
61
(
6
), pp.
487
492
.10.1007/s002239900372
47.
Boskey
,
A. L.
, and
Mendelsohn
,
R.
,
2005
, “
Infrared Spectroscopic Characterization of Mineralized Tissues
,”
Vib. Spectrosc.
,
38
(
1–2
), pp.
107
114
.10.1016/j.vibspec.2005.02.015
48.
Tjhia
,
C. K.
,
Odvina
,
C. V.
,
Rao
,
D. S.
,
Stover
,
S. M.
,
Wang
,
X.
, and
Fyhrie
,
D. P.
,
2011
, “
Mechanical Property and Tissue Mineral Density Differences Among Severely Suppressed Bone Turnover (Ssbt) Patients, Osteoporotic Patients, and Normal Subjects
,”
Bone
,
49
(
6
), pp.
1279
1289
.10.1016/j.bone.2011.09.042
49.
Busse
,
B.
,
Hahn
,
M.
,
Soltau
,
M.
,
Zustin
,
J.
,
Puschel
,
K.
,
Duda
,
G. N.
, and
Amling
,
M.
,
2009
, “
Increased Calcium Content and Inhomogeneity of Mineralization Render Bone Toughness in Osteoporosis: Mineralization, Morphology and Biomechanics of Human Single Trabeculae
,”
Bone
,
45
(
6
), pp.
1034
1043
.10.1016/j.bone.2009.08.002
50.
Nyman
,
J. S.
,
Roy
,
A.
,
Shen
,
X.
,
Acuna
,
R. L.
,
Tyler
,
J. H.
, and
Wang
,
X.
,
2006
, “
The Influence of Water Removal on the Strength and Toughness of Cortical Bone
,”
J. Biomech.
,
39
(
5
), pp.
931
938
.10.1016/j.jbiomech.2005.01.012
51.
Sedlin
,
E. D.
, and
Hirsch
,
C.
,
1966
, “
Factors Affecting the Determination of the Physical Properties of Femoral Cortical Bone
,”
Acta. Orthop. Scand.
,
37
(
1
), pp.
29
48
.10.3109/17453676608989401
52.
Gourion-Arsiquaud
,
S.
,
Allen
,
M. R.
,
Burr
,
D. B.
,
Vashishth
,
D.
,
Tang
,
S. Y.
, and
Boskey
,
A. L.
,
2010
, “
Bisphosphonate Treatment Modifies Canine Bone Mineral and Matrix Properties and Their Heterogeneity
,”
Bone
,
46
(
3
), pp.
666
672
.10.1016/j.bone.2009.11.011
53.
Donnelly
,
E.
,
Meredith
,
D. S.
,
Nguyen
,
J. T.
,
Gladnick
,
B. P.
,
Rebolledo
,
B. J.
,
Shaffer
,
A. D.
,
Lorich
,
D. G.
,
Lane
,
J. M.
, and
Boskey
,
A. L.
,
2012
, “
Reduced Cortical Bone Compositional Heterogeneity With Bisphosphonate Treatment in Postmenopausal Women With Intertrochanteric and Subtrochanteric Fractures
,”
J. Bone Miner. Res.
,
27
(
3
), pp.
672
678
.10.1002/jbmr.560
54.
Launey
,
M. E.
,
Buehler
,
M. J.
, and
Ritchie
,
R. O.
,
2010
, “
On the Mechanistic Origins of Toughness in Bone
,”
Annu. Rev. Mater. Res.
,
40
(1), pp.
25
53
.10.1146/annurev-matsci-070909-104427
55.
Wang
,
X.
, and
Puram
,
S.
,
2004
, “
The Toughness of Cortical Bone and Its Relationship With Age
,”
Ann. Biomed. Eng.
,
32
(
1
), pp.
123
135
.10.1023/B:ABME.0000007797.92559.5e
56.
Ciarelli
,
T. E.
,
Fyhrie
,
D. P.
, and
Parfitt
,
A. M.
,
2003
, “
Effects of Vertebral Bone Fragility and Bone Formation Rate on the Mineralization Levels of Cancellous Bone From White Females
,”
Bone
,
32
(
3
), pp.
311
315
.10.1016/S8756-3282(02)00975-4
57.
Renders
,
G. A.
,
Mulder
,
L.
,
Van Ruijven
,
L. J.
, and
Van Eijden
,
T. M.
,
2006
, “
Degree and Distribution of Mineralization in the Human Mandibular Condyle
,”
Calcif. Tissue Int.
,
79
(
3
), pp.
190
196
.10.1007/s00223-006-0015-5
58.
Mulder
,
L.
,
Koolstra
,
J. H.
,
De Jonge
,
H. W.
, and
Van Eijden
,
T. M.
,
2006
, “
Architecture and Mineralization of Developing Cortical and Trabecular Bone of the Mandible
,”
Anat. Embryol. (Berl)
,
211
(
1
), pp.
71
78
.10.1007/s00429-005-0054-0
59.
Smith
,
L. J.
,
Schirer
,
J. P.
, and
Fazzalari
,
N. L.
,
2010
, “
The Role of Mineral Content in Determining the Micromechanical Properties of Discrete Trabecular Bone Remodeling Packets
,”
J. Biomech.
,
43
(
16
), pp.
3144
3149
.10.1016/j.jbiomech.2010.07.038
60.
Paschalis
,
E. P.
,
Betts
,
F.
,
Dicarlo
,
E.
,
Mendelsohn
,
R.
, and
Boskey
,
A. L.
,
1997
, “
FTIR Microspectroscopic Analysis of Normal Human Cortical and Trabecular Bone
,”
Calcif. Tissue Int.
,
61
(
6
), pp.
480
486
.10.1007/s002239900371
61.
Fyhrie
,
D. P.
, and
Schaffler
,
M. B.
,
1994
, “
Failure Mechanisms in Human Vertebral Cancellous Bone
,”
Bone
,
15
(
1
), pp.
105
109
.10.1016/8756-3282(94)90900-8
62.
Mulder
,
L.
,
Koolstra
,
J. H.
,
Den Toonder
,
J. M.
, and
Van Eijden
,
T. M.
,
2007
, “
Intratrabecular Distribution of Tissue Stiffness and Mineralization in Developing Trabecular Bone
,”
Bone
,
41
(
2
), pp.
256
265
.10.1016/j.bone.2007.04.188
63.
Skedros
,
J. G.
,
Knight
,
A. N.
,
Farnsworth
,
R. W.
, and
Bloebaum
,
R. D.
,
2012
, “
Do Regional Modifications in Tissue Mineral Content and Microscopic Mineralization Heterogeneity Adapt Trabecular Bone Tracts for Habitual Bending? Analysis in the Context of Trabecular Architecture of Deer Calcanei
,”
J. Anat.
,
220
(
3
), pp.
242
255
.10.1111/j.1469-7580.2011.01470.x
64.
Lotz
,
J. C.
,
Cheal
,
E. J.
, and
Hayes
,
W. C.
,
1995
, “
Stress Distributions Within the Proximal Femur During Gait and Falls: Implications for Osteoporotic Fracture
,”
Osteoporos. Int.
,
5
(
4
), pp.
252
261
.10.1007/BF01774015
65.
Gao
,
H.
,
Ji
,
B.
,
Jager
,
I. L.
,
Arzt
,
E.
, and
Fratzl
,
P.
,
2003
, “
Materials Become Insensitive to Flaws at Nanoscale: Lessons From Nature
,”
Proc. Natl. Acad. Sci. U.S.A.
,
100
(
10
), pp.
5597
5600
.10.1073/pnas.0631609100
66.
Bonderer
,
L. J.
,
Studart
,
A. R.
, and
Gauckler
,
L. J.
,
2008
, “
Bioinspired Design and Assembly of Platelet Reinforced Polymer Films
,”
Science
,
319
(
5866
), pp.
1069
1073
.10.1126/science.1148726
67.
Yao
,
H. M.
,
Dao
,
M.
,
Carnelli
,
D.
,
Tai
,
K. S.
, and
Ortiz
,
C.
,
2011
, “
Size-Dependent Heterogeneity Benefits the Mechanical Performance of Bone
,”
J. Mech. Phys. Solids
,
59
(
1
), pp.
64
74
.10.1016/j.jmps.2010.09.012
68.
Wang
,
X.
,
Zauel
,
R. R.
,
Rao
,
D. S.
, and
Fyhrie
,
D. P.
,
2008
, “
Cancellous Bone Lamellae Strongly Affect Microcrack Propagation and Apparent Mechanical Properties: Separation of Patients With Osteoporotic Fracture From Normal Controls Using a 2D Nonlinear Finite Element Method (Biomechanical Stereology)
,”
Bone
,
42
(
6
), pp.
1184
1192
.10.1016/j.bone.2008.01.022
69.
Mcnamara
,
L. M.
,
Van Der Linden
,
J. C.
,
Weinans
,
H.
, and
Prendergast
,
P. J.
,
2006
, “
Stress-Concentrating Effect of Resorption Lacunae in Trabecular Bone
,”
J. Biomech.
,
39
(
4
), pp.
734
741
.10.1016/j.jbiomech.2004.12.027
70.
Smit
,
T. H.
, and
Burger
,
E. H.
,
2000
, “
Is BMU-Coupling a Strain-Regulated Phenomenon? A Finite Element Analysis
,”
J. Bone Miner. Res.
,
15
(
2
), pp.
301
307
.10.1359/jbmr.2000.15.2.301
71.
Slyfield
,
C. R.
,
Tkachenko
,
E. V.
,
Fischer
,
S. E.
,
Ehlert
,
K. M.
,
Yi
,
I. H.
,
Jekir
,
M. G.
,
O'brien
,
R. G.
,
Keaveny
,
T. M.
, and
Hernandez
,
C. J.
,
2012
, “
Mechanical Failure Begins Preferentially Near Resorption Cavities in Human Vertebral Cancellous Bone Under Compression
,”
Bone
,
50
(
6
), pp.
1281
1287
.10.1016/j.bone.2012.02.636
72.
Hernandez
,
C. J.
,
Gupta
,
A.
, and
Keaveny
,
T. M.
,
2006
, “
A Biomechanical Analysis of the Effects of Resorption Cavities on Cancellous Bone Strength
,”
J. Bone Miner. Res.
,
21
(
8
), pp.
1248
1255
.10.1359/jbmr.060514
73.
Van Rietbergen
,
B.
,
Weinans
,
H.
,
Huiskes
,
R.
, and
Odgaard
,
A.
,
1995
, “
A New Method to Determine Trabecular Bone Elastic Properties and Loading Using Micromechanical Finite-Element Models
,”
J. Biomech.
,
28
(
1
), pp.
69
81
.10.1016/0021-9290(95)80008-5
74.
Gross
,
T.
,
Pahr
,
D. H.
,
Peyrin
,
F.
, and
Zysset
,
P. K.
,
2012
, “
Mineral Heterogeneity Has a Minor Influence on the Apparent Elastic Properties of Human Cancellous Bone: A SRμCT-Based Finite Element Study
,”
Comput. Methods Biomech. Biomed. Eng.
,
15
(
11
), pp.
1137
1144
.10.1080/10255842.2011.581236
75.
Renders
,
G. A.
,
Mulder
,
L.
,
Langenbach
,
G. E.
,
Van Ruijven
,
L. J.
, and
Van Eijden
,
T. M.
,
2008
, “
Biomechanical Effect of Mineral Heterogeneity in Trabecular Bone
,”
J. Biomech.
,
41
(
13
), pp.
2793
2798
.10.1016/j.jbiomech.2008.07.009
76.
Renders
,
G. A.
,
Mulder
,
L.
,
Van Ruijven
,
L. J.
,
Langenbach
,
G. E.
, and
Van Eijden
,
T. M.
,
2011
, “
Mineral Heterogeneity Affects Predictions of Intratrabecular Stress and Strain
,”
J. Biomech.
,
44
(
3
), pp.
402
407
.10.1016/j.jbiomech.2010.10.004
77.
Chevalier
,
Y.
,
Pahr
,
D.
,
Allmer
,
H.
,
Charlebois
,
M.
, and
Zysset
,
P.
,
2007
, “
Validation of a Voxel-Based Fe Method for Prediction of the Uniaxial Apparent Modulus of Human Trabecular Bone Using Macroscopic Mechanical Tests and Nanoindentation
,”
J. Biomech.
,
40
(
15
), pp.
3333
3340
.10.1016/j.jbiomech.2007.05.004
78.
Currey
,
J. D.
,
2003
, “
How Well Are Bones Designed to Resist Fracture?
,”
J. Bone Miner. Res.
,
18
(
4
), pp.
591
598
.10.1359/jbmr.2003.18.4.591
79.
Yang
,
Q. D.
,
Cox
,
B. N.
,
Nalla
,
R. K.
, and
Ritchie
,
R. O.
,
2006
, “
Fracture Length Scales in Human Cortical Bone: The Necessity of Nonlinear Fracture Models
,”
Biomaterials
,
27
(
9
), pp.
2095
2113
.10.1016/j.biomaterials.2005.09.040
80.
Buchanan
,
D.
, and
Ural
,
A.
,
2010
, “
Finite Element Modeling of the Influence of Hand Position and Bone Properties on the Colles' Fracture Load During a Fall
,”
ASME J. Biomech. Eng.
,
132
(
8
), p.
081007
.10.1115/1.4001681
81.
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
.10.1016/j.jbiomech.2005.10.018
82.
Ural
,
A.
,
2009
, “
Prediction of Colles' Fracture Load in Human Radius Using Cohesive Finite Element Modeling
,”
J. Biomech.
,
42
(
1
), pp.
22
28
.10.1016/j.jbiomech.2008.10.011
83.
Ural
,
A.
, and
Mischinski
,
S.
,
2013
, “
Multiscale Modeling of Bone Fracture Using Cohesive Finite Elements
,”
Eng. Fract. Mech.
,
103
(1), pp.
141
152
.10.1016/j.engfracmech.2012.05.008
84.
Bruno
,
P.
,
Waldron
,
J.
, and
Ural
,
A.
,
2014
, “
Influence of Reduced Compositional Heterogeneity on Fracture Resistance in Cortical Bone
,”
Trans. Orthop. Res. Soc.
,
39
, p.
1496
.
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