Abstract

Cancellous bone is an anisotropic structure with architectural and mechanical properties that vary due to both skeletal site and disease state. This anisotropy means that, in order to accurately and consistently measure the mechanical properties of cancellous bone, experiments should be performed along the primary mechanical axis (PMA), that is, the orientation in which the mechanical properties are at their maximum value. Unfortunately, some degree of misalignment will always be present, and the magnitude of the resulting error is expected to be architecture dependent. The goal of this work is to quantify the dependence of the misalignment error, expressed in terms of change in apparent elastic modulus (ΔE), on both the bone volume fraction (BV/TV) and the degree of anisotropy (DA). Finite element method (FEM) models of bovine cancellous bone from five different skeletal sites were created at 5 deg and 20deg from the PMA determined for each region. An additional set of models was created using image dilation/erosion steps in order to control for BV/TV and better isolate the effect of DA. Misalignment error was found to increase with increasing DA and decreasing BV/TV. At 5deg misaligned from the PMA, error is relatively low (<5%) in all cases but increases to 8–24% error at 20deg. These results suggest that great care is needed to avoid introducing misalignment error into experimental studies, particularly when studying regions with high anisotropy and/or low bone volume fraction, such as vertebral or osteoporotic bone.

References

1.
Bailey
,
A. J.
,
Sims
,
T. J.
,
Ebbesen
,
E. N.
,
Mansell
,
J. P.
,
Thomsen
,
J. S.
, and
Mosekilde
,
L.
,
1999
, “
Age-Related Changes in the Biochemical Properties of Human Cancellous Bone Collagen: Relationship to Bone Strength
,”
Calcif. Tissue Int.
,
65
(
3
), pp.
203
210
.10.1007/s002239900683
2.
Ding
,
M.
,
Odgaard
,
A.
,
Linde
,
F.
, and
Hvid
,
I.
,
2002
, “
Age-Related Variations in the Microstructure of Human Tibial Cancellous Bone
,”
J. Orthop. Res.
,
20
(
3
), pp.
615
621
.10.1016/S0736-0266(01)00132-2
3.
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
4.
Hobatho
,
M. C.
,
Rho
,
J. Y.
, and
Ashman
,
R. B.
,
1997
, “
Anatomical Variation of Human Cancellous Bone Mechanical Properties In Vitro
,”
Stud. Health Technol. Inf.
,
40
, pp.
157
173
.10.3233/978-1-60750-884-7-157
5.
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
6.
Link
,
T. M.
,
Majumdar
,
S.
,
Augat
,
P.
,
Lin
,
J. C.
,
Newitt
,
D.
,
Lu
,
Y.
,
Lane
,
N. E.
, and
Genant
,
H. K.
,
1998
, “
In Vivo High Resolution MRI of the Calcaneus: Differences in Trabecular Structure in Osteoporosis Patients
,”
J. Bone Miner. Res.
,
13
(
7
), pp.
1175
1182
.10.1359/jbmr.1998.13.7.1175
7.
Gong
,
H.
,
Zhang
,
M.
,
Yeung
,
H. Y.
, and
Qin
,
L.
,
2005
, “
Regional Variations in Microstructural Properties of Vertebral Trabeculae With Aging
,”
J. Bone Miner. Metab.
,
23
(
2
), pp.
174
180
.10.1007/s00774-004-0557-4
8.
Keaveny
,
T. M.
,
Borchers
,
R. E.
,
Gibson
,
L. J.
, and
Hayes
,
W. C.
,
1993
, “
Theoretical Analysis of the Experimental Artifact in Trabecular Bone Compressive Modulus
,”
J. Biomech.
,
26
(
4–5
), pp.
599
607
.10.1016/0021-9290(93)90021-6
9.
Keaveny
,
T. M.
,
Guo
,
X.
,
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.
,
27
(
9
), pp.
1127
1136
.10.1016/0021-9290(94)90053-1
10.
Linde
,
F.
,
Hvid
,
I.
, and
Madsen
,
F.
,
1992
, “
The Effect of Specimen Geometry on the Mechanical Behaviour of Trabecular Bone Specimens
,”
J. Biomech.
,
25
(
4
), pp.
359
368
.10.1016/0021-9290(92)90255-Y
11.
Yan
,
Y. B.
,
Qi
,
W.
,
Wang
,
J.
,
Liu
,
L. F.
,
Teo
,
E. C.
,
Tianxia
,
Q.
,
Ba
,
J.
, and
Lei
,
W.
,
2011
, “
Relationship Between Architectural Parameters and Sample Volume of Human Cancellous Bone in Micro-CT Scanning
,”
Med. Eng. Phys.
,
33
(
6
), pp.
764
769
.10.1016/j.medengphy.2011.01.014
12.
Rho
,
J. Y.
, and
Pharr
,
G. M.
,
1999
, “
Effects of Drying on the Mechanical Properties of Bovine Femur Measured by Nanoindentation
,”
J. Mater. Sci. Mater. Med.
,
10
(
8
), pp.
485
488
.10.1023/A:1008901109705
13.
Öhman
,
C.
,
Baleani
,
M.
,
Perilli
,
E.
,
Dall'Ara
,
E.
,
Tassani
,
S.
,
Baruffaldi
,
F.
, and
Viceconti
,
M.
,
2007
, “
Mechanical Testing of Cancellous Bone From the Femoral Head: Experimental Errors Due to Off-Axis Measurements
,”
J. Biomech.
,
40
(
11
), pp.
2426
2433
.10.1016/j.jbiomech.2006.11.020
14.
Turner
,
C.
, and
Cowin
,
S.
,
1988
, “
Errors Induced by Off-Axis Measurement of the Elastic Properties of Bone
,”
ASME J. Biomech. Eng.
,
110
(
3
), pp.
213
215
.10.1115/1.3108433
15.
Wang
,
X.
,
Liu
,
X.
, and
Niebur
,
G. L.
,
2004
, “
Preparation of on-Axis Cylindrical Trabecular Bone Specimens Using Micro-CT Imaging
,”
ASME J. Biomech. Eng.
,
126
(
1
), pp.
122
125
.10.1115/1.1645866
16.
Odgaard
,
A.
,
Kabel
,
J.
,
van Rietbergen
,
B.
,
Dalstra
,
M.
, and
Huiskes
,
R.
,
1997
, “
Fabric and Elastic Principal Directions of Cancellous Bone Are Closely Related
,”
J. Biomech.
,
30
(
5
), pp.
487
495
.10.1016/S0021-9290(96)00177-7
17.
Odgaard
,
A.
,
1997
, “
Three-Dimensional Methods for Quantification of Cancellous Bone Architecture
,”
Bone
,
20
(
4
), pp.
315
328
.10.1016/S8756-3282(97)00007-0
18.
Hodgskinson
,
R.
, and
Currey
,
J.
,
1990
, “
The Effect of Variation in Structure on the Young's Modulus of Cancellous Bone: A Comparison of Human and Non-Human Material
,”
Proc. Inst. Mech. Eng., Part H
,
204
(
2
), pp.
115
121
.10.1243/PIME_PROC_1990_204_240_02
19.
Hodgskinson
,
R.
, and
Currey
,
J. D.
,
1993
, “
Separate Effects of Osteoporosis and Density on the Strength and Stiffness of Human Cancellous Bone
,”
Clin. Biomech.
,
8
(
5
), pp.
262
268
.10.1016/0268-0033(93)90036-H
20.
Nazarian
,
A.
,
Stauber
,
M.
,
Zurakowski
,
D.
,
Snyder
,
B. D.
, and
Müller
,
R.
,
2006
, “
The Interaction of Microstructure and Volume Fraction in Predicting Failure in Cancellous Bone
,”
Bone
,
39
(
6
), pp.
1196
1202
.10.1016/j.bone.2006.06.013
21.
Hernandez
,
C. J.
,
Beaupre
,
G. S.
,
Keller
,
T. S.
, and
Carter
,
D. R.
,
2001
, “
The Influence of Bone Volume Fraction and Ash Fraction on Bone Strength and Modulus
,”
Bone
,
29
(
1
), pp.
74
78
.10.1016/S8756-3282(01)00467-7
22.
Niebur
,
G.
,
Yuen
,
J.
,
Hsia
,
A.
, and
Keaveny
,
T.
,
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
23.
Hollister
,
S. J.
,
Brennan
,
J.
, and
Kikuchi
,
N.
,
1994
, “
A Homogenization Sampling Procedure for Calculating Trabecular Bone Effective Stiffness and Tissue Level Stress
,”
J. Biomech.
,
27
(
4
), pp.
433
444
.10.1016/0021-9290(94)90019-1
24.
Guldberg
,
R. E.
,
Hollister
,
S. J.
, and
Charras
,
G. T.
,
1998
, “
The Accuracy of Digital Image-Based Finite Element Models
,”
ASME J. Biomech. Eng.
,
120
(
2
), pp.
289
295
.10.1115/1.2798314
25.
Homminga
,
J.
,
Huiskes
,
R.
,
Van Rietbergen
,
B.
,
Rüegsegger
,
P.
, and
Weinans
,
H.
,
2001
, “
Introduction and Evaluation of a Gray-Value Voxel Conversion Technique
,”
J. Biomech.
,
34
(
4
), pp.
513
517
.10.1016/S0021-9290(00)00227-X
26.
Lievers
,
W.
,
Waldman
,
S.
, and
Pilkey
,
A.
,
2010
, “
Minimizing Specimen Length in Elastic Testing of End-Constrained Cancellous Bone
,”
J. Mech. Behav. Biomed. Mater.
,
3
(
1
), pp.
22
30
.10.1016/j.jmbbm.2009.02.001
27.
Ulrich
,
D.
,
van Rietbergen
,
B.
,
Weinans
,
H.
, and
Rüegsegger
,
P.
,
1998
, “
Finite Element Analysis of Trabecular Bone Structure: A Comparison of Image-Based Meshing Techniques
,”
J. Biomech.
,
31
(
12
), pp.
1187
1192
.10.1016/S0021-9290(98)00118-3
28.
Otsu
,
N.
,
1979
, “
A Threshold Selection Method From Gray-Level Histograms
,”
IEEE Trans. Syst. Man Cybern.
,
9
(
1
), pp.
62
66
.10.1109/TSMC.1979.4310076
29.
Odgaard
,
A.
, and
Gundersen
,
H.
,
1993
, “
Quantification of Connectivity in Cancellous Bone, With Special Emphasis on 3-D Reconstructions
,”
Bone
,
14
(
2
), pp.
173
182
.10.1016/8756-3282(93)90245-6
30.
Lievers
,
W.
,
Petryshyn
,
A.
,
Poljsak
,
A.
,
Waldman
,
S.
, and
Pilkey
,
A.
,
2010
, “
Specimen Diameter and “Side Artifacts” in Cancellous Bone Evaluated Using End-Constrained Elastic Tension
,”
Bone
,
47
(
2
), pp.
371
377
.10.1016/j.bone.2010.03.024
31.
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
32.
Keaveny
,
T. M.
,
Pinilla
,
T. P.
,
Crawford
,
R. P.
,
Kopperdahl
,
D. L.
, and
Lou
,
A.
,
1997
, “
Systematic and Random Errors in Compression Testing of Trabecular Bone
,”
J. Orthop. Res.
,
15
(
1
), pp.
101
110
.10.1002/jor.1100150115
33.
Whitehouse
,
W.
,
1974
, “
The Quantitative Morphology of Anisotropic Trabecular Bone
,”
J. Microsc.
,
101
(
2
), pp.
153
168
.10.1111/j.1365-2818.1974.tb03878.x
34.
Snyder
,
B.
,
Piazza
,
S.
,
Edwards
,
W.
, and
Hayes
,
W.
,
1993
, “
Role of Trabecular Morphology in the Etiology of Age-Related Vertebral Fractures
,”
Calcif. Tissue Int.
,
53
(
S1
), pp.
S14
S22
.10.1007/BF01673396
35.
Simmons
,
C. A.
, and
Hipp
,
J. A.
,
1997
, “
Method-Based Differences in the Automated Analysis of the Three-Dimensional Morphology of Trabecular Bone
,”
J. Bone Miner. Res.
,
12
(
6
), pp.
942
947
.10.1359/jbmr.1997.12.6.942
36.
Schindelin
,
J.
,
Arganda-Carreras
,
I.
,
Frise
,
E.
,
Kaynig
,
V.
,
Longair
,
M.
,
Pietzsch
,
T.
,
Preibisch
,
S.
,
Rueden
,
C.
,
Saalfeld
,
S.
,
Schmid
,
B.
,
Tinevez
,
J. Y.
,
White
,
D. J.
,
Hartenstein
,
V.
,
Eliceiri
,
K.
,
Tomancak
,
P.
, and
Cardona
,
A.
,
2012
, “
Fiji: An Open-Source Platform for Biological-Image Analysis
,”
Nat. Methods
,
9
(
7
), pp.
676
682
.10.1038/nmeth.2019
37.
Doube
,
M.
,
Kłosowski
,
M. M.
,
Arganda-Carreras
,
I.
,
Cordelières
,
F. P.
,
Dougherty
,
R. P.
,
Jackson
,
J. S.
,
Schmid
,
B.
,
Hutchinson
,
J. R.
, and
Shefelbine
,
S. J.
,
2010
, “
BoneJ: Free and Extensible Bone Image Analysis in ImageJ
,”
Bone
,
47
(
6
), pp.
1076
1079
.10.1016/j.bone.2010.08.023
38.
Müller
,
R.
,
Koller
,
B.
,
Hildebrand
,
T.
,
Laib
,
A.
,
Gianolini
,
S.
, and
Rüegsegger
,
P.
,
1996
, “
Resolution Dependency of Microstructural Properties of Cancellous Bone Based on Three-Dimensional Mu-Tomography
,”
Technol. Health Care
,
4
(
1
), pp.
113
119
.10.3233/THC-1996-4112
39.
Kamibayashi
,
L.
,
Wyss
,
U.
,
Cooke
,
T.
, and
Zee
,
B.
,
1995
, “
Changes in Mean Trabecular Orientation in the Medial Condyle of the Proximal Tibia in Osteoarthritis
,”
Calcif. Tissue Int.
,
57
(
1
), pp.
69
73
.10.1007/BF00299000
40.
Nikodem
,
A.
,
2012
, “
Correlations Between Structural and Mechanical Properties of Human Trabecular Femur Bone
,”
Acta Bioeng. Biomech.
,
14
(
2
), pp.
37
46
.10.5277/abb120205
41.
Li
,
B.
, and
Aspden
,
R. M.
,
1997
, “
Composition and Mechanical Properties of Cancellous Bone From the Femoral Head of Patients With Osteoporosis or Osteoarthritis
,”
J. Bone Miner. Res.
,
12
(
4
), pp.
641
651
.10.1359/jbmr.1997.12.4.641
42.
Ciarelli
,
T. E.
,
Fyhrie
,
D. P.
,
Schaffler
,
M. B.
, and
Goldstein
,
S. A.
,
2000
, “
Variations in Three-Dimensional Cancellous Bone Architecture of the Proximal Femur in Female Hip Fractures and in Controls
,”
J. Bone Miner. Res.
,
15
(
1
), pp.
32
40
.10.1359/jbmr.2000.15.1.32
43.
Mao
,
H.
,
Rumpler
,
R.
, and
Göransson
,
P.
,
2020
, “
An Inverse Method for Characterisation of the Static Elastic Hooke's Tensors of Solid Frame of Anisotropic Open-Cell Materials
,”
Int. J. Eng. Sci.
,
147
, p.
103198
.10.1016/j.ijengsci.2019.103198
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