This study investigated the effects of intraspecimen variations in tissue mineral density (TMD) on the apparent-level stiffness of human trabecular bone. High-resolution finite element (FE) models were created for each of 12 human trabecular bone specimens, using both microcomputed tomography (μCT) and “gold-standard” synchrotron radiation μCT (SRμCT) data. Our results confirm that incorporating TMD spatial variation reduces the calculated apparent stiffness compared to homogeneous TMD models. This effect exists for both μCT- and SRμCT-based FE models, but is exaggerated in μCT-based models. This study provides a direct comparison of μCT to SRμCT data and is thereby able to conclude that the influence of including TMD heterogeneity is overestimated in μCT-based models.

References

References
1.
Bevill
,
G.
,
Eswaran
,
S. K.
,
Farahmand
,
F.
, and
Keaveny
,
T. M.
,
2009
, “
The Influence of Boundary Conditions and Loading Mode on High-Resolution Finite Element-Computed Trabecular Tissue Properties
,”
Bone
,
44
(
4
), pp.
573
578
.10.1016/j.bone.2008.11.015
2.
Kabel
,
J.
,
van Rietbergen
,
B.
,
Dalstra
,
M.
,
Odgaard
,
A.
, and
Huiskes
,
R.
,
1999
, “
The Role of an Effective Isotropic Tissue Modulus in the Elastic Properties of Cancellous Bone
,”
J. Biomech.
,
32
(
7
) pp.
673
680
.10.1016/S0021-9290(99)00045-7
3.
Ladd
,
A. J.
,
Kinney
,
J. H.
,
Haupt
,
D. L.
, and
Goldstein
,
S. A.
,
1998
, “
Finite-Element Modeling of Trabecular Bone: Comparison With Mechanical Testing and Determination of Tissue Modulus
,”
J. Orthop. Res.
,
16
(
5
), pp.
622
8
.10.1002/jor.1100160516
4.
Ulrich
,
D.
,
Hildebrand
,
T.
,
Van Rietbergen
,
B.
,
Müller
,
R.
, and
Rüegsegger
,
P.
,
1997
, “
The Quality of Trabecular Bone Evaluated With Micro-Computed Tomography, FEA, and Mechanical Testing
,”
Stud. Health Technol. Inf.
,
40
, pp.
97
112
.10.3233/978-1-60750-884-7-97
5.
Van Rietbergen
,
B.
,
Weinans
,
H.
,
Huiskes
,
R.
, and
Odgaard
,
A. A.
,
1995
, “
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
6.
Boivin
,
G.
, and
Meunier
,
P. J.
,
2002
, “
Changes in Bone Remodeling Rate Influence the Degree of Mineralization of Bone
,”
Connect. Tissue Res.
,
43
(
2–3
), pp.
535
537
.10.1080/03008200290000934
7.
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
8.
Misof
,
B. M.
,
Roschger
,
P.
,
Cosman
,
F.
,
Kurland
,
E. S.
,
Tesch
,
W.
,
Messmer
,
P.
,
Dempster
,
D. W.
,
Nieves
,
J.
,
Shane
,
E.
,
Fratzl
,
P.
,
Klaushofer
,
K.
,
Bilezikian
,
J.
, and
Lindsay
,
R.
,
2003
, “
Effects of Intermittent Parathyroid Hormone Administration on Bone Mineralization Density in Iliac Crest Biopsies From Patients With Osteoporosis: A Paired Study Before and After Treatment
,”
J. Clin. Endocrinol. Metab.
,
88
(
3
), pp.
1150
1156
.10.1210/jc.2002-021988
9.
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
10.
Yao
,
W.
,
Cheng
,
Z.
,
Koester
,
K. J.
,
Ager
,
J. W.
,
Balooch
,
M.
,
Pham
,
A.
,
Chefo
,
S.
,
Busse
,
C.
,
Ritchie
,
R. O.
, and
Lane
,
N. E.
,
2007
, “
The Degree of Bone Mineralization is Maintained With Single Intravenous Bisphosphonates in Aged Estrogen-Deficient Rats and Is a Strong Predictor of Bone Strength
,”
Bone
,
41
(
5
), pp.
804
812
.10.1016/j.bone.2007.06.021
11.
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
12.
Bouxsein
,
M. L.
,
2003
, “
Bone Quality: Where Do We Go From Here?
,”
Osteoporosis Int.
,
14
(
5
), pp.
S118
S127
.10.1007/s00198-003-1489-x
13.
Burr
,
D. B.
,
2004
, “
Bone Quality: Understanding What Matters
,”
J. Musculoskeletal Neuronal Interact.
,
4
(
2
), pp.
184
186
.
14.
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
15.
Mulder
,
L.
,
van Ruijven
,
L. J.
,
Koolstra
,
J. H.
, and
van Eijden
,
T. M.
,
2007
, “
Biomechanical Consequences of Developmental Changes in Trabecular Architecture and Mineralization of the Pig Mandibular Condyle
,”
J. Biomech.
,
40
(
7
), pp.
1575
1582
.10.1016/j.jbiomech.2006.07.030
16.
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
17.
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
18.
Jaasma
,
M. J.
,
Bayraktar
,
H. H.
,
Niebur
,
G. L.
, and
Keaveny
,
T. M.
,
2001
, “
The Effects of Intraspecimen Variations in Tissue Modulus on the Apparent Mechanical Properties of Trabecular Bone
,”
Transactions of the Annual Meeting—Orthopaedic Research Society
, San Francisco, p.
513
.
19.
Easley
,
S. K.
,
Jekir
,
M. G.
,
Burghardt
,
A. J.
,
Li
,
M.
, and
Keaveny
,
T. M.
,
2010
, “
Contribution of the Intra-Specimen Variations in Tissue Mineralization to PTH and Raloxifene-Induced Changes in Stiffness of Rat Vertebrae
,”
Bone
,
46
(
4
), pp.
1162
1169
.10.1016/j.bone.2009.12.009
20.
Kazakia
,
G. J.
,
Burghardt
,
A. J.
,
Cheung
,
S.
, and
Majumdar
,
S.
,
2008
, “
Assessment of Bone Tissue Mineralization by Conventional X-Ray Microcomputed Tomography: Comparison With Synchrotron Radiation Microcomputed Tomography and Ash Measurements
,”
Med. Phys.
,
35
(
5
), pp.
3170
3179
.10.1118/1.2924210
21.
Feldkamp
,
L. A.
,
Goldstein
,
S. A.
,
Parfitt
,
A. M.
,
Jesion
,
G.
, and
Kleerekoper
,
M.
,
1989
, “
The Direct Examination of Three-Dimensional Bone Architecture in vitro by Computed Tomography
,”
J. Bone Miner. Res.
,
4
(
1
), pp.
3
11
.10.1002/jbmr.5650040103
22.
Burghardt
,
A. J.
,
Kazakia
,
G. J.
,
Laib
,
A.
, and
Majumdar
,
S.
,
2008
, “
Quantitative Assessment of Bone Tissue Mineralization With Polychromatic Micro-Computed Tomography
,”
Calcif. Tissue Int.
,
83
(
2
), pp.
129
138
.10.1007/s00223-008-9158-x
23.
Jorgensen
,
S. M.
,
Demirkaya
,
O.
, and
Ritman
,
E. L.
,
1998
, “
Three-Dimensional Imaging of Vasculature and Parenchyma in Intact Rodent Organs With X-Ray Micro-CT
,”
Am. J. Physiol.
,
275
(3), pp.
H1103
H1114
.
24.
Ding
,
M.
,
Odgaard
,
A.
, and
Hvid
,
I.
,
1999
, “
Accuracy of Cancellous Bone Volume Fraction Measured by Micro-CT Scanning
,”
J. Biomech.
,
32
(
3
), pp.
323
326
.10.1016/S0021-9290(98)00176-6
25.
Goodenough
,
D.
,
Weaver
,
K.
,
Davis
,
D.
, and
LaFalce
,
S.
,
1982
, “
Volume Averaging Limitations of Computed Tomography
,”
Am. J. Roentgenol.
,
138
(
2
), pp.
313
316
.10.2214/ajr.138.2.313
26.
Adams
,
M. F.
,
Bayraktar
,
H. H.
,
Keaveny
,
T. M,
, and
Papadopoulos
,
P.
,
2004
, “
Ultrascalable Implicit Finite Element Analyses in Solid Mechanics With Over a Half a Billion Degrees of Freedom
,”
Proceeding of the ACM/IEEE High Performance Networking and Computing
, Nov. 6–12, p.
34
.10.1109/SC.2004.62
27.
Bevill
,
G.
, and
Keaveny
,
T. M.
,
2009
, “
Trabecular Bone Strength Predictions Using Finite Element Analysis of Micro-Scale Images at Limited Spatial Resolution
,”
Bone
,
44
(
4
), pp.
579
584
.10.1016/j.bone.2008.11.020
28.
Currey
,
J. D.
,
1988
, “
The Effect of Porosity and Mineral Content on the Young's Modulus of Elasticity of Compact Bone
,”
J. Biomech.
,
21
(
2
), pp.
131
139
.10.1016/0021-9290(88)90006-1
29.
Schaffler
,
M. B.
, and
Burr
,
D. B.
,
1988
, “
Stiffness of Compact Bone: Effects of Porosity and Density
,”
J. Biomech.
,
21
(
1
), pp.
13
16
.10.1016/0021-9290(88)90186-8
30.
Kaneko
,
T. S.
,
Pejcic
,
M. R.
,
Tehranzadeh
,
J.
, and
Keyak
,
J. H.
,
2003
, “
Relationships Between Material Properties and CT Scan Data of Cortical Bone With and Without Metastatic Lesions
,”
Med. Eng. Phys.
,
25
(
6
), pp.
445
454
.10.1016/S1350-4533(03)00030-4
31.
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 SRmuCT-Based Finite Element Study
,”
Comput. Methods Biomech. Biomed. Eng.
,
15
(
11
), pp.
1137
1144
.10.1080/10255842.2011.581236
32.
Fajardo
,
R. J.
,
Cory
,
E.
,
Patel
,
N. D.
,
Nazarian
,
A.
,
Laib
,
A.
,
Manoharan
,
R. K.
,
Schmitz
,
J. E.
,
Desilva
,
J. M.
,
Maclatchy
,
L. M.
,
Snyder
,
B. D,
, and
Bouxsein
,
M. L.
,
2008
, “
Specimen Size and Porosity Can Introduce Error Into μCT-Based Tissue Mineral Density Measurements
,”
Bone
,
44
(
1
), pp.
176
184
.10.1016/j.bone.2008.08.118
33.
Mulder
,
L.
,
Koolstra
,
J. H.
, and
Van Eijden
,
T. M.
, “
Accuracy of Microct in the Quantitative Determination of the Degree and Distribution of Mineralization in Developing Bone
,”
Acta Radiol.
,
45
(
7
), pp.
769
777
.10.1080/02841850410008171
34.
Nazarian
,
A.
,
Snyder
,
B. D.
,
Zurakowski
,
D.
, and
Muller
,
R.
,
2008
, “
Quantitative Micro-Computed Tomography: A Non-Invasive Method to Assess Equivalent Bone Mineral Density
,”
Bone
,
43
(
2
), pp.
302
311
.10.1016/j.bone.2008.04.009
35.
Nuzzo
,
S.
,
Peyrin
,
F.
,
Cloetens
,
P.
,
Baruchel
,
J.
, and
Boivin
,
G.
,
2002
, “
Quantification of the Degree of Mineralization of Bone in Three Dimensions Using Synchrotron Radiation Microtomography
,”
Med. Phys.
,
29
(
11
), pp.
2672
2681
.10.1118/1.1513161
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