The high-resolution peripheral quantitative computed tomography (HR-pQCT) provides unprecedented visualization of bone microstructure and the basis for constructing patient-specific microfinite element (μFE) models. Based on HR-pQCT images, we have developed a plate-and-rod μFE (PR μFE) method for whole bone segments using individual trabecula segmentation (ITS) and an adaptive cortical meshing technique. In contrast to the conventional voxel approach, the complex microarchitecture of the trabecular compartment is simplified into shell and beam elements based on the trabecular plate-and-rod configuration. In comparison to voxel-based μFE models of μCT and measurements from mechanical testing, the computational and experimental gold standards, nonlinear analyses of stiffness and yield strength using the HR-pQCT-based PR μFE models demonstrated high correlation and accuracy. These results indicated that the combination of segmented trabecular plate-rod morphology and adjusted cortical mesh adequately captures mechanics of the whole bone segment. Meanwhile, the PR μFE modeling approach reduced model size by nearly 300-fold and shortened computation time for nonlinear analysis from days to within hours, permitting broader clinical application of HR-pQCT-based nonlinear μFE modeling. Furthermore, the presented approach was tested using a subset of radius and tibia HR-pQCT scans of patients with prior vertebral fracture in a previously published study. Results indicated that yield strength for radius and tibia whole bone segments predicted by the PR μFE model was effective in discriminating vertebral fracture subjects from nonfractured controls. In conclusion, the PR μFE model of HR-pQCT images accurately predicted mechanics for whole bone segments and can serve as a valuable clinical tool to evaluate musculoskeletal diseases.

References

1.
Boutroy
,
S.
,
Bouxsein
,
M. L.
,
Munoz
,
F.
, and
Delmas
,
P. D.
,
2005
, “
In Vivo Assessment of Trabecular Bone Microarchitecture by High-Resolution Peripheral Quantitative Computed Tomography
,”
J. Clin. Endocrinol. Metab.
,
90
(
12
), pp.
6508
6515
.
2.
Burghardt
,
A. J.
,
Buie
,
H. R.
,
Laib
,
A.
,
Majumdar
,
S.
, and
Boyd
,
S. K.
,
2010
, “
Reproducibility of Direct Quantitative Measures of Cortical Bone Microarchitecture of the Distal Radius and Tibia by HR-pQCT
,”
Bone
,
47
(
3
), pp.
519
528
.
3.
MacNeil
,
J. A.
, and
Boyd
,
S. K.
,
2007
, “
Accuracy of High-Resolution Peripheral Quantitative Computed Tomography for Measurement of Bone Quality
,”
Med. Eng. Phys.
,
29
(
10
), pp.
1096
1105
.
4.
Krause
,
M.
,
Museyko
,
O.
,
Breer
,
S.
,
Wulff
,
B.
,
Duckstein
,
C.
,
Vettorazzi
,
E.
,
Glueer
,
C.
,
Püschel
,
K.
,
Engelke
,
K.
, and
Amling
,
M.
,
2014
, “
Accuracy of Trabecular Structure by HR-pQCT Compared to Gold Standard muCT in the Radius and Tibia of Patients With Osteoporosis and Long-Term Bisphosphonate Therapy
,”
Osteoporosis Int.
,
25
(
5
), pp.
1595
1606
.
5.
Zhou
,
B.
,
Zhang
,
X. H.
,
Sekhon
,
K. K.
,
Adams
,
M. F.
,
McMahon
,
D. J.
,
Bilezikian
,
J. P.
,
Shane
,
E.
, and
Guo
,
X. E.
,
2016
, “
High-Resolution Peripheral Quantitative Computed Tomography (HR-pQCT) Can Assess Microstructural and Biomechanical Properties of Both Human Distal Radius and Tibia: Ex Vivo Computational and Experimental Validations
,”
Bone
,
86
, pp.
58
67
.
6.
Nishiyama
,
K. K.
,
Macdonald
,
H. M.
,
Buie
,
H. R.
,
Hanley
,
D. A.
, and
Boyd
,
S. K.
,
2010
, “
Postmenopausal Women With Osteopenia Have Higher Cortical Porosity and Thinner Cortices at the Distal Radius and Tibia Than Women With Normal aBMD: An In Vivo HR-pQCT Study
,”
J. Bone Miner. Res.
,
25
, pp.
882
890
.
7.
Macdonald
,
H. M.
,
Nishiyama
,
K. K.
,
Kang
,
J.
,
Hanley
,
D. A.
, and
Boyd
,
S. K.
,
2011
, “
Age-Related Patterns of Trabecular and Cortical Bone Loss Differ Between Sexes and Skeletal Sites: A Population-Based HR-pQCT Study
,”
J. Bone Miner. Res.
,
26
(
1
), pp.
50
62
.
8.
Boutroy
,
S.
,
Van Rietbergen
,
B.
,
Sornay-Rendu
,
E.
,
Munoz
,
F.
,
Bouxsein
,
M. L.
, and
Delmas
,
P. D.
,
2008
, “
Finite Element Analysis Based on In Vivo HR-pQCT Images of the Distal Radius Is Associated With Wrist Fracture in Postmenopausal Women
,”
J. Bone Miner. Res.
,
23
(
3
), pp.
392
399
.
9.
Liu
,
X. S.
,
Cohen
,
A.
,
Shane
,
E.
,
Yin
,
P. T.
,
Stein
,
E. M.
,
Rogers
,
H.
,
Kokolus
,
S. L.
,
McMahon
,
D. J.
,
Lappe
,
J. M.
,
Recker
,
R. R.
, and
Lang
,
T.
,
2010
, “
Bone Density, Geometry, Microstructure, and Stiffness: Relationships Between Peripheral and Central Skeletal Sites Assessed by DXA, HR-pQCT, and cQCT in Premenopausal Women
,”
J. Bone Miner. Res.
,
25
(
10
), pp.
2229
2238
.
10.
Nishiyama
,
K. K.
,
Macdonald
,
H. M.
,
Hanley
,
D. A.
, and
Boyd
,
S. K.
,
2013
, “
Women With Previous Fragility Fractures Can Be Classified Based on Bone Microarchitecture and Finite Element Analysis Measured With HR-pQCT
,”
Osteoporosis Int.
,
24
(
5
), pp.
1733
1740
.
11.
Liu
,
X. S.
,
Stein
,
E. M.
,
Zhou
,
B.
,
Zhang
,
C. A.
,
Nickolas
,
T. L.
,
Cohen
,
A.
,
Thomas
,
V.
,
McMahon
,
D. J.
,
Cosman
,
F.
,
Nieves
,
J.
, and
Shane
,
E.
,
2012
, “
Individual Trabecula Segmentation (ITS)-Based Morphological Analyses and Microfinite Element Analysis of HR-pQCT Images Discriminate Postmenopausal Fragility Fractures Independent of DXA Measurements
,”
J. Bone Miner. Res.
,
27
(
2
), pp.
263
272
.
12.
Vilayphiou
,
N.
,
Boutroy
,
S.
,
Szulc
,
P.
,
van Rietbergen
,
B.
,
Munoz
,
F.
,
Delmas
,
P. D.
, and
Chapurlat
,
R.
,
2011
, “
Finite Element Analysis Performed on Radius and Tibia HR-pQCT Images and Fragility Fractures at All Sites in Men
,”
J. Bone Miner. Res.
,
26
(
5
), pp.
965
973
.
13.
Vilayphiou
,
N.
,
Boutroy
,
S.
,
Sornay-rendu
,
E.
,
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
.
14.
Johnell
,
O.
, and
Kanis
,
J. A.
,
2006
, “
An Estimate of the Worldwide Prevalence and Disability Associated With Osteoporotic Fractures
,”
Osteoporosis Int.
,
17
(
12
), pp.
1726
1733
.
15.
Miller
,
P. D.
, and
Leonard
,
M. B.
,
2006
, “
Clinical Use of Bone Mass Measurements in Adults for the Assessment and Management of Osteoporosis
,”
Primer on the Metabolic Bone Disease and Disorders of Mineral Metabolism
, 6th ed.,
American Society for Bone and Mineral Research
,
Washington, DC
, pp.
150
161
.
16.
Ulrich
,
D.
,
van Rietbergen
,
B.
,
Laib
,
A.
, and
Ruegsegger
,
P.
,
1999
, “
The Ability of Three-Dimensional Structural Indices to Reflect Mechanical Aspects of Trabecular Bone
,”
Bone
,
25
(
1
), pp.
55
60
.
17.
Schileo
,
E.
,
Taddei
,
F.
,
Malandrino
,
A.
,
Cristofolini
,
L.
, and
Viceconti
,
M.
,
2007
, “
Subject-Specific Finite Element Models Can Accurately Predict Strain Levels in Long Bones
,”
J. Biomech.
,
40
(
13
), pp.
2982
2989
.
18.
Sornay-Rendu
,
E.
,
Boutroy
,
S.
,
Munoz
,
F.
, and
Delmas
,
P. D.
,
2007
, “
Alterations of Cortical and Trabecular Architecture Are Associated With Fractures in Postmenopausal Women, Partially Independent of Decreased BMD Measured by DXA: The OFELY Study
,”
J. Bone Miner. Res.
,
22
(
3
), pp.
425
433
.
19.
Stein
,
E. M.
,
Liu
,
X. S.
,
Nickolas
,
T. L.
,
Cohen
,
A.
,
McMahon
,
D. J.
,
Zhou
,
B.
,
Zhang
,
C.
,
Kamanda-Kosseh
,
M.
,
Cosman
,
F.
,
Nieves
,
J.
, and
Guo
,
X. E.
,
2012
, “
Microarchitectural Abnormalities Are More Severe in Postmenopausal Women With Vertebral Compared to Nonvertebral Fractures
,”
J. Clin. Endocrinol. Metab.
,
97
(
10
), pp.
E1918
1926
.
20.
Stein
,
E. M.
,
Sajda
,
P.
,
Saha
,
P. K.
,
Wehrli
,
F. W.
,
Bevill
,
G.
,
Keaveny
,
T. M.
, and
Guo
,
X. E.
,
2010
, “
Abnormal Microarchitecture and Reduced Stiffness at the Radius and Tibia in Postmenopausal Women With Fractures
,”
J. Bone Miner. Res.
,
25
(
12
), pp.
2572
2581
.
21.
Liu
,
X. S.
,
Sajda
,
P.
,
Saha
,
P. K.
,
Wehrli
,
F. W.
,
Bevill
,
G.
,
Keaveny
,
T. M.
, and
Guo
,
X. E.
,
2008
, “
Complete Volumetric Decomposition of Individual Trabecular Plates and Rods and Its Morphological Correlations With Anisotropic Elastic Moduli in Human Trabecular Bone
,”
J. Bone Miner. Res.
,
23
(
2
), pp.
223
235
.
22.
Christen
,
D.
,
Webster
,
D. J.
, and
Muller
,
R.
,
2010
, “
Multiscale Modelling and Nonlinear Finite Element Analysis as Clinical Tools for the Assessment of Fracture Risk
,”
Philos. Trans. R. Soc., A
,
368
(
1920
), pp.
2653
2668
.
23.
Liu
,
X. S.
,
Zhang
,
X. H.
,
Sekhon
,
K. K.
,
Adams
,
M. F.
,
McMahon
,
D. J.
,
Bilezikian
,
J. P.
,
Shane
,
E.
, and
Guo
,
X. E.
,
2010
, “
High-Resolution Peripheral Quantitative Computed Tomography Can Assess Microstructural and Mechanical Properties of Human Distal Tibial Bone
,”
J. Bone Miner. Res.
,
25
, pp.
746
756
.
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.
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
.
26.
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.
,
27
(
9
), pp.
1127
1136
.
27.
Niebur
,
G. L.
,
Feldstein
,
M. J.
,
Yuen
,
J. C.
,
Chen
,
T. J.
, and
Keaveny
,
T. M.
,
2000
, “
High-Resolution Finite Element Models With Tissue Strength Asymmetry Accurately Predict Failure of Trabecular Bone
,”
J. Biomech.
,
33
(
12
), pp.
1575
1583
.
28.
van Lenthe
,
G. H.
, and
Muller
,
R.
,
2006
, “
Prediction of Failure Load Using Micro-Finite Element Analysis Models: Toward In Vivo Strength Assessment
,”
Drug Discovery Today Technol.
,
3
(
2
), pp.
221
229
.
29.
Wolfram
,
U.
,
Gross
,
T.
,
Pahr
,
D. H.
,
Schwiedrzik
,
J.
,
Wilke
,
H. J.
, and
Zysset
,
P. K.
,
2012
, “
Fabric-Based Tsai-Wu Yield Criteria for Vertebral Trabecular Bone in Stress and Strain Space
,”
J. Mech. Behav. Biomed. Mater.
,
15
, pp.
218
228
.
30.
Pistoia
,
W.
,
Van Rietbergen
,
B.
,
Lochmüller
,
E. M.
,
Lill
,
C. A.
,
Eckstein
,
F.
, and
Rüegsegger
,
P.
,
2002
, “
Estimation of Distal Radius Failure Load With Micro-Finite Element Analysis Models Based on Three-Dimensional Peripheral Quantitative Computed Tomography Images
,”
Bone
,
30
(
6
), pp.
842
848
.
31.
Hosseini
,
H. S.
,
Dünki
,
A.
,
Fabech
,
J.
,
Stauber
,
M.
,
Vilayphiou
,
N.
,
Pahr
,
D.
,
Pretterklieber
,
M.
,
Wandel
,
J.
,
van Rietbergen
,
B.
, and
Zysset
,
P. K.
,
2017
, “
Fast Estimation of Colles' Fracture Load of the Distal Section of the Radius by Homogenized Finite Element Analysis Based on HR-pQCT
,”
Bone
,
97
, pp.
65
75
.
32.
Kroker
,
A.
,
Zhu
,
Y.
,
Manske
,
S. L.
,
Barber
,
R.
,
Mohtadi
,
N.
, and
Boyd
,
S. K.
,
2017
, “
Quantitative In Vivo Assessment of Bone Microarchitecture in the Human Knee Using HR-pQCT
,”
Bone
,
97
, pp.
43
48
.
33.
Kroker
,
A.
,
Bhatla
,
J. L.
,
Emery
,
C. A.
,
Manske
,
S. L.
, and
Boyd
,
S. K.
,
2018
, “
Subchondral Bone Microarchitecture in ACL Reconstructed Knees of Young Women: A Comparison With Contralateral and Uninjured Control Knees
,”
Bone
,
111
, pp.
1
8
.
34.
Ibanez
,
L.
,
Schroeder
,
W.
,
Ng
,
L.
, and
Cates
,
J.
,
2005
, “
The ITK Software Guide
,” Kitware, Clifton Park, NY.
35.
Wang
,
J.
,
Zhou
,
B.
,
Liu
,
X. S.
,
Fields
,
A. J.
,
Sanyal
,
A.
,
Shi
,
X.
,
Adams
,
M.
,
Keaveny
,
T. M.
, and
Guo
,
X. E.
,
2015
, “
Trabecular Plates and Rods Determine Elastic Modulus and Yield Strength of Human Trabecular Bone
,”
Bone
,
72
, pp.
71
80
.
36.
Liu
,
X. S.
,
Wang
,
J.
,
Zhou
,
B.
,
Stein
,
E.
,
Shi
,
X.
,
Adams
,
M.
,
Shane
,
E.
, and
Guo
,
X. E.
,
2013
, “
Fast Trabecular Bone Strength Predictions of HR-pQCT and Individual Trabeculae Segmentation-Based Plate and Rod Finite Element Model Discriminate Postmenopausal Vertebral Fractures
,”
J. Bone Miner. Res.
,
28
(
7
), pp.
1666
1678
.
37.
Wang
,
H.
,
Liu
,
X. S.
,
Zhou
,
B.
,
Wang
,
J.
,
Ji
,
B.
,
Huang
,
Y.
,
Hwang
,
K. C.
, and
Guo
,
X. E.
,
2013
, “
Accuracy of Individual Trabecula Segmentation Based Plate and Rod Finite Element Models in Idealized Trabecular Bone Microstructure
,”
J. Biomech. Eng.
,
135
(
4
), p.
044502
.
38.
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
.
39.
McCalden
,
R. W.
,
McGeough
,
J. A.
,
Barker
,
M. B.
, and
Court-Brown
,
C. M.
,
1993
, “
Age-Related Changes in the Tensile Properties of Cortical Bone. The Relative Importance of Changes in Porosity, Mineralization, and Microstructure
,”
J. Bone Jt. Surg. Am.
,
75
(
8
), pp.
1193
1205
.
40.
Schaffler
,
M. B.
, and
Burr
,
D. B.
,
1988
, “
Stiffness of Compact Bone: Effects of Porosity and Density
,”
J. Biomech.
,
21
(
1
), pp.
13
16
.
41.
Wachter
,
N. J.
,
Augat
,
P.
,
Krischak
,
G. D.
,
Sarkar
,
M. R.
,
Mentzel
,
M.
,
Kinzl
,
L.
, and
Claes
,
L.
,
2001
, “
Prediction of Strength of Cortical Bone In Vitro by Microcomputed Tomography
,”
Clin. Biomech.
,
16
(
3
), pp.
252
256
.
42.
Folsch
,
C.
,
Mittelmeier
,
W.
,
Bilderbeek
,
U.
,
Timmesfeld
,
N.
,
von Garrel
,
T.
, and
Matter
,
H. P.
,
2012
, “
Effect of Storage Temperature on Allograft Bone
,”
Transfus. Med. Hemother
,
39
, pp.
36
40
.
43.
Hamer
,
A. J.
,
Strachan
,
J. R.
,
Black
,
M. M.
,
Ibbotson
,
C. J.
,
Stockley
,
I.
, and
Elson
,
R. A.
,
1996
, “
Biochemical Properties of Cortical Allograft Bone Using a New Method of Bone Strength Measurement. A Comparison of Fresh, Fresh-Frozen, and Irradiated Bone
,”
J. Bone Jt. Surg. Br
,
78
(3), pp.
363
368
.https://www.ncbi.nlm.nih.gov/pubmed/8636167#
44.
Wieding
,
J.
,
Mick
,
E.
,
Wree
,
A.
, and
Bader
,
R.
,
2015
, “
Influence of Three Different Preservative Techniques on the Mechanical Properties of the Ovine Cortical Bone
,”
Acta Bioeng. Biomech.
,
17
(1), pp.
137
146
https://www.ncbi.nlm.nih.gov/pubmed/25952021.
45.
Buie
,
H. R.
,
Campbell
,
G. M.
,
Klinck
,
R. J.
,
MacNeil
,
J. A.
, and
Boyd
,
S. K.
,
2007
, “
Automatic Segmentation of Cortical and Trabecular Compartments Based on a Dual Threshold Technique for In Vivo Micro-CT Bone Analysis
,”
Bone
,
41
(
4
), pp.
505
515
.
46.
Papadopoulos
,
P.
, and
Lu
,
J.
,
2001
, “
On the Formulation and Numerical Solution of Problems in Anisotropic Finite Plasticity
,”
Comput. Methods Appl. Mech. Eng.
,
190
(
37–38
), pp.
4889
4910
.
47.
Papadopoulos
,
P.
, and
Lu
,
J.
,
1998
, “
A General Framework for the Numerical Solution of Problems in Finite Elasto-Plasticity
,”
Comput. Methods Appl. Mech. Eng.
,
159
(
1–2
), pp.
1
18
.
48.
Goldstein
,
S. A.
,
1987
, “
The Mechanical Properties of Trabecular Bone: Dependence on Anatomic Location and Function
,”
J. Biomech.
,
20
(
11–12
), pp.
1055
1061
.
49.
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
.
50.
Saha
,
P. K.
, and
Chaudhuri
,
B. B.
,
1996
, “
3D Digital Topology Under Binary Transformation With Applications
,”
Comput. Vision Image Understanding
,
63
(
3
), pp.
418
429
.
51.
Saha
,
P. K.
,
Chaudhuri
,
B. B.
, and
Majumder
,
D. D.
,
1997
, “
A New Shape Preserving Parallel Thinning Algorithm for 3D Digital Images
,”
Pattern Recognit.
,
30
(
12
), pp.
1939
1955
.
52.
Delone
,
B.
,
1934
, “
Sur la sphère vide
,” A la mémoire de George Voronoi.,
6
, pp. 793–800.
You do not currently have access to this content.