Abstract

Vertebral fractures are the most common osteoporotic fractures, but clinical means for assessment of vertebral bone integrity are limited in accuracy, as they typically use surrogate measures that are indirectly related to mechanics. The objective of this study was to examine the extent to which intravertebral strain distributions and changes in cancellous bone texture generated by a load of physiological magnitude can be characterized using a clinically available imaging modality. We hypothesized that digital tomosynthesis-based digital volume correlation (DTS-DVC) and image texture-based metrics of cancellous bone microstructure can detect development of mechanical strains under load. Isolated cadaveric T11 vertebrae and L2–L4 vertebral segments were DTS imaged in a nonloaded state and under physiological load levels. Axial strain, maximum principal strain, maximum compressive and tensile principal strains, and von Mises equivalent strain were calculated using the DVC technique. The change in textural parameters (line fraction deviation, anisotropy, and fractal parameters) under load was calculated within the cancellous centrum. The effect of load on measured strains and texture variables was tested using mixed model analysis of variance, and relationships of strain and texture variables with donor age, bone density parameters, and bone size were examined using regression models. Magnitudes and heterogeneity of intravertebral strain measures correlated with applied loading and were significantly different from background noise. Image texture parameters were found to change with applied loading, but these changes were not observed in the second experiment testing L2–L4 segments. DTS-DVC-derived strains correlated with age more strongly than did bone mineral density (BMD) for T11.

References

1.
Samelson
,
E. J.
,
Hannan
,
M. T.
,
Zhang
,
Y.
,
Genant
,
H. K.
,
Felson
,
D. T.
, and
Kiel
,
D. P.
,
2006
, “
Incidence and Risk Factors for Vertebral Fracture in Women and Men: 25-Year Follow-Up Results From the Population-Based Framingham Study
,”
J Bone Miner. Res.
,
21
(
8
), pp.
1207
1214
.10.1359/jbmr.060513
2.
Felsenberg
,
D.
,
Silman
,
A. J.
,
Lunt
,
M.
,
Armbrecht
,
G.
,
Ismail
,
A. A.
,
Finn
,
J. D.
,
Cockerill
,
W. C.
,
Banzer
,
D.
,
Benevolenskaya
,
L. I.
,
Bhalla
,
A.
,
Bruges Armas
,
J.
,
Cannata
,
J. B.
,
Cooper
,
C.
,
Dequeker
,
J.
,
Eastell
,
R.
,
Felsch
,
B.
,
Gowin
,
W.
,
Havelka
,
S.
,
Hoszowski
,
K.
,
Jajic
,
I.
,
Janott
,
J.
,
Johnell
,
O.
,
Kanis
,
J. A.
,
Kragl
,
G.
,
Lopes Vaz
,
A.
,
Lorenc
,
R.
,
Lyritis
,
G.
,
Masaryk
,
P.
,
Matthis
,
C.
,
Miazgowski
,
T.
,
Parisi
,
G.
,
Pols
,
H. A.
,
Poor
,
G.
,
Raspe
,
H. H.
,
Reid
,
D. M.
,
Reisinger
,
W.
,
Schedit-Nave
,
C.
,
Stepan
,
J. J.
,
Todd
,
C. J.
,
Weber
,
K.
,
Woolf
,
A. D.
,
Yershova
,
O. B.
,
Reeve
,
J.
, and
O'Neill
,
T. W.
,
2002
, “
Incidence of Vertebral Fracture in Europe: Results From the European Prospective Osteoporosis Study (EPOS
),”
J. Bone Miner. Res.
,
17
(
4
), pp.
716
724
.10.1359/jbmr.2002.17.4.716
3.
Burge
,
R.
,
Dawson-Hughes
,
B.
,
Solomon
,
D. H.
,
Wong
,
J. B.
,
King
,
A.
, and
Tosteson
,
A.
,
2007
, “
Incidence and Economic Burden of Osteoporosis-Related Fractures in the United States, 2005–2025
,”
J. Bone Miner. Res.
,
22
(
3
), pp.
465
475
.10.1359/jbmr.061113
4.
Sambrook
,
P.
, and
Cooper
,
C.
,
2006
, “
Osteoporosis
,”
Lancet
,
367
(
9527
), pp.
2010
2018
.10.1016/S0140-6736(06)68891-0
5.
Culham
,
E. G.
,
Jimenez
,
H. A.
, and
King
,
C. E.
,
1994
, “
Thoracic Kyphosis, Rib Mobility, and Lung Volumes in Normal Women and Women With Osteoporosis
,”
Spine (Phila Pa 1976)
,
19
(
11
), pp.
1250
1255
.10.1097/00007632-199405310-00010
6.
Di Bari
,
M.
,
Chiarlone
,
M.
,
Matteuzzi
,
D.
,
Zacchei
,
S.
,
Pozzi
,
C.
,
Bellia
,
V.
,
Tarantini
,
F.
,
Pini
,
R.
,
Masotti
,
G.
, and
Marchionni
,
N.
,
2004
, “
Thoracic Kyphosis and Ventilatory Dysfunction in Unselected Older Persons: An Epidemiological Study in Dicomano, Italy
,”
J. Am. Geriatr. Soc.
,
52
(
6
), pp.
909
915
.10.1111/j.1532-5415.2004.52257.x
7.
Schlaich
,
C.
,
Minne
,
H. W.
,
Bruckner
,
T.
,
Wagner
,
G.
,
Gebest
,
H. J.
,
Grunze
,
M.
,
Ziegler
,
R.
, and
Leidig-Bruckner
,
G.
,
1998
, “
Reduced Pulmonary Function in Patients With Spinal Osteoporotic Fractures
,”
Osteoporos. Int.
,
8
(
3
), pp.
261
267
.10.1007/s001980050063
8.
Miyakoshi
,
N.
,
Kasukawa
,
Y.
,
Sasaki
,
H.
,
Kamo
,
K.
, and
Shimada
,
Y.
,
2009
, “
Impact of Spinal Kyphosis on Gastroesophageal Reflux Disease Symptoms in Patients With Osteoporosis
,”
Osteoporos Int
,
20
(
7
), pp.
1193
1198
.10.1007/s00198-008-0777-x
9.
Klotzbuecher
,
C. M.
,
Ross
,
P. D.
,
Landsman
,
P. B.
,
Abbott
,
T. A.
, 3rd.
, and
Berger
,
M.
,
2010
, “
Patients With Prior Fractures Have an Increased Risk of Future Fractures: A Summary of the Literature and Statistical Synthesis
,”
J. Bone Miner. Res.
,
15
(
4
), pp.
721
739
.10.1359/jbmr.2000.15.4.721
10.
Ettinger
,
B.
,
Black
,
D. M.
,
Mitlak
,
B. H.
,
Knickerbocker
,
R. K.
,
Nickelsen
,
T.
,
Genant
,
H. K.
,
Christiansen
,
C.
,
Delmas
,
P. D.
,
Zanchetta
,
J. R.
,
Stakkestad
,
J.
,
Gluer
,
C. C.
,
Krueger
,
K.
,
Cohen
,
F. J.
,
Eckert
,
S.
,
Ensrud
,
K. E.
,
Avioli
,
L. V.
,
Lips
,
P.
, and
Cummings
,
S. R.
,
1999
, “
Reduction of Vertebral Fracture Risk in Postmenopausal Women With Osteoporosis Treated With Raloxifene: Results From a 3-Year Randomized Clinical Trial. Multiple Outcomes of Raloxifene Evaluation (MORE) Investigators
,”
JAMA
,
282
(
7
), pp.
637
645
.10.1001/jama.282.7.637
11.
Lindsay
,
R.
,
Silverman
,
S. L.
,
Cooper
,
C.
,
Hanley
,
D. A.
,
Barton
,
I.
,
Broy
,
S. B.
,
Licata
,
A.
,
Benhamou
,
L.
,
Geusens
,
P.
,
Flowers
,
K.
,
Stracke
,
H.
, and
Seeman
,
E.
,
2001
, “
Risk of New Vertebral Fracture in the Year Following a Fracture
,”
JAMA
,
285
(
3
), pp.
320
323
.10.1001/jama.285.3.320
12.
Black
,
D. M.
,
Arden
,
N. K.
,
Palermo
,
L.
,
Pearson
,
J.
, and
Cummings
,
S. R.
,
1999
, “
Prevalent Vertebral Deformities Predict Hip Fractures and New Vertebral Deformities but Not Wrist Fractures. Study of Osteoporotic Fractures Research Group
,”
J. Bone Miner. Res.
,
14
(
5
), pp.
821
828
.10.1359/jbmr.1999.14.5.821
13.
Delmas
,
P. D.
,
Genant
,
H. K.
,
Crans
,
G. G.
,
Stock
,
J. L.
,
Wong
,
M.
,
Siris
,
E.
, and
Adachi
,
J. D.
,
2003
, “
Severity of Prevalent Vertebral Fractures and the Risk of Subsequent Vertebral and Nonvertebral Fractures: Results From the More Trial
,”
Bone
,
33
(
4
), pp.
522
532
.10.1016/S8756-3282(03)00241-2
14.
Curtis
,
J. R.
,
Arora
,
T.
,
Matthews
,
R. S.
,
Taylor
,
A.
,
Becker
,
D. J.
,
Colon-Emeric
,
C.
,
Kilgore
,
M. L.
,
Morrisey
,
M. A.
,
Saag
,
K. G.
,
Safford
,
M. M.
,
Warriner
,
A.
, and
Delzell
,
E.
,
2010
, “
Is Withholding Osteoporosis Medication After Fracture Sometimes Rational? A Comparison of the Risk for Second Fracture Versus Death
,”
J. Am. Med. Dir. Assoc.
,
11
(
8
), pp.
584
591
.10.1016/j.jamda.2009.12.004
15.
Melton
,
L. J.
, 3rd
,
Atkinson
,
E. J.
,
Cooper
,
C.
,
O'Fallon
,
W. M.
, and
Riggs
,
B. L.
,
1999
, “
Vertebral Fractures Predict Subsequent Fractures
,”
Osteoporos. Int.
,
10
(
3
), pp.
214
221
.10.1007/s001980050218
16.
Cranney
,
A.
,
Jamal
,
S. A.
,
Tsang
,
J. F.
,
Josse
,
R. G.
, and
Leslie
,
W. D.
,
2007
, “
Low Bone Mineral Density and Fracture Burden in Postmenopausal Women
,”
CMAJ
,
177
(
6
), pp.
575
580
.10.1503/cmaj.070234
17.
Myers
,
B. S.
,
Arbogast
,
K. B.
,
Lobaugh
,
B.
,
Harper
,
K. D.
,
Richardson
,
W. J.
, and
Drezner
,
M. K.
,
2009
, “
Improved Assessment of Lumbar Vertebral Body Strength Using Supine Lateral Dual-Energy x-Ray Absorptiometry
,”
J. Bone Miner. Res.
,
9
(
5
), pp.
687
693
.10.1002/jbmr.5650090514
18.
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
19.
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
20.
Viguet-Carrin
,
S.
,
Roux
,
J. P.
,
Arlot
,
M. E.
,
Merabet
,
Z.
,
Leeming
,
D. J.
,
Byrjalsen
,
I.
,
Delmas
,
P. D.
, and
Bouxsein
,
M. L.
,
2006
, “
Contribution of the Advanced Glycation End Product Pentosidine and of Maturation of Type I Collagen to Compressive Biomechanical Properties of Human Lumbar Vertebrae
,”
Bone
,
39
(
5
), pp.
1073
1079
.10.1016/j.bone.2006.05.013
21.
Guenoun
,
D.
,
Le Corroller
,
T.
,
Acid
,
S.
,
Pithioux
,
M.
,
Pauly
,
V.
,
Ariey-Bonnet
,
D.
,
Chabrand
,
P.
, and
Champsaur
,
P.
,
2013
, “
Radiographical Texture Analysis Improves the Prediction of Vertebral Fracture: An Ex Vivo Biomechanical Study
,”
Spine (Phila Pa 1976)
,
38
(
21
), pp.
E1320
E1326
.10.1097/BRS.0b013e3182a28fa9
22.
Crawford
,
R. P.
,
Cann
,
C. E.
, and
Keaveny
,
T. M.
,
2003
, “
Finite Element Models Predict In Vitro Vertebral Body Compressive Strength Better Than Quantitative Computed Tomography
,”
Bone
,
33
(
4
), pp.
744
750
.10.1016/S8756-3282(03)00210-2
23.
Dall'Ara
,
E.
,
Pahr
,
D.
,
Varga
,
P.
,
Kainberger
,
F.
, and
Zysset
,
P.
,
2012
, “
QCT-Based Finite Element Models Predict Human Vertebral Strength In Vitro Significantly Better Than Simulated DEXA
,”
Osteoporos. Int.
,
23
(
2
), pp.
563
572
.10.1007/s00198-011-1568-3
24.
Imai
,
K.
,
Ohnishi
,
I.
,
Bessho
,
M.
, and
Nakamura
,
K.
,
2006
, “
Nonlinear Finite Element Model Predicts Vertebral Bone Strength and Fracture site
,”
Spine (Phila Pa 1976)
,
31
(
16
), pp.
1789
1794
.10.1097/01.brs.0000225993.57349.df
25.
Kopperdahl
,
D. L.
,
Aspelund
,
T.
,
Hoffmann
,
P. F.
,
Sigurdsson
,
S.
,
Siggeirsdottir
,
K.
,
Harris
,
T. B.
,
Gudnason
,
V.
, and
Keaveny
,
T. M.
,
2014
, “
Assessment of Incident Spine and Hip Fractures in Women and Men Using Finite Element Analysis of CT Scans
,”
J. Bone Miner. Res.
,
29
(
3
), pp.
570
580
.10.1002/jbmr.2069
26.
Wang
,
X.
,
Sanyal
,
A.
,
Cawthon
,
P. M.
,
Palermo
,
L.
,
Jekir
,
M.
,
Christensen
,
J.
,
Ensrud
,
K. E.
,
Cummings
,
S. R.
,
Orwoll
,
E.
,
Black
,
D. M.
, and
Keaveny
,
T. M.
,
for the Osteoporotic Fractures in Men (MrOS) Research Group
2012
, “
Prediction of New Clinical Vertebral Fractures in Elderly Men Using Finite Element Analysis of CT Scans
,”
J. Bone Miner. Res.
,
27
(
4
), pp.
808
816
.10.1002/jbmr.1539
27.
Hussein
,
A. I.
,
Louzeiro
,
D. T.
,
Unnikrishnan
,
G. U.
, and
Morgan
,
E. F.
,
2018
, “
Differences in Trabecular Microarchitecture and Simplified Boundary Conditions Limit the Accuracy of Quantitative Computed Tomography-Based Finite Element Models of Vertebral Failure
,”
ASME J Biomech. Eng.
,
140
(
2
), p. 021004.10.1115/1.4038609
28.
Chen
,
Y.
,
Dall Ara
,
E.
,
Sales
,
E.
,
Manda
,
K.
,
Wallace
,
R.
,
Pankaj
,
P.
, and
Viceconti
,
M.
,
2017
, “
Micro-CT Based Finite Element Models of Cancellous Bone Predict Accurately Displacement Once the Boundary Condition is Well Replicated: A Validation Study
,”
J. Mech. Behav. Biomed. Mater.
,
65
, pp.
644
651
.10.1016/j.jmbbm.2016.09.014
29.
Bay
,
B. K.
,
Smith
,
T. S.
,
Fyhrie
,
D. P.
, and
Saad
,
M.
,
1999
, “
Digital Volume Correlation: Three-Dimensional Strain Mapping Using X-Ray Tomography
,”
Exp. Mech.
,
39
(
3
), pp.
217
226
.10.1007/BF02323555
30.
Palanca
,
M.
,
Bodey
,
A. J.
,
Giorgi
,
M.
,
Viceconti
,
M.
,
Lacroix
,
D.
,
Cristofolini
,
L.
, and
Dall'Ara
,
E.
,
2017
, “
Local Displacement and Strain Uncertainties in Different Bone Types by Digital Volume Correlation of Synchrotron Microtomograms
,”
J. Biomech.
,
58
, pp.
27
36
.10.1016/j.jbiomech.2017.04.007
31.
Le Cann
,
S.
,
Tudisco
,
E.
,
Perdikouri
,
C.
,
Belfrage
,
O.
,
Kaestner
,
A.
,
Hall
,
S.
,
Tagil
,
M.
, and
Isaksson
,
H.
,
2017
, “
Characterization of the Bone-Metal Implant Interface by Digital Volume Correlation of in-Situ Loading Using Neutron Tomography
,”
J. Mech. Behav. Biomed. Mater.
,
75
, pp.
271
278
.10.1016/j.jmbbm.2017.07.001
32.
Ridzwan
,
M. I. Z.
,
Sukjamsri
,
C.
,
Pal
,
B.
,
van Arkel
,
R. J.
,
Bell
,
A.
,
Khanna
,
M.
,
Baskaradas
,
A.
,
Abel
,
R.
,
Boughton
,
O.
,
Cobb
,
J.
, and
Hansen
,
U. N.
,
2018
, “
Femoral Fracture Type Can Be Predicted From Femoral Structure: A Finite Element Study Validated by Digital Volume Correlation Experiments
,”
J. Orthop. Res.
,
36
(
3
), pp.
993
1001
.10.1002/jor.23669
33.
Rapagna
,
S.
,
Berahmani
,
S.
,
Wyers
,
C. E.
,
van den Bergh
,
J. P. W.
,
Reynolds
,
K. J.
,
Tozzi
,
G.
,
Janssen
,
D.
, and
Perilli
,
E.
,
2019
, “
Quantification of Human Bone Microarchitecture Damage in Press-Fit Femoral Knee Implantation Using HR-pQCT and Digital Volume Correlation
,”
J. Mech. Behav. Biomed. Mater.
,
97
, pp.
278
287
.10.1016/j.jmbbm.2019.04.054
34.
Oravec
,
D.
,
Flynn
,
M. J.
,
Zauel
,
R.
,
Rao
,
S.
, and
Yeni
,
Y. N.
,
2019
, “
Digital Tomosynthesis Based Digital Volume Correlation: A Clinically Viable Noninvasive Method for Direct Measurement of Intravertebral Displacements Using Images of the Human Spine Under Physiological Load
,”
Med. Phys.
,
46
(
10
), pp.
4553
4562
.10.1002/mp.13750
35.
Mettler
,
F. A.
, Jr.
Huda
,
W.
,
Yoshizumi
,
T. T.
, and
Mahesh
,
M.
,
2008
, “
Effective Doses in Radiology and Diagnostic Nuclear Medicine: A Catalog
,”
Radiology
,
248
(
1
), pp.
254
263
.10.1148/radiol.2481071451
36.
Zhang
,
Y.
,
Li
,
X.
,
Segars
,
W. P.
, and
Samei
,
E.
,
2014
, “
Comparison of Patient Specific Dose Metrics Between Chest Radiography, Tomosynthesis, and CT for Adult Patients of Wide Ranging Body Habitus
,”
Med. Phys.
,
41
(
2
), p.
023901
.10.1118/1.4859315
37.
Yeni
,
Y. N.
,
Wu
,
B.
,
Huang
,
L.
, and
Oravec
,
D.
,
2013
, “
Mechanical Loading Causes Detectable Changes in Morphometric Measures of Trabecular Structure in Human Cancellous Bone
,”
ASME J. Biomech. Eng.
,
135
(
5
), p.
54505
.10.1115/1.4024136
38.
Gillard
,
F.
,
Boardman
,
R.
,
Mavrogordato
,
M.
,
Hollis
,
D.
,
Sinclair
,
I.
,
Pierron
,
F.
, and
Browne
,
M.
,
2014
, “
The Application of Digital Volume Correlation (DVC) to Study the Microstructural Behaviour of Trabecular Bone During Compression
,”
J. Mech. Behav. Biomed. Mater.
,
29
, pp.
480
499
.10.1016/j.jmbbm.2013.09.014
39.
Oravec
,
D.
,
Yaldo
,
O.
,
Bolton
,
C.
,
Flynn
,
M. J.
,
van Holsbeeck
,
M.
, and
Yeni
,
Y. N.
,
2019
, “
Digital Tomosynthesis and Fractal Analysis Predict Prevalent Vertebral Fractures in Patients With Multiple Myeloma: A Preliminary In Vivo Study
,”
AJR Am. J. Roentgenol.
, 213(1), pp.
W38
W44
.10.2214/AJR.18.20700
40.
Takasu
,
M.
,
Kaichi
,
Y.
,
Awai
,
K.
,
Asaoku
,
H.
,
Kuroda
,
Y.
, and
Sakai
,
A.
,
2014
, “
Vertebral Fracture Risk of Multiple Myeloma Assessed by a CT-Based Finite Element and Trabecular Structure Analysis
,”
Clin. Lymphoma, Myeloma Leukemia
,
14
(
1
), pp.
12
13
.10.1016/j.clml.2013.12.012
41.
Kim
,
W.
,
Oravec
,
D.
,
Nekkanty
,
S.
,
Yerramshetty
,
J.
,
Sander
,
E. A.
,
Divine
,
G. W.
,
Flynn
,
M. J.
, and
Yeni
,
Y. N.
,
2015
, “
Digital Tomosynthesis (DTS) for Quantitative Assessment of Trabecular Microstructure in Human Vertebral Bone
,”
Med. Eng. Phys.
,
37
(
1
), pp.
109
120
.10.1016/j.medengphy.2014.11.005
42.
Kim
,
W.
,
Oravec
,
D.
,
Divine
,
G. W.
,
Flynn
,
M. J.
, and
Yeni
,
Y. N.
,
2017
, “
Effect of View, Scan Orientation and Analysis Volume on Digital Tomosynthesis (DTS) Based Textural Analysis of Bone
,”
Ann. Biomed. Eng.
,
45
(
5
), pp.
1236
1246
.10.1007/s10439-017-1792-x
43.
Oravec
,
D.
,
Zauel
,
R.
,
Flynn
,
M. J.
, and
Yeni
,
Y. N.
,
2020
, “
Vertebral Stiffness Measured Via Tomosynthesis-Based Digital Volume Correlation is Strongly Correlated With Reference Values From Micro-CT-Based DVC
,”
Med. Eng. Phys.
,
84
, pp.
169
173
.10.1016/j.medengphy.2020.08.008
44.
Iyer
,
S.
,
Christiansen
,
B. A.
,
Roberts
,
B. J.
,
Valentine
,
M. J.
,
Manoharan
,
R. K.
, and
Bouxsein
,
M. L.
,
2010
, “
A Biomechanical Model for Estimating Loads on Thoracic and Lumbar Vertebrae
,”
Clin. Biomech.
,
25
(
9
), pp.
853
858
.10.1016/j.clinbiomech.2010.06.010
45.
Zauel
,
R.
,
Yeni
,
Y. N.
,
Bay
,
B. K.
,
Dong
,
X. N.
, and
Fyhrie
,
D. P.
,
2006
, “
Comparison of the Linear Finite Element Prediction of Deformation and Strain of Human Cancellous Bone to 3D Digital Volume Correlation Measurements
,”
ASME J. Biomech. Eng.
,
128
(
1
), pp.
1
6
.10.1115/1.2146001
46.
Malvern
,
L.
,
1969
,
Introduction to Continuum Mechanics
,
Prentice Hall
,
Engle Cliffs, NJ
, pp.
301
320
.
47.
Yeni
,
Y. N.
,
Kim
,
W.
,
Oravec
,
D.
,
Nixon
,
M.
,
Divine
,
G. W.
, and
Flynn
,
M. J.
,
2018
, “
Assessment of Vertebral Wedge Strength Using Cancellous Textural Properties Derived From Digital Tomosynthesis and Density Properties From Dual Energy X-Ray Absorptiometry and High Resolution Computed Tomography
,”
J. Biomech.
,
79
, pp.
191
197
.10.1016/j.jbiomech.2018.08.019
48.
Nelson
,
F.
,
Bokhari
,
O.
,
Oravec
,
D.
,
Kim
,
W.
,
Flynn
,
M.
,
Lumley
,
C.
,
McPhilamy
,
A.
, and
Yeni
,
Y. N.
,
2017
, “
The Use of Tomosynthesis in the Global Study of Knee Subchondral Insufficiency Fractures
,”
Acad. Radiol.
,
24
(
2
), pp.
175
183
.10.1016/j.acra.2016.09.015
49.
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
50.
Liu
,
L.
, and
Morgan
,
E. F.
,
2007
, “
Accuracy and Precision of Digital Volume Correlation in Quantifying Displacements and Strains in Trabecular Bone
,”
J. Biomech.
,
40
(
15
), pp.
3516
3520
.10.1016/j.jbiomech.2007.04.019
51.
Verhulp
,
E.
,
van Rietbergen
,
B.
, and
Huiskes
,
R.
,
2004
, “
A Three-Dimensional Digital Image Correlation Technique for Strain Measurements in Microstructures
,”
J. Biomech.
,
37
(
9
), pp.
1313
1320
.10.1016/j.jbiomech.2003.12.036
52.
Hardisty
,
M. R.
, and
Whyne
,
C. M.
,
2009
, “
Whole Bone Strain Quantification by Image Registration: A Validation Study
,”
ASME J. Biomech. Eng.
,
131
(
6
), p.
064502
.10.1115/1.3127249
53.
ASTM
,
2014
, “
Standard Practice for Use of the Terms Precision and Bias in ASTM Test Methods
,” ASTM International, West Conshohocken, PA, Standard No. ASTM E177-14.
54.
Baim
,
S.
,
Wilson
,
C. R.
,
Lewiecki
,
E. M.
,
Luckey
,
M. M.
,
Downs
,
R. W.
, Jr
,., and
Lentle
,
B. C.
,
2005
, “
Precision Assessment and Radiation Safety for Dual-Energy X-Ray Absorptiometry: Position Paper of the International Society for Clinical Densitometry
,”
J. Clin. Densitom.
,
8
(
4
), pp.
371
378
.10.1385/JCD:8:4:371
55.
Oliviero
,
S.
,
Giorgi
,
M.
, and
Dall'Ara
,
E.
,
2018
, “
Validation of Finite Element Models of the Mouse Tibia Using Digital Volume Correlation
,”
J. Mech. Behav. Biomed. Mater.
,
86
, pp.
172
184
.10.1016/j.jmbbm.2018.06.022
56.
Hussein
,
A. I.
, and
Morgan
,
E. F.
,
2013
, “
The Effect of Intravertebral Heterogeneity in Microstructure on Vertebral Strength and Failure Patterns
,”
Osteoporos. Int.
,
24
(
3
), pp.
979
989
.10.1007/s00198-012-2039-1
57.
Eswaran
,
S. K.
,
Gupta
,
A.
, and
Keaveny
,
T. M.
,
2007
, “
Locations of Bone Tissue at High Risk of Initial Failure During Compressive Loading of the Human Vertebral Body
,”
Bone
,
41
(
4
), pp.
733
739
.10.1016/j.bone.2007.05.017
58.
Fields
,
A. J.
,
Lee
,
G. L.
, and
Keaveny
,
T. M.
,
2010
, “
Mechanisms of Initial Endplate Failure in the Human Vertebral Body
,”
J. Biomech.
,
43
(
16
), pp.
3126
3131
.10.1016/j.jbiomech.2010.08.002
59.
Shirazi-Adl
,
S. A.
,
Shrivastava
,
S. C.
, and
Ahmed
,
A. M.
,
1984
, “
Stress Analysis of the Lumbar Disc-Body Unit in Compression. A Three-Dimensional Nonlinear Finite Element Study
,”
Spine (Phila Pa 1976)
,
9
(
2
), pp.
120
134
.10.1097/00007632-198403000-00003
60.
Reiser
,
I.
, and
Glick
,
S.
,
2014
,
Tomosynthesis Imaging
,
CRC Press
,
Boca Raton, FL
.
61.
Rose
,
A.
,
1973
,
Vision: Human and Electronic
,
Plenum Press
,
New York and London
.
62.
Homminga
,
J.
,
Weinans
,
H.
,
Gowin
,
W.
,
Felsenberg
,
D.
, and
Huiskes
,
R.
,
2001
, “
Osteoporosis Changes the Amount of Vertebral Trabecular Bone at Risk of Fracture but Not the Vertebral Load Distribution
,”
Spine (Phila Pa 1976)
,
26
(
14
), pp.
1555
1560
.10.1097/00007632-200107150-00010
63.
Christiansen
,
B. A.
,
Kopperdahl
,
D. L.
,
Kiel
,
D. P.
,
Keaveny
,
T. M.
, and
Bouxsein
,
M. L.
,
2011
, “
Mechanical Contributions of the Cortical and Trabecular Compartments Contribute to Differences in Age-Related Changes in Vertebral Body Strength in Men and Women Assessed by QCT-Based Finite Element Analysis
,”
J. Bone Miner. Res.
,
26
(
5
), pp.
974
983
.10.1002/jbmr.287
64.
Samelson
,
E. J.
,
Christiansen
,
B. A.
,
Demissie
,
S.
,
Broe
,
K. E.
,
Louie-Gao
,
Q.
,
Cupples
,
L. A.
,
Roberts
,
B. J.
,
Manoharam
,
R.
,
D'Agostino
,
J.
,
Lang
,
T.
,
Kiel
,
D. P.
, and
Bouxsein
,
M. L.
,
2012
, “
QCT Measures of Bone Strength at the Thoracic and Lumbar Spine: The Framingham Study
,”
J. Bone Miner. Res.
,
27
(
3
), pp.
654
663
.10.1002/jbmr.1482
65.
Polikeit
,
A.
,
Nolte
,
L. P.
, and
Ferguson
,
S. J.
,
2004
, “
Simulated Influence of Osteoporosis and Disc Degeneration on the Load Transfer in a Lumbar Functional Spinal Unit
,”
J. Biomech.
,
37
(
7
), pp.
1061
1069
.10.1016/j.jbiomech.2003.11.018
66.
Hussein
,
A. I.
,
Mason
,
Z. D.
, and
Morgan
,
E. F.
,
2013
, “
Presence of Intervertebral Discs Alters Observed Stiffness and Failure Mechanisms in the Vertebra
,”
J. Biomech.
,
46
(
10
), pp.
1683
1688
.10.1016/j.jbiomech.2013.04.004
67.
Nazarian
,
A.
, and
Muller
,
R.
,
2004
, “
Time-Lapsed Microstructural Imaging of Bone Failure Behavior
,”
J. Biomech.
,
37
(
1
), pp.
55
65
.10.1016/S0021-9290(03)00254-9
You do not currently have access to this content.