Accurate individualized muscle architecture data are crucial for generating subject-specific musculoskeletal models to investigate movement and dynamic muscle function. Diffusion tensor imaging (DTI) magnetic resonance (MR) imaging has emerged as a promising method of gathering muscle architecture data in vivo; however, its accuracy in estimating parameters such as muscle fiber lengths for creating subject-specific musculoskeletal models has not been tested. Here, we provide a validation of the method of using anatomical magnetic resonance imaging (MRI) and DTI to gather muscle architecture data in vivo by directly comparing those data obtained from MR scans of three human cadaveric lower limbs to those from dissections. DTI was used to measure fiber lengths and pennation angles, while the anatomical images were used to estimate muscle mass, which were used to calculate physiological cross-sectional area (PCSA). The same data were then obtained through dissections, where it was found that on average muscle masses and fiber lengths matched well between the two methods (4% and 1% differences, respectively), while PCSA values had slightly larger differences (6%). Overall, these results suggest that DTI is a promising technique to gather in vivo muscle architecture data, but further refinement and complementary imaging techniques may be needed to realize these goals.

References

1.
Lieber
,
R. L.
, and
Fridén
,
J.
,
2000
, “
Functional and Clinical Significance of Skeletal Muscle Architecture
,”
Muscle Nerve
,
23
(
11
), pp.
1647
66
.
2.
Delp
,
S. L.
,
Loan
,
J. P.
,
Hoy
,
M. G.
,
Zajac
,
F. E.
,
Topp
,
E. L.
, and
Rosen
,
J. M.
,
1990
, “
An Interactive Graphics-Based Model of the Lower Extremity to Study Orthopaedic Surgical Procedures
,”
IEEE Trans Biomed Eng
,
37
(
8
), pp.
757
67
.
3.
Delp
,
S. L.
, and
Loan
,
J. P.
,
1995
, “
A Graphics-Based Software System to Develop and Analyze Models of Musculoskeletal Structures
,”
Comput. Biol. Med.
,
25
(
1
), pp.
21
34
.
4.
Hutchinson
,
J. R.
,
Anderson
,
F. C.
,
Blemker
,
S. S.
, and
Delp
,
S. L.
,
2005
, “
Analysis of Hindlimb Muscle Moment Arms in Tyrannosaurus Rex Using a Three-Dimensional Musculoskeletal Computer Model: Implications for Stance, Gait, and Speed
,”
Paleobiology
,
31
(
4
), pp.
676
701
.
5.
Delp
,
S. L.
,
Anderson
,
F. C.
,
Arnold
,
A. S.
,
Loan
,
P.
,
Habib
,
A.
,
John
,
C. T.
,
Guendelman
,
E.
, and
Thelen
,
D. G.
,
2007
, “
OpenSim: Open-Source Software to Create and Analyze Dynamic Simulations of Movement
,”
IEEE Trans Biomed Eng
,
54
(
11
), pp.
1940
1950
.
6.
Arnold
,
E. M.
,
Ward
,
S. R.
,
Lieber
,
R. L.
, and
Delp
,
S. L.
,
2010
, “
A Model of the Lower Limb for Analysis of Human Movement
,”
Ann. Biomed. Eng.
,
38
(
2
), pp.
269
279.
7.
O'Neill
,
M. C.
,
Lee
,
L. F.
,
Larson
,
S. G.
,
Demes
,
B.
,
Stern
,
J. T.
, and
Umberger
,
B. R.
,
2013
, “
A Three-Dimensional Musculoskeletal Model of the Chimpanzee (Pan troglodytes) Pelvis and Hind Limb
,”
J. Exp. Biol.
,
216
(
19
), pp.
3709
3723
.
8.
Rankin
,
J
,
Rubenson
,
J
, and
Hutchinson
,
J. R.
,
2016
, “
Inferring Muscle Functional Roles of the Ostrich Pelvic Limb During Walking and Running Using Computer Optimization
,”
J. R. Soc. Interface
,
13
(
118
).
9.
Charles
,
J. P.
,
Cappellari
,
O.
,
Spence
,
A. J.
,
Wells
,
D. J.
, and
Hutchinson
,
J. R.
,
2016
, “
Muscle Moment Arms and Sensitivity Analysis of a Mouse Hindlimb Musculoskeletal Model
,”
J. Anat.
,
229
(
4
), pp.
514
535
.
10.
Handsfield
,
G. G.
,
Meyer
,
C. H.
,
Hart
,
J. M.
,
Abel
,
M. F.
, and
Blemker
,
S. S.
,
2014
, “
Relationships of 35 Lower Limb Muscles to Height and Body Mass Quantified Using MRI
,”
J. Biomech.
,
47
(
3
), pp.
631
638
.
11.
Gerus
,
P.
,
Rao
,
G.
, and
Berton
,
E.
,
2012
, “
Subject-Specific Tendon-Aponeurosis Definition in Hill-Type Model Predicts Higher Muscle Forces in Dynamic Tasks
,”
PLoS One
,
7
(
8
), p.
e44406
.
12.
de Oliveira
,
L. F.
, and
Menegaldo
,
L. L.
,
2010
, “
Individual-Specific Muscle Maximum Force Estimation Using Ultrasound for Ankle Joint Torque Prediction Using an EMG-Driven Hill-Type Model
,”
J. Biomech.
,
43
(
14
), pp.
2816
21
.
13.
Scovil
,
C. Y.
, and
Ronsky
,
J. L.
,
2006
, “
Sensitivity of a Hill-Based Muscle Model to Perturbations in Model Parameters
,”
J. Biomech.
,
39
(
11
), pp.
2055
2063
.
14.
Ackland
,
D. C.
,
Lin
,
Y. C.
, and
Pandy
,
M. G.
,
2012
, “
Sensitivity of Model Predictions of Muscle Function to Changes in Moment Arms and Muscle-Tendon Properties: A Monte Carlo Analysis
,”
J. Biomech.
,
45
(
8
), pp.
1463
1471
.
15.
Valente
,
G.
,
Pitto
,
L.
,
Testi
,
D.
,
Seth
,
A.
,
Delp
,
S. L.
,
Stagni
,
R.
,
Viceconti
,
M.
, and
Taddei
,
F.
,
2014
, “
Are Subject-Specific Musculoskeletal Models Robust to the Uncertainties in Parameter Identification?
,”
PLoS One
,
9
(
11
), p.
e112625
.
16.
Navacchia
,
A.
,
Myers
,
C. A.
,
Rullkoetter
,
P. J.
, and
Shelburne
,
K. B.
,
2016
, “
Prediction of In Vivo Knee Joint Loads Using a Global Probabilistic Analysis
,”
ASME J. Biomech. Eng.
,
138
(
3
), p.
4032379
.
17.
Arnold
,
A. S.
,
Salinas
,
S.
,
Asakawa
,
D. J.
, and
Delp
,
S. L.
,
2000
, “
Accuracy of Muscle Moment Arms Estimated From MRI-Based Musculoskeletal Models of the Lower Extremity
,”
Comput. Aided Surg.
,
5
(
2
), pp.
108
119
.
18.
Modenese
,
L.
,
Ceseracciu
,
E.
,
Reggiani
,
M.
, and
Lloyd
,
D. G.
,
2016
, “
Estimation of Musculotendon Parameters for Scaled and Subject Specific Musculoskeletal Models Using an Optimization Technique
,”
J. Biomech.
,
49
(
2
), pp.
141
148
.
19.
Wu
,
W.
,
Lee
,
P. V.
,
Bryant
,
A. L.
,
Galea
,
M.
, and
Ackland
,
D. C.
,
2016
, “
Subject-Specific Musculoskeletal Modeling in the Evaluation of Shoulder Muscle and Joint Function
,”
J. Biomech.
,
49
(
15
), pp.
3626
3634
.
20.
Bolsterlee
,
B.
,
Veeger
,
H. E.
,
van der Helm
,
F. C.
,
Gandevia
,
S. C.
, and
Herbert
,
R. D.
,
2015
, “
Comparison of Measurements of Medial Gastrocnemius Architectural Parameters From Ultrasound and Diffusion Tensor Images
,”
J. Biomech.
,
48
(
6
), pp.
1133
1140
.
21.
Lee
,
D.
,
Li
,
Z.
,
Sohail
,
Q. Z.
,
Jackson
,
K.
,
Fiume
,
E.
, and
Agur
,
A.
,
2015
, “
A Three-Dimensional Approach to Pennation Angle Estimation for Human Skeletal Muscle
,”
Comput. Methods Biomech. Biomed. Eng.
,
18
(
13
), pp.
1474
1484
.
22.
Assaf
,
Y.
, and
Pasternak
,
O.
,
2008
, “
Diffusion Tensor Imaging (DTI)-Based White Matter Mapping in Brain Research: A Review
,”
J. Mol. Neurosci.
,
34
(
1
), pp.
51
61
.
23.
Chen
,
L.
,
Hu
,
X.
,
Ouyang
,
L.
,
He
,
N.
,
Liao
,
Y.
,
Liu
,
Q.
,
Zhou
,
M.
,
Wu
,
M.
,
Huang
,
X.
, and
Gong
,
Q.
,
2016
, “
A Systematic Review and Meta-Analysis of Tract-Based Spatial Statistics Studies Regarding Attention-Deficit/Hyperactivity Disorder
,”
Neurosci. Biobehav. Rev.
,
68
, pp.
838
847
.
24.
Eierud
,
C.
,
Craddock
,
R. C.
,
Fletcher
,
S.
,
Aulakh
,
M.
,
King-Casas
,
B.
,
Kuehl
,
D.
, and
LaConte
,
S. M.
,
2014
, “
Neuroimaging After Mild Traumatic Brain Injury: Review and Meta-Analysis
,”
Neuroimage Clin.
,
4
, pp.
283
94
.
25.
Soares
,
J. M.
,
Marques
,
P.
,
Alves
,
V.
, and
Sousa
,
N.
,
2013
, “
A Hitchhiker's Guide to Diffusion Tensor Imaging
,”
Front. Neurosci.
,
7
, p.
31
.
26.
Seif
,
M.
,
Lu
,
H.
,
Boesch
,
C.
,
Reyes
,
M.
, and
Vermathen
,
P.
,
2015
, “
Image Registration for Triggered and Non-Triggered DTI of the Human Kidney: Reduced Variability of Diffusion Parameter Estimation
,”
J. Magn. Reson. Imaging
,
41
(
5
), pp.
1228
1235
.
27.
Hsu
,
E. W.
,
Buckley
,
D. L.
,
Bui
,
J. D.
,
Blackband
,
S. J.
, and
Forder
,
J. R.
,
2001
, “
Two-Component Diffusion Tensor MRI of Isolated Perfused Hearts
,”
Magn. Reson. Med.
,
45
(
6
), pp.
1039
1045
.
28.
Hsu
,
E. W.
, and
Mori
,
S.
,
1995
, “
Analytical Expressions for the NMR Apparent Diffusion Coefficients in an Anisotropic System and a Simplified Method for Determining Fiber Orientation
,”
Magn. Reson. Med.
,
34
(
2
), pp.
194
200
.
29.
Damon
,
B. M.
,
Ding
,
Z.
,
Anderson
,
A. W.
,
Freyer
,
A. S.
, and
Gore
,
J. C.
,
2002
, “
Validation of Diffusion Tensor MRI-Based Muscle Fiber Tracking
,”
Magn. Reson. Med.
,
48
(
1
), pp.
97
104
.
30.
Deux
,
J. F.
,
Malzy
,
P.
,
Paragios
,
N.
,
Bassez
,
G.
,
Luciani
,
A.
,
Zerbib
,
P.
,
Roudot-Thoraval
,
F.
,
Vignaud
,
A.
,
Kobeiter
,
H.
, and
Rahmouni
,
A.
,
2008
, “
Assessment of Calf Muscle Contraction by Diffusion Tensor Imaging
,”
Eur. Radiol.
,
18
(
10
), pp.
2303
2310
.
31.
Heemskerk
,
A. M.
,
Sinha
,
T. K.
,
Wilson
,
K. J.
,
Ding
,
Z.
, and
Damon
,
B. M.
,
2010
, “
Repeatability of DTI-Based Skeletal Muscle Fiber Tracking
,”
NMR Biomed.
,
23
(
3
), pp.
294
303
.
32.
Sinha
,
U.
,
Sinha
,
S.
,
Hodgson
,
J. A.
, and
Edgerton
,
R. V.
,
2011
, “
Human Soleus Muscle Architecture at Different Ankle Joint Angles From Magnetic Resonance Diffusion Tensor Imaging
,”
J. Appl. Physiol.
,
110
(
3
), pp.
807
819
.
33.
Froeling
,
M.
,
Nederveen
,
A. J.
,
Heijtel
,
D. F.
,
Lataster
,
A.
,
Bos
,
C.
,
Nicolay
,
K.
,
Maas
,
M.
,
Drost
,
M. R.
, and
Strijkers
,
G. J.
,
2012
, “
Diffusion-Tensor MRI Reveals the Complex Muscle Architecture of the Human Forearm
,”
J. Magn. Reson. Imaging
,
36
(
1
), pp.
237
248
.
34.
Froeling
,
M.
,
Oudeman
,
J.
,
Strijkers
,
G. J.
,
Maas
,
M.
,
Drost
,
M. R.
,
Nicolay
,
K.
, and
Nederveen
,
A. J.
,
2015
, “
Muscle Changes Detected With Diffusion-Tensor Imaging After Long-Distance Running
,”
Radiology
,
274
(
2
), pp.
548
62
.
35.
Damon
,
B. M.
,
Froeling
,
M.
,
Buck
,
A. K.
,
Oudeman
,
J.
,
Ding
,
Z.
,
Nederveen
,
A. J.
,
Bush
,
E. C.
, and
Strijkers
,
G. J.
,
2017
, “
Skeletal Muscle Diffusion Tensor-MRI Fiber Tracking: Rationale, Data Acquisition and Analysis Methods, Applications and Future Directions
,”
NMR Biomed
,
30
(
3
), p. e3563.
36.
Sieben
,
J. M.
,
van Otten
,
I.
,
Lataster
,
A.
,
Froeling
,
M.
,
Nederveen
,
A. J.
,
Strijkers
,
G. J.
, and
Drost
,
M. R.
,
2016
, “
In Vivo Reconstruction of Lumbar Erector Spinae Architecture Using Diffusion Tensor MRI
,”
Clin. Spine Surg.
,
29
(
3
), pp.
E139
E145
.
37.
Bolsterlee
,
B.
,
Finni
,
T.
,
D'Souza
,
A.
,
Eguchi
,
J.
,
Clarke
,
E. C.
, and
Herbert
,
R. D.
,
2018
, “
Three-Dimensional Architecture of the Whole Human Soleus Muscle In Vivo
,”
PeerJ
,
6
, p.
e4610
.
38.
Mendez
,
J.
, and
Keys
,
A.
,
1960
, “
Density and Composition of Mammalian Skeletal Muscle
,”
Metabolism
,
9
(
2
), pp.
184
188
.https://eurekamag.com/research/024/450/024450136.php
39.
Wickiewicz
,
T. L.
,
Roy
,
R. R.
,
Powell
,
P. L.
, and
Edgerton
,
V. R.
,
1983
, “
Muscle Architecture of the Human Lower Limb
,”
Clin. Orthop. Relat. Res.
,
179
(
1
), pp.
275
283
.
40.
Ward
,
S. R.
,
Eng
,
C. M.
,
Smallwood
,
L. H.
, and
Lieber
,
R. L.
,
2009
, “
Are Current Measurements of Lower Extremity Muscle Architecture Accurate?
,”
Clin. Orthop. Relat. Res.
,
467
(
4
), pp.
1074
1082
.
41.
Ward
,
S. R.
, and
Lieber
,
R. L.
,
2005
, “
Density and Hydration of Fresh and Fixed Human Skeletal Muscle
,”
J. Biomech.
,
38
(
11
), pp.
2317
2320
.
42.
Jiang
,
H.
,
van Zijl
,
P. C.
,
Kim
,
J.
,
Pearlson
,
G. D.
, and
Mori
,
S.
,
2006
, “
DtiStudio: Resource Program for Diffusion Tensor Computation and Fiber Bundle Tracking
,”
Comput Methods Programs Biomed
,
81
(
2
), pp.
106
116
.
43.
Aja-Fernandez
,
S.
,
Niethammer
,
M.
,
Kubicki
,
M.
,
Shenton
,
M. E.
, and
Westin
,
C. F.
,
2008
, “
Restoration of DWI Data Using a Rician LMMSE Estimator
,”
IEEE Trans. Med. Imaging
,
27
(
10
), pp.
1389
1403
.
44.
Cook
,
P. A.
,
Bai
,
Y.
,
Nedjati-Gilani
,
S.
,
Seunarine
,
K. K.
,
Hall
,
M. G.
,
Parker
,
G. J.
, and
Alexander
,
D. C.
,
2006
, “
Camino: Open-Source Diffusion-MRI Reconstruction and Processing
,”
14th Scientific Meeting of the International Society for Magnetic Resonance in Medicine
, Seattle, WA, May 6–12, p. p2759.
45.
Yushkevich
,
P. A.
,
Piven
,
J.
,
Hazlett
,
H. C.
,
Smith
,
R. G.
,
Ho
,
S.
,
Gee
,
J. C.
, and
Gerig
,
G.
,
2006
, “
User-Guided 3D Active Contour Segmentation of Anatomical Structures: Significantly Improved Efficiency and Reliability
,”
Neuroimage
,
31
(
3
), pp.
1116
1128
.
46.
Schneider
,
C. A.
,
Rasband
,
W. S.
, and
Eliceiri
,
K. W.
,
2012
, “
NIH Image to ImageJ: 25 Years of Image Analysis
,”
Nat. Methods
,
9
(
7
), pp.
671
675
.
47.
Raiteri
,
B. J.
,
Cresswell
,
A. G.
, and
Lichtwark
,
G. A.
,
2016
, “
Three-Dimensional Geometrical Changes of the Human Tibialis Anterior Muscle and Its Central Aponeurosis Measured With Three-Dimensional Ultrasound During Isometric Contractions
,”
PeerJ
,
4
, p.
e2260
.
48.
Zajac
,
F. E.
,
1989
, “
Muscle and Tendon: Properties, Models, Scaling, and Application to Biomechanics and Motor Control
,”
Crit. Rev. Biomed. Eng.
,
17
(
4
), pp.
359
411
.http://e.guigon.free.fr/rsc/article/Zajac89.pdf
49.
Narici
,
M. V.
,
Maganaris
,
C. N.
,
Reeves
,
N. D.
, and
Capodaglio
,
P.
,
2003
, “
Effect of Aging on Human Muscle Architecture
,”
J. Appl. Physiol.
,
95
(
6
), pp.
2229
2234
.
50.
Cutts
,
A.
,
1988
, “
The Range of Sarcomere Lengths in the Muscles of the Human Lower Limb
,”
J. Anat.
,
160
, pp.
79
88
.https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1262051/pdf/janat00172-0084.pdf
51.
Chen
,
X.
, and
Delp
,
S. L.
,
2016
, “
Human Soleus Sarcomere Lengths Measured Using In Vivo Microendoscopy at Two Ankle Flexion Angles
,”
J. Biomech.
,
49
(
16
), pp.
4164
4167
.
52.
Chen
,
X.
,
Sanchez
,
G. N.
,
Schnitzer
,
M. J.
, and
Delp
,
S. L.
,
2016
, “
Changes in Sarcomere Lengths of the Human Vastus Lateralis Muscle With Knee Flexion Measured Using In Vivo Microendoscopy
,”
J. Biomech.
,
49
(
13
), pp.
2989
2994
.
53.
Yanagisawa
,
O.
,
Kurihara
,
T.
,
Kobayashi
,
N.
, and
Fukubayashi
,
T.
,
2011
, “
Strenuous Resistance Exercise Effects on Magnetic Resonance Diffusion Parameters and Muscle-Tendon Function in Human Skeletal Muscle
,”
J. Magn. Reson. Imaging
,
34
(
4
), pp.
887
894
.
You do not currently have access to this content.