Valentina Mazzoli1,2,3, Jos Oudeman1, Marco A Marra3, Klaas Nicolay2, Nico Verdonschot3, Andre M Sprengers3, Martijn Froeling4, Aart J Nederveen1, and Gustav J Strijkers5
1Department of Radiology, Academic Medical Center, Amsterdam, Netherlands, 2Biomedical NMR, Department of Biomedical Engineering, Eindhoven University of Technology, Eindhoven, Netherlands, 3Orthopaedic Research Lab, Radboud University Medical Center, Nijmegen, Netherlands, 4Department of Radiology, University Medical Center, Utrecht, Netherlands, 5Biomedical Engineering and Physics, Academic Medical Center, Amsterdam, Netherlands
Synopsis
The
aim of this study is to explore Diffusion Tensor Imaging in the assessment of
passive muscle elongation. We investigated two dorsiflexor and two plantarflexor
muscles of the lower leg with the foot in dorsiflexion, neutral and plantarflexion
position. Significant negative correlation was found between changes in
fiberlength caused by passive muscle lengthening and radial diffusivity for all
muscles. Furthermore the rate of change in radial diffusivity was compatible
with a cylindrical model with constant volume. These findings give more insight
into diffusion mechanisms in skeletal muscles and are highly relevant for
biomechanical models.Introduction
Mechanisms of
muscle contraction and force generation in healthy subjects and patients with
muscle disorders is an intensely studied topic and relevant for numerous
clinical applications.
Diffusion Tensor Imaging offers unique
opportunities as it provides both architectural parameters as well as
information on tissue status. DTI in skeletal muscle has been shown to be
sensitive to transient effects including joint positioning as well as fiber
lengthening and shortening [1]. Increased water diffusion perpendicular to the
axis of the fiber was reported in the soleus and gastrocnemius muscle during
plantarflexion and this was empirically explained with an increase in muscle
cross sectional area, although no connections were made between changes in
fiberlength and diffusion coefficients. Understanding this connection could be
useful for a better modeling of muscle (patho)physiology.
The aim of this study is to investigate the
relationship between changes in diffusion parameters and fiberlength in the
lower leg as a result of muscle shortening/lengthening in passive stretch.
Materials and Methods
The right lower leg
of 5 male healthy volunteers (27±2 years) was scanned using a 3T Philips
Achieva scanner. A custom-built device was used to fixate the foot in 3
different positions (15° dorsiflexion, neutral and 30° plantarflexion). A
SE-EPI DTI scan with the following parameters was used: FOV: 192x156 mm2;
TE/TR: 51.63/11191 ms; matrix size: 64x52; 50 slices; voxel size: 3x3x5 mm3;
12 diffusion encoding directions; b-value: 400s/mm2. Each measurement
was performed twice on the same subject within the same measurement day.
A mDixon scan was
performed for each foot position and used for anatomical reference. Four
different muscle groups were segmented from the out-of-phase scan: soleus
(SOL), extensor digitorum longus (EDL), fibularis longus (FL) and tibialis
anterior (TA).
The DTI data were
fitted to a tensor model using a WLLS algorithm, and diffusion parameters (λ1,
FA and RD=(λ2+λ3)/2) were calculated.
Fiberlength was
calculated after automatic tendon segmentation, using a method previously
described [2].
Changes in length
and diffusion parameters are expressed as relative change with respect to the
neutral position (ΔXdorsi=Xdorsi-Xneutral and ΔXplantar=Xplantar-Xneutral).
Next, muscle fibers
were modeled as cylinders with constant volume. In order to test the model, percentage
changes in the square of fiber radius calculated from the change in fiberlength
were correlated with measured percentage changes in radial diffusivity (according
to Einstein’s equation of diffusion r2=2Dt).
Results
Figure 1 shows the
relative changes in length and diffusion parameters in dorsiflexion and plantarflexion,
with respect to neutral foot position.
Significant
(p<0.02) negative correlation was found between Δfiberlength and ΔRD for all
the investigated muscles (Table 1). On the other hand, no significant changes in
diffusivities were observed in the axial direction (λ
1). ΔFA showed significant
positive correlation with change in fiberlength for all muscles except the
EDL.
The square of the
change in fiber radius is seen to significantly correlate with change in radial
diffusion for all muscles (Figure 2 and
Table 2).
Discussions
Our results show
significant negative correlations in all investigated muscles between the
changes in RD and the changes in fiberlength with respect to neutral foot
position. The general change in fiberlength from dorsiflexion to plantarflexion
position is in agreement with results previously obtained using ultrasonography[3].
Different muscles showed different rate of change in fiberlength and diffusion
parameters. In particular it was observed that plantarflexor muscles (SOL and FL) lengthened in dorsiflexion and decreased their radial diffusivity, while the opposite
behavior was observed for the dorsiflexor muscles (EDL and TA).
On the other hand, λ1 did not show significant changes
with foot positions, indicating that intracellular proteins and other barriers that
hinder diffusion of water molecules in the axial direction are not influenced
by the change in length of the structure.
The rate of change
in diffusivity perpendicular to the fiber is in agreement with expected changes
in the square of the radius, indicating that in first approximation muscle
fibers can be adequately described by a simple cylindrical model and that
changes in RD can be used to predict changes in fiberlength. In fact
assuming a cylindrical model and using Einstein’s equation, we obtain that the
product between the diffusivity and the length is constant.
Taken together, our
data shows that DTI is a valuable tool in the assessment of muscle passive elongation
and shortening, and suggest that RD could
be used in the assessment of muscle functioning and abnormalities. These
findings advance the physiological interpretation of diffusion coefficients
derived from the tensor model and could potentially have an important role in
biomechanical models of muscle functioning.
Acknowledgements
No acknowledgement found.References
[1]
N. Schwenzer et al, NMR Biomed. 22 (2009) 1047–1053.
[2]
J. Oudeman et al, Proc Intl Soc Mag
Reson Med 22. Volume 22; 2014:3580.
[3] C. N. Maganaris et al, J.
Physiol. 1998; 512(Pt 2): 603–614.