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Research Papers

Magnetic Resonance Imaging Assessment of Mechanical Interactions Between Human Lower Leg Muscles in Vivo

[+] Author and Article Information
Cengizhan Ozturk

Institute of Biomedical Engineering,
Boğaziçi University,
Istanbul 34342, Turkey

Peter A. Huijing

Research Instituut ‘Move’ Faculteit Bewegingswetenschappen,
Vrije Universiteit,
Amsterdam 1082, The Netherlands

Can A. Yucesoy

Institute of Biomedical Engineering,
Boğaziçi University,
Istanbul 34342, Turkey
e-mail: can.yucesoy@boun.edu.tr

1Corresponding author.

Contributed by the Bioengineering Division of ASME for publication in the JOURNAL OF BIOMECHANICAL ENGINEERING. Manuscript received September 21, 2012; final manuscript received May 7, 2013; accepted manuscript posted May 16, 2013; published online July 10, 2013. Assoc. Editor: Brian D. Stemper.

J Biomech Eng 135(9), 091003 (Jul 10, 2013) (9 pages) Paper No: BIO-12-1424; doi: 10.1115/1.4024573 History: Received September 21, 2012; Revised May 07, 2013; Accepted May 16, 2013

Evidence on epimuscular myofascial force transmission (EMFT) was shown for undissected muscle in situ. We hypothesize that global length changes of gastrocnemius muscle-tendon complex in vivo will cause sizable and heterogeneous local strains within all muscles of the human lower leg. Our goal is to test this hypothesis. A method was developed and validated using high-resolution 3D magnetic resonance image sets and Demons nonrigid registration algorithm for performing large deformation analyses. Calculation of strain tensors per voxel in human muscles in vivo allowed quantifying local heterogeneous tissue deformations and volume changes. After hip and knee movement (Δ knee angle ≈ 25 deg) but without any ankle movement, local lengthening within m. gastrocnemius was shown to occur simultaneously with local shortening (maximally by +34.2% and −32.6%, respectively) at different locations. Moreover, similar local strains occur also within other muscles, despite being kept at constant muscle-tendon complex length. This is shown for synergistic m. soleus and deep flexors, as well as for antagonistic anterior crural and peroneal muscle groups: minimum peak lengthening and shortening equaled 23.3% and 25.54%, respectively despite global isometric conditions. These findings confirm our hypothesis and show that in vivo, muscles are in principle not independent mechanically.

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Figures

Grahic Jump Location
Fig. 1

Schematic of the leg and trunk within the MRI instrument. (a) Undeformed state. The body is prone on a table (solid line) that is can be moved in and out of the bore of the MRI machine. MRI compatible ankle-foot orthosis (see inset for a picture) was used to fix the ankle angle at 90°, in such a way to leave a small space between posterior side of the lower leg and the ankle-foot orthosis and also between anterior side of the lower leg and MR patient table to avoid exertion of other external forces. The ankle-foot orthosis was secured onto the patient table using support material. The tips of the toes were not allowed to contact the bore of the MRI machine in order to prevent the foot from being loaded mechanically. (b) The deformed state. The trunk of the subject is now supported and brought as close as possible to the bore wall. This creates movement in hip as well as knee joints, but leaves the lower leg in a similar position. In any case the ankle angle is unchanged.

Grahic Jump Location
Fig. 2

Examples of MR images of the lower leg. (a) Longitudinal image of the lower leg representing a sagittal slice illustrating the locations of the group of cross-sectional slices (white solid rectangle) to be analyzed for strains. For all subjects, the most proximal cross-sectional slice of the slice group was located at the upper third of the imaged portion of the lower leg, a level corresponding to the mid-belly of m. gastrocnemius. The white dashed rectangle encloses the group of cross-sectional slices on which the method was tested by imposing known deformations on m. gastrocnemius. Strains induced as a result of this test were analyzed only for the group of cross-sectional slices enclosed by white solid rectangle for which deformations were maximal. (b) An example of a cross-sectional image of the slice group with anatomical identification of muscles or muscle groups and bones (tibia and fibula). Five anatomical regions of interest were distinguished: m. gastrocnemius, m. soleus, deep flexor muscles, peroneal muscles, and anterior crural muscles. The dashed horizontal line indicates the location of sagittal image shown in (a).

Grahic Jump Location
Fig. 3

Typical example of a validity test: Comparison of known imposed deformations and those calculated using Demons algorithm. (a) and (b) Known deformations imposed artificially as shown on cross-sectional and sagittal images, respectively. The white horizontal line in (a) denotes the location of sagittal images shown in (b) and (d). (c) and (d) Corresponding deformations detected using Demons algorithm by comparing original (undeformed) and artificially deformed images. Deformations were visualized on a grid at certain pixel intervals (7 × 11 pixels, for better visualization of the combined image and grid). Note that deformations are found exclusively within gastrocnemius muscle (i.e., the only location where they had been imposed). (e) Strain errors higher than actually imposed strains are mapped (scaled according to the color grayscale bar on the right). The errors occur particularly at the boundary of deformed and undeformed volumes. The white curve indicates the peak error (7.88%) occurring at the boundary. For the enlarged part of this curve (f), the decrease in error as a function of distance in voxels is shown in graph (inset g). Note that within three voxels, the error decreased below the mean error in deformed volume. The thick white dashed lines (perimeter) delimit the regions of interest within the image and thin white dashed lines separate deformed m. gastrocnemius from the remaining volume. The vertical arrow between (b) and (d) indicates the location of the slice group for which deformations and strains were analyzed due to changing knee angle.

Grahic Jump Location
Fig. 4

A typical example of deformations calculated as caused by changing joint angles. (a) A cross-sectional slice acquired in the undeformed state. A regular grid (made up of lines connecting voxel group centers) is imposed on the image at certain pixel intervals (7 × 11 pixels) for better visualization. (b) The corresponding slice acquired in the deformed state. Using Demons algorithm, displacement fields are calculated. Based on these displacement fields, the regular grid in (a) is deformed. Such deformed grid is imposed on this image.

Grahic Jump Location
Fig. 5

Effect of altered knee angle: Local lengthening and shortening effects (first and third principal strain). Box and whisker plots: The horizontal line inside each box represents the median strain value; the upper and lower edges of each box itself represent upper and lower quartiles respectively (i.e., the 75th and 25th percentiles), and lines extending from each end of the box (whiskers) indicate the peak values of the principal strains plotted. Interquartile ranges (IQR i.e., absolute value of the difference between upper and lower quartiles) were considered as a measure of strain heterogeneity within each anatomical region. Data were represented per anatomical region of interest (muscle or muscle group) and analyzed across all subjects.

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