We aimed to investigate the association between mobility and skeletal muscle strength by using magnetic resonance diffusion tensor imaging (DTI). This study included 20 healthy male volunteers (mean age, 21.8 ± 1.1 years). The maximum voluntary strength (MVC) of each participant was measured with the ankle joint in plantar and dorsal flexion using an instrument for measuring muscle strength. Moreover, magnetic resonance imaging (MRI) was performed with the ankle joint at rest, in plantar flexion, and in dorsal flexion. For imaging, a 1.5-T MRI device was used, and a diffusion-weighted stimulated echo-planar imaging pulse sequence. Tensor eigenvalues (λ), fractional anisotropy (FA), and the apparent diffusion coefficient (ADC) were calculated from data obtained by DTI. The resulting MRI data were compared to the data on muscle mobility or strength and statistically analyzed. Regarding changes in DTI indices during muscle movements, anisotropy of the tibialis anterior was significantly increased from rest to plantar flexion (P < 0.01), whereas no significant change was observed in dorsal flexion (n.s.). In contrast, the extent of significant changes in anisotropy of the medial gastrocnemius (mGC) and soleus (SOL) was small at plantar flexion (mGC, P < 0.01; SOL, n.s.), whereas the indices were significantly increased at dorsal flexion (P < 0.01). Regarding the correlation between MVC of each skeletal muscle and the DTI indices, FA and λ3 were significantly correlated in movements involving the muscles, whereas no significant correlation was observed in movements not involving them. Changes in intramuscular water molecules by elongation and contraction of the skeletal muscle fibers could be assumed to affect changes in diffusional anisotropy. When muscles contract, the space between myocytes was reduced and they might become increasingly dense. Moreover, diffusional anisotropy increased with increasing MVC, whereas ADC remained unchanged. DTI was suggested to produce measurements similar to the degree of muscle strength.
Diffusion tensor imaging (DTI) is a technique that allows calculation of the diffusion direction of water molecules into the body [
The skeletal muscles are directly associated with quality of life (QOL) and activities of daily living (ADL) and comprise a medically important organ that is affected by age-related disease and mobility impairments. Assessments of the skeletal muscles are considered important in the field of sports medicine. Various methods used to assess the skeletal muscles include electromyography, muscle biopsy, ultrasonography, computed tomography (CT), and magnetic resonance imaging (MRI). In particular, MRI is attracting increasing attention as a modality that allows noninvasive three-dimensional assessment. Many studies of the skeletal muscles using MRI have been reported, including assessments of muscle morphology [
Studies using DTI on skeletal muscles include many reports on the assessment of muscle morphology, whereas few have examined muscle function. The motor function of the skeletal muscles is associated with contraction and relaxation of muscle fibers, in other words, changes in muscle fiber structure. The ability to measure muscle morphology with DTI suggests that muscle function can also be assessed by a detailed assessment of the measurements. In 2005, Heemskerk et al., who studied mice, reported that the physiological cross-sectional area (PCSA) and λ3 of the skeletal muscles were in a proportional relationship [
In the present study of healthy volunteers, we measure fluctuations in DTI indices during skeletal muscle contraction and relaxation using DTI and also aim to reveal the correlation between the indices and muscle strength.
The present study was approved by the ethics committee of our institution and included 20 healthy adult male volunteers who received a sufficient explanation of the experiment and provided informed consent. The subjects for the experiment were chosen using a bulletin board inside the college. Their characteristics were as follows: age, 21.8 ± 1.1 years (mean ± standard deviation); height, 1.72 ± 0.05 m; weight, 59.4 ± 7.8 kg; and body mass index (BMI), 20.0 ± 5.1 kg/m2. The imaging sites were the skeletal muscles of the lower leg (tibialis anterior [TA], soleus [SOL], and medial gastrocnemius [mGC]). The inclusion criteria were no current or previous treatment for any disorder of the sites and no regular exercise. The study period took three months to scan MRI and two months for analysis.
1) Exercise tolerance
The participants lay in the supine position with the knee joints completely extended for MRI, and the exercise positions included the ankle joint at rest, dorsal flexion, and plantar flexion. For MRI of the ankle joint at dorsal and plantar flexion, the ankle joint was held at 50% maximum voluntary contraction (MVC). Moreover, MVC was measured prior to imaging. During exercise, the distal portion of the knee joint and the proximal portion of the ankle joint were fixed to prevent the imaging sites from departing from the predetermined imaging range. MRI and measurement of the MVC were performed with the participants in the same posture by the same fixation. For the measurement, we used a custom made myodynamometer for the lower leg that we developed from a Molten-made digital myodynamometer for the lower limb.
2) MR imaging
For MRI, a 1.5-Tesla magnetic resonance scanner (Signa Horizon Lx Ver. 9.0; General Electric Healthcare, Tokyo, Japan) and knee coil (General Electric Healthcare) were used. On this device, the maximum magnetic field gradient amplitude is 22 mT/m, while the maximum slew rate is 77 mT/m/m. The imaging range of the lower leg was an area around the greatest diameter of the lower leg.
For the DTI pulse sequence, we used the single-shot diffusion-weighted stimulated-echo echo-planar imaging (DW-STE EPI) pulse sequence that we had independently developed (
The imaging parameters used in the present study were as follows: repetition time (TR)/echo time (TE)/mix- ing time (TM), 4000/44.1/208.2 ms; Δ/δ, 225.9/11.4; b-value, 800 s/mm2; number of excitations (NEX), 8; field of view (FOV), 240 × 240 mm2; matrix size, 128 × 128; number of slices, 6; slice thickness, 8 mm with no gap; motion probing gradient (MPG) moment, six axes (xy, xz, yz, −xy, −xz, −yz); and total DW-STE scanning time, 224 s. To determine the anatomical locations of the skeletal muscles, T1-spoiled gradient recalled acquisition in the steady state (SPGR) was used. The parameters were as follows: TR/TE, 20/5 ms; frip angle, 40˚; NEX, 1; FOV, 240 × 240 mm2; matrix size, 128 × 128; number of slices, 5; and slice thickness, 8 mm with no gap. The slice center was set at the greatest diameter of the lower leg on the sagittal localized images.
3) Diffusion tensor processing
Imaging data were processed by a free software provided by the University of Tokyo (dTV2, currently unavailable). Tensor analysis of the signals of each vector component yielded three eigenvalues corresponding to the axes of the tensor ellipsoid (λ1, λ2, and λ3). From these eigenvalues, the apparent diffusion coefficient (ADC) was calculated using the following equation [
The fractional anisotropy (FA) was calculated using the following equation [
While TA, mGC, and SOL in the imaged lower leg were targeted for measurement, the regions of interest (ROI) were carefully selected on T1-weighted SPGR images (
4) Statistical processing
To test for significant differences in changes in the DTI indices due to muscle movement, the nonparametric Wilcoxon signed-rank test was performed with a significance level of 5%. Moreover, to test for correlations between MVC and DTI indices of the lower leg, the nonparametric Spearman rank correlation coefficient test was performed with a significance level of 5%.
Changes in the DTI indices of the skeletal muscles of the lower leg with the ankle joint positioned at dorsal flexion and rest.
The DTI indices were measured when the ankle joint was positioned at dorsal flexion and rest (
FA | λ1 | λ2 | λ3 | ADC | ||
---|---|---|---|---|---|---|
TA | Dorsal flexion | 0.027 | 0.0001 | 0.0001 | 0.0008 | 0.89 |
Plantar flexion | 0.62 | 0.82 | 0.89 | 0.91 | 0.0001 | |
mGM | Dorsal flexion | 0.004 | 0.64 | 0.004 | 0.006 | 0.0001 |
Plantar flexion | 0.0001 | 0.0004 | 0.00008 | 0.00008 | 0.007 | |
SOL | Dorsal flexion | 0.052 | 0.026 | 0.73 | 0.76 | 0.0001 |
Plantar flexion | 0.001 | 0.0002 | 0.0001 | 0.0001 | 0.21 |
In TA, FA (−3.95%, P < 0.05) was significantly decreased, whereas λ1 (9.66%, P < 0.01), λ2 (10.5%, P < 0.01), λ3 (13.1%, P < 0.01), and ADC (9.57%, P < 0.01) were significantly increased. All of the DTI indices were significantly changed. In the mGC, FA (4.25%, P < 0.01) was significantly increased, whereas λ2 (−3.14%, P < 0.01), λ3 (−3.70%, P < 0.01), and ADC (−1.61%, P < 0.01) were significantly decreased. No significant change was observed in λ1 (0.248%, n.s.). In the SOL, λ1 (1.46%, P < 0.05) was significantly increased, whereas no significant change was observed in FA (3.052%, n.s.), λ2 (−0.75%, n.s,), λ3 (−0.93%, n.s.), and ADC (0.00%, n.s.).
Changes in the DTI indices of the skeletal muscles of the lower leg with the ankle joint positioned at plantar flexion and rest.
The DTI indices were measured with the ankle joint positioned at plantar flexion and rest (
The TA showed no significant change in any of the DTI indices, namely FA (−0.96%, n.s.), λ1 (−1.00%, n.s.), λ2 (0.20%, n.s.), λ3 (−0.03%, n.s.), and ADC (−0.50%, n.s.). In the mGC, FA (−11.5%, P < 0.01) was significantly decreased, whereas λ1 (10.9%, P < 0.01), λ2 (20.6%, P < 0.01), λ3 (23.9%, P < 0.01), and ADC (16.7%, P < 0.01) were significantly increased. Significant changes were observed in all of the DTI indices. In the SOL, FA (−6.15%, P < 0.01) was significantly decreased, whereas λ1 (17.4%, P < 0.01), λ2 (21.8%, P < 0.01), λ3 (22.9%, P < 0.01), and ADC (19.7%, P < 0.01) were significantly increased. Significant changes were observed in all of the DTI indices.
Association between Skeletal Muscle Strength of the Lower Leg and the DTI IndicesThe MVC and DTI indices of the leg were compared and assessed. Statistical analysis (
FA | λ1 | λ2 | λ3 | ADC | ||
---|---|---|---|---|---|---|
TA | Dorsal flexion | 0.7 | 0.11 | 0.04 | 0.67 | 0.31 |
Plantar flexion | 0.23 | 0.19 | 0.12 | 0.45 | 0.33 | |
mGM | Dorsal flexion | 0.17 | 0.36 | 0.16 | 0.32 | 0.33 |
Plantar flexion | 0.47 | 0.02 | 0.01 | 0.44 | 0.19 | |
SOL | Dorsal flexion | 0.62 | 0.17 | 0.22 | 0.56 | 0.32 |
Plantar flexion | 0.78 | 0.05 | 0.23 | 0.59 | 0.3 |
revealed that, in the TA at dorsal flexion, MVC was significantly correlated with FA (r = 0.701, P < 0.01) and λ3 (r = 0.675, P < 0.01) but not with λ2, λ3, and ADC. In the TA at plantar flexion, a significant difference was observed in λ3; however, no significant correlation was obtained with any other DTI index. In the mGC at dorsal flexion, no significant correlation was obtained with any of the DTI indices. In the mGC at plantar flexion, a significant correlation was observed with FA (r = 0.478, P < 0.05) and λ3 (r = 0.447, P < 0.05) but not with λ2, λ3, or ADC. In the SOL at dorsal flexion, a significant correlation was observed with FA (r = 0.625, P < 0.01) and λ3 (r = 0.560, P < 0.05) but not with λ2, λ3, or ADC. Likewise, in the SOL at plantar flexion, a significant correlation was observed with FA (r = 0.784, P < 0.01) and λ3 (r = 0.600, P < 0.05) but not with λ2, λ3, or ADC.
Although MRI is mainly used for morphological measurements, its use for functional measurement has also attracted attention in recent years. We focused here on DTI, a technique that allows the measurement of diffusional anisotropy of water molecules. Among the skeletal muscle movements, contractions in which they actively shorten and exert force to the outside world are called concentric contractions. In the present study, we aimed to investigate the association between muscle contraction and tension resulting from this movement with measurements taken using DTI.
A lot of studies in neural area using DTI were reported, because DTI is quantitatively possible to evaluate the micro structure. By way of example, it is also used for supporting brain tumor resection surgery, which has high accuracy [
1) Changes in DTI indices due to muscle contractions
The involved skeletal muscles vary among muscle movements. While the major muscles involved in plantar flexion, the gastrocnemius and SOL, were targeted in the present study, the major muscle involved in dorsal flexion is the TA. We performed DTI while these two opposing movements were performed. The fibrous cells of the skeletal muscles, called muscle fibers, measure 10 - 150 μm in diameter and are several centimeters to several tens of centimeters in length. Muscle fibers are specialized and contain special structures for contraction. Their minimal functional unit is a contraction unit called a sarcomere, which consists of proteins called myosin and actin that slide past each other (contract) to exert tension [
Our experiment showed markedly significant differences in the indices of the involved muscles between at rest and at flexion (
2) Association between muscle tension and DTI indices
In the present study, MVC was compared to DTI indices at rest. As a result, volunteers with a higher MVC showed a higher FA and a lower λ3. MVC was significantly correlated with FA and λ3 (
PCSA is defined as the total sum of the cross-sectional areas of muscle fibers and calculated by dividing muscle volume by muscle fiber length. There is also a report that PCSA was directly calculated by measuring contiguous cross-sections obtained by MRI [
3) Advantages and limitations
This study found a correlation between the muscle function (contraction and force) and DTI indices. Thereby, not only the structure, it was arrow for us to evaluate the motor function of muscle. Muscle function evaluation is using a dynamometer and exercise test. However, a lot of measurement biases are mixed in this test, such as conditions and environment at the time of measurement. The method in this study has a potential to evaluate the motion and the function quantitatively, which removed biases as much as possible. Skeletal muscle is a locomotorium, so the organ is changing the form at the time of the measurement state. In other words, skeletal muscle is a very important dynamic measurement. However, the method takes a few minutes for measurement so dynamic measurement is difficult. Thus, it is necessary for skeletal muscle dynamic measurement to develop the technologies such as the compressed sensing technique, which makes it possible to omit the k-space [
This study’s findings suggest that skeletal muscle contractions and tension can be assessed by measuring muscle fiber contraction, muscle tension, and restricted diffusion of water molecules based on DTI indices. DTI allows not only measurements of traditionally used anatomical and morphological features but also the assessment of the functional aspects of muscles. Thus, this technique can be expected to be useful for not only disease evaluation but also the field of sports medicine.
This work was supported by Japanese Ministry of Education, Culture, Sports, Science, and Technology Grant- in-Aid for Young Scientists (B) No. 26860982, 2014.
JunichiHata,HaruyukiNagata,KazukiEndo,YujiKomaki,MasakazuSato,TomokazuNumano,KazuoYagi, (2015) Assessment of Human Skeletal Muscle Contraction and Force by Diffusion Tensor Imaging. Open Journal of Radiology,05,189-198. doi: 10.4236/ojrad.2015.54026