Electromechanical Delay from Mechanomyography in Long-Term Strength Trained Men

JEPonline

Sérgio Luiz Ferreira Andrade, Gabriel Hunzicker Skiba, Eddy Krueger, André Luiz Félix Rodacki

Motor Behavior Studies Center, Federal University of Parana, Curitiba, Parana, Brazil

ABSTRACT

Andrade SF, Krueger E, Hunzicker G, Rodacki AF. Electromechanical Delay from Mechanomyography in Long-Term Strength Trained Men. JEPonline 2016;19 (3):110-119. The purpose of this study was to compare the electromechanical delay (EMD) between long-term strength trained and untrained subjects using the mechanomyographic (MMG) response of electrically evoked contractions. Twenty-two men (age 24.7 ± 3.1, body mass 68 ± 14.16 kg, height 1.73 ± 0.06 m) were assigned to a long-term trained group (TRE) and a non-trained (NOT) group. The tibial nerve was stimulated with eight progressive pulses to evoke mechanical responses in the soleus muscle. The onset of the mechanical activity was recorded from accelerometry for EMD calculations. No significant differences (P>0.05) were found between TRE and NOT for Δt EMG-MMG (14.10 ± 6.65 ms and 14.15 ± 6.08 ms), Δt Stim-MMG (25.58 ± 7.0 ms and 24.70 ± 6.64 ms), Stim-MMG NORM (2.24 ± 0.57 a.u. and 2.36 ± 0.56 a.u.), and MMGPEAK (10.75 ± 9.87 mG and 17.30 ± 18.98 mG). The results suggest that the delay of the mechanical response of the soleus may not be sensitive to long-term strength training.

Key Words: Electromechanical Delay, Mechanomyography, Electromyography, Strength Training

INTRODUCTION

Neural adaptations promoted by strength training (ST) at the central nervous system have been demonstrated to result in an increased rate of force development (1,29). This is important since the time needed to build-up force within the muscles plays an important role in stabilizing the joints during rapid tasks and, thus allows for responding to balance perturbations (36). Also, peripheral adaptations have a major influence on the onset of force production (21).

Although electromyography (EMG) has been widely used to investigate training-induced changes in the pattern of motor unit recruitment, as result of central drive adjustments (7), 2 EMG analysis relies solely on the detected summation of action potentials. Hence, EMG cannot provide information about the peripheral adaptations in the muscle’s mechanical properties (e.g., muscle-tendon complex stiffness) or the dimensional changes (i.e., lateral thickening) that occur during the onset of a contraction (9,19).

Mechanomyography (MMG) is a non-invasive measure of the low-frequency vibrations caused by oscillations of the muscle fibers during a contraction (9). The MMG data are collected with specific transducers (e.g., accelerometer) attached to the skin surface over the muscle to detect the pressure waves propagating through the subcutaneous tissues. It is believed that MMG allows for locally exploring the underpinning events of force production to a larger extent than conventional EMG analysis (4). The MMG analysis has also been proposed to reflect motor unit coding (2), which makes it a cheap, complimentary tool to investigate the mechanical characteristics of muscle contractions (12-14).

One field of application of MMG is the analysis of the electromechanical delay (EMD) (10). The EMD depicts a measure of the time delay between the electrical stimulus of a motor neuron (i.e., EMG) and the onset of muscle contraction. This latency period has been demonstrated to indicate several factors, such as the mechanical properties of the series elastic components (SEC), the time course of propagation of the action potential throughout the muscle membrane, the excitation-contraction coupling process, and the stretching of the SEC in the contractile apparatus (8). This information has important applications to the efficiency and safety of performing some rapid skills, which depend on the latency between muscle activation and the onset of force output. For example, during the early phase of explosive actions, a longer EMD of the hamstrings relative to the quadriceps muscles might render the knee unstable and prone to injury (18).

Current research on the effects of ST on EMD are scarce and conflicting (16). Costa and colleagues (11) found no changes in the EMD after 3 days of dynamic resistance training. Other studies (17) also reported no changes in neuromuscular performance of reflex contractions after 16 wks of ST. Only one study found EMD decreases after 12 wks of isometric training (25). It could be argued that the discrepancy between studies may be related to the short period of training and methodological detection procedures (e.g., accelerometers or microphones) of the mechanical activity of the muscle. Therefore, this study aimed to determine the EMD from MMG signal analysis between long-term strength trained and untrained young male subjects. It was hypothesized that long-term strength trained subjects display shorter EMD latencies than their untrained counterparts.

METHODS Subjects Twenty-two healthy volunteers provided written informed consent prior joining the study, which was approved by the local institutional review board and in conformity with Helsinki Declaration of 1975, as revised in 1983. Exclusion criteria included recent history of injury, musculoskeletal pathology, and use of prescription medications. Subjects were assigned to a trained group (TRE, n = 11; age, 25.4 ± 3.7 yrs; body mass, 85.2 ± 9.4 kg; height, 1.76 ± 0.07 m) and a non-trained group (NOT, n = 11; age, 21.1 ± 2.9 yrs; body mass, 69.3 ± 4.8 kg; height, 1.73 ± 0.06 m). Subjects in the TRE group reported to be engaged in strength training at least 3 times·wk-1 for a minimum of 5 yrs. All Subjects of the TRE group reported to perform squats, leg-press, and calf raises in their training routines on a 3 regular basis. Subjects in the NOT group were not engaged in any exercise programs for least 6 months prior to the study. The physical characteristics of the subjects are shown in Table 1.

Table 1. Physical Characteristics for Strength-Trained (ST) and Untrained (NOT) Groups. Mass Stature MT (cm) (kg) (m) BMI (kg·m-²) Left Right

NOT 69.3 ± 4.8 1.73 ± 0.06 23.1 ± 1.6 6.5 ± 1.7 6.9 ± 1.7 TRE 85.2 ± 9.4 1.76 ± 0.07 25.5 ± 2.9 6.5 ± 1.7 6.9 ± 1.5 Data are in mean ± SD. BMI: Body mass index; MT: muscle thickness

Procedures Ultrasound Measurements Muscle thickness (MT) was measured with B-Mode ultrasonography using a 11 MHz ultrasound linear probe with 5 cm width (Logiq Book XP, General Electric, Milan, Italy). With subjects lying prone, the scanning head was positioned perpendicularly to the skin over the gastrocnemius aponeurosis ~10 cm above the Kager’s triangle. In order to avoid tissue depression, the scanner was fully coated with a thick layer of water-soluble transmission gel. A built-in software cursor was used to measure the distance from the gastrocnemius upper aponeurosis to the muscle-bone interface. Test and retest intraclass correlation coefficient was 0.982.

Electromyography and Mechanomyography Measurements The EMG and MMG signals of the soleus muscle were recorded using bipolar self- adhesive surface electrodes (Trigno Wireless System, DelsysTM, Boston, Massachusetts). The EMG sensor has a built-in triaxial accelerometer (MMG) in 1.5 G sensitive, where G is 9.8 m/s2 (gravity acceleration). The MMG axes were related to the perpendicular, transverse, and longitudinal-axis of the muscle anatomical position. The hybrid sensor was positioned according to the SENIAM recommendations for acquisition of the soleus EMG. Before recordings, submaximal voluntary contractions were performed to check for signal quality. Signals acquisitions were registered in 4 kHz and 296.3 Hz to EMG and MMG, respectively. The signals were acquired with low-pass filter in 500 Hz (EMG) and 50 Hz (MMG) cut-off frequencies. The interval between the electrical stimulus artifact and the onset of the MMG response was calculated in a custom software routine written in Matlab (Mathworks, Natick, MA, USA). The intraclass coefficient correlation was 0.89, indicating a good reliability of the measurement.

The subjects were comfortably positioned in lying prone position. The knee joint was positioned at approximately 5° of flexion with the leg supported by a cushion. Two carbon silicon electrodes (35 x 35 mm) were positioned 20 mm apart at the popliteal fossa, with the cathode as the proximal electrode. The tibial nerve was stimulated by an electrical stimulator (Dualpex model 961 Sport, QuarkTM, São Paulo, Brazil) adjusted to deliver monophasic pulses of 1 ms width. Eight pulses with 10-sec intervals were discharged at current intensities from 30 to 80 mA.

Statistical Analyses 4 The data were analyzed with SPSS version 19.0 (SPSS Inc, Chicago, IL). Descriptive statistics were expressed as means ± standard deviations. The data did not meet the criteria of normality and justified the use of non-parametric analysis. Wilcoxon signed rank test was applied to test differences between the groups. Significance level was set at P<0.05. Effect size (EF, Cohen’s d) was calculated so that 0.2-0.5 is a small ES, 0.5-0.8 is a medium ES, and >0.8 is a large ES.

RESULTS

Comparisions between both groups showed that body mass (P=0.0098, d = 1.27) and BMI (P=0.0176, d = 0.99) were higher in the TRE group. Soleus muscle thickness (P=0.832, d = 0.33) was not statistically different from both groups. The TRE showed lower Δt Stim- EMG (P=0.009, d = 0.54) in comparison to the NOT group. No differences were found to Δt EMG-MMG (Figure 2, P=0.9095, d = 0.0075), Δt Stim-MMG (Figure 1, P=0.3896, d = 0.12), Stim-MMGNORM (P=0.3382, d = 0.20), and MMGPEAK (Figure 2, P=0.4077, d = 0.42) in comparison to the NOT group.

Figure 1. Electromechanical Delay (ms). Untrained Group (Red Color) and Strength Trained Group (Green Color). *P=0.0090. +outliers 5

Figure 2. Normalized Delay and Mechanomyography Peak. Untrained Group (Red Color) and Strength Trained Group (Green Color). +outliers

DISCUSSION

This study compared the EMD of long-term strength trained subjects and untrained subjects through the mechanomyographic response of electrically evoked contractions in the soleus. The main findings indicated that long-term ST elicited no detectable changes in the EMD. This observation is in agreement with others that investigated the EMD of knee extensor muscles after a strength or power training programs. Hakkinen and Komi (17) reported unaltered EMD after 24 wks of training; whereas, the power trained group showed an increased rate of force development. Accordingly, Costa and colleagues (11) observed no EMD differences after 3 d of resistance training. These observations suggest that the EMD is affected by specific mechanisms other than strength-related adaptations.

The EMD derives from several processes, such as excitation-contraction coupling, contraction of the contractile component, and stretching of the SEC (8). Indeed, previous investigations suggested that shorter EMDs could be attributed to adaptations in the stiffness of the SEC, particularly at the muscle-tendon complex (16,23,24). However, in this present study, the absence of differences in the EMD between the trained and the untrained subjects may indicate that the internal muscle-tendon unit structures of the soleus are not sensitive to ST. This is in line with the idea that adaptations to exercise programs are specific to the task (21,27,28).

Studies are conflicting with respect to the training-induced alterations in the EMD. Kubo and co-workers (25) showed that 12 wks of isometric training reduced the EMD of the quadriceps muscle and suggested increased stiffness of the SEC at the muscle-tendon unit to explain a faster force application to the bone. Grosset and colleagues (16) showed that longer EMDs were associated with a decreased musculo-tendinous stiffness after 10 wks of endurance or plyometric training. Mitchell and Cohen (26) attributed the higher rate of torque development of power athletes to the shorter EMD, compared to endurance- trained subjects and a control group. On the other hand, Zhou et al. (39) observed that the EMD remained unchanged after 7 wks of sprint training. 6 In the present study, it is noteworthy to point out that we examined the EMD from the onset of low-frequency oscillations produced by an electrically evoked muscle twitch while most studies assessed the EMD from voluntary actions. Therefore, it is difficult to draw comparisons with other studies. We chose to investigate the MMG signal because it has been demonstrated to allow the time lapse of mechanical responses at the muscle fibers even before the onset of torque production is detectable (10).

It has been suggested that slow-twitch fibers present higher stiffness due to their slower cross-bridge formation (15). Thus, it may be speculated that the soleus has an inherently high muscle-tendon stiffness due to its tonic characteristic, which would hinder training- induced adaptations at the SEC. In fact, previous investigations have demonstrated only mild hypertrophy and strength gains following resistance training of the soleus. This suggest that the soleus muscle might be low-responsive compared to fast-twitch muscles (33,37,38). For instance, Alkner and Tesch (3) failed to counteract the loss of function on the plantar flexors during 90 d of bed rest followed by a resistance training program; whereas, the atrophy in the knee extensors was fully reversed. As an important anti- gravitational muscle during the standing posture, it is reasonable to assume that the soleus activation must have a very short EMD in order to rapidly counteract anterior- posterior body oscillations. Further investigations on the EMD of predominantly fast-twitch muscles (e.g., vastus lateralis) are warranted to confirm this assumption.

Few studies have investigated the EMD using the MMG signal under evoked contractions (34,35). Recently, MMG has been reported as a complementary tool to EMG analysis, due to its effectiveness to examine the mechanical nature of the muscle (9,20). The MMG can detect muscle fiber oscillations at its unique resonance frequency, and it also provides important information with respect to the mechanical events that occur during muscle activity (6,30). To the best of our knowledge, this was the first study to use MMG to assess the EMD under evoked contractions in well-trained and experienced individuals. It has been proposed that several factors influence the MMG signal, including the active stiffness of the fibers (2), intramuscular pressure (32), muscle viscosity (5), and the thickness of subcutaneous fat between the MMG sensor and the muscle surface (22,32). In the current study, it was assumed that trained individuals would display thicker muscle and connective tissue layers due to hypertrophy. This would increase the signal "damping" effect exerted by the surrounding tissues (31), thereby resulting in a detection of a longer EMD. However, ultrasound measurements (Table 1) showed no differences between groups for the SFT and MT (P>0.05).

CONCLUSIONS

This study compared the electromechanical delay from mechanomyographic signal between long-term strength trained and untrained subjects. The results of the present study suggest that the delay of the mechanical response of the soleus may not be sensitive to long-term strength training. The intrinsic characteristics of the soleus may demand specific training regimens (such as power training) to elicit a shorter electromechanical delay. 7

ACKNOWLEDGMENTS We would like to thank Centro Universitário Autônomo do Brasil (UNIBRASIL) for providing the settings to conduct the experimental procedures, to Benny Wong and Mayara Abreu for their technical assistance and to CAPES for scholarships and financial resources.

Address for correspondence: Sergio L. F. Andrade, Department of Physical Education of the Federal University of Paraná, Paraná, Brazil, 82800-170, Email: slfandrade@yahoo. com

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