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Effects of involuntary eccentric contraction training by neuromuscular electrical stimulation on the enhancement of muscle strength
Effects of an involuntary eccentric contraction training by neuromuscular electrical stimulation on the enhancement of muscle strength Jongsang Son, Dongyeop Lee, Youngho Kim PII: DOI: Reference:
S0268-0033(14)00134-X doi: 10.1016/j.clinbiomech.2014.06.003 JCLB 3803
To appear in:
Clinical Biomechanics
Received date: Revised date: Accepted date:
2 January 2014 2 June 2014 2 June 2014
Please cite this article as: Son, Jongsang, Lee, Dongyeop, Kim, Youngho, Effects of an involuntary eccentric contraction training by neuromuscular electrical stimulation on the enhancement of muscle strength, Clinical Biomechanics (2014), doi: 10.1016/j.clinbiomech.2014.06.003
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Effects of an involuntary eccentric contraction training by neuromuscular electrical
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stimulation on the enhancement of muscle strength
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Jongsang Son, Ph.D., Dongyeop Lee, M.S., and *Youngho Kim, Ph.D.
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Department of Biomedical Engineering and Institute of Medical Engineering, Yonsei University (Wonju Campus), Maeji-ri, Heungeop-myeon, Wonju-si, Gangwon-do, 220-710 Republic of
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Korea
*Corresponding author
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Email: [email protected] or [email protected]
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Fax: +82-33-760-2806
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Phone: +82-33-760-2492
Abstract: 245 words
Main text: 2815 words 5 figures and 1 table
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Abstract
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Background: Neuromuscular electrical stimulation is well known as a modality to improve the
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performance of neuromuscular system, but its clinical value on muscle strengthening remains
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equivocal. In this study, we designed a system for an involuntary eccentric contraction of biceps brachii muscles using a continuous passive movement and a commercial functional electrical
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stimulation devices.
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Methods: To investigate the effects of an involuntary eccentric contraction training by neuromuscular electrical stimulation on the enhancement of muscle strength, seven healthy men
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between the ages of 24 and 29 years participated in this study. Participants were trained two
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times per week for 12 weeks. Each exercise session was performed for 30 minutes with no rest
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intervals. Isometric elbow flexion torque and biceps brachii muscle thickness were chosen as evaluation indices, and were measured at pre-/post-training. Findings: After the 12-week training, the isometric elbow flexion torque of the trained side significantly increased by approximately 23% compared to the initial performance (p < 0.01). Meanwhile, the torque of the untrained side showed no significant change (p = 0.862). During the 12-week training period, the biceps brachii muscle thickness of the trained side significantly increased by around 8% at rest and 16% at maximum voluntary contraction (p < 0.01). Interpretation: The developed system and the technique show promising results, suggesting that it has the potential to be used to increase the muscle strength in patients with neuromuscular disease and to be implemented in design rehabilitative protocols. Keywords: Electromyostimulation, Strength training, Rehabilitation
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Introduction
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Neuromuscular electrical stimulation (NMES) is well known as a modality to improve
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performance of the neuromuscular system by reducing immobilization-associated muscle
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weakness, strengthening muscles, and improving impaired muscle function (Vanderthommen and Duchateau, 2007; Hortobágyi and Maffiuletti, 2011). Balogun et al. (1993) showed that the
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quadriceps femoris muscle strength of healthy subjects can be increased by 10% to 20% with 3
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to 6 weeks of high-intensity stimulation. Babault et al. (2007) reported that NMES application on quadriceps for strengthening muscles in athletes is effective after 12 weeks. These positive
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effects can be also found in clinical studies with neuromuscular or musculoskeletal patients.
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Snyder-Mackler et al. (1995) found that NMES is effective in strengthening the quadriceps
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femoris muscle and enhancing functional recovery after reconstruction surgery of the anterior cruciate ligament. Stevens et al. (2004) investigated the effect of high-intensity NMES on quadriceps strength and voluntary activation following total knee arthroplasty, and reported that the weak NMES-treated legs of 4 of the 5 patients had surpassed the strength of the contralateral leg at 6 months. Hu et al. (2012) developed an electromyography-driven electromechanical robot system integrated with NMES for wrist training after stroke, and suggested that assistance from the robot helped to improve movement accuracy and that the NMES helped increase muscle activation for the wrist joint and suppress excessive muscular activities from the elbow joint. These studies provide evidence that direct electrical stimulation can be used in the development of motor treatments for muscles and the enhancement of muscle strength. NMES research has typically focused on isometric or concentric contraction of the muscles to be treated. A number of studies have demonstrated that eccentric training has advantages over 3
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concentric training. For example, Colliander and Tesch (1990) compared the adaptive responses to two different resistance trainings, i.e. 12 maximum bilateral concentric or six pairs of
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maximum bilateral eccentric and concentric quadriceps muscle actions, and suggested that
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increases in peak torque and strength-related performance parameters, such as vertical jump
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height and three-repetition maximum half-squat, were greater following the maximum concentric and eccentric training than the resistance training using concentric muscle actions only. Dudley
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et al. (1991) also emphasized the importance of eccentric actions in performance adaptations to
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resistance training, showing similar results by Colliander and Tesch (1990). These results could be regarded as an outcome from neural adaptations produced by eccentric muscle actions, and
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those adaptations seem to be related to more efficient motor unit recruitment patterns after
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eccentric training than concentric training (Gabriel et al., 2006; Hortobágyi and Maffiuletti, 2011;
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de Souza-Teixeira and de Paz, 2012).
In order to improve the effects of each NMES and eccentric training on muscle strength, Yanagi et al. (2003) developed a hybrid strengthening technique, by combining NMES and eccentric contraction, in which an agonist performs a volitional concentric contraction against an electrically stimulated antagonist. They applied this hybrid exercise to the elbow flexors and extensors of twelve healthy men, training the participants 3 times per week for 12 weeks. After the training, elbow extension torques increased significantly, and cross-sectional areas increased in all muscles. They proposed a novel modality for muscle strengthening definitely, but there are some limitations in the technique. First, the hybrid exercise might not be adequate for patients severely affected with neuromuscular disease because they need to be able to generate agonist muscle forces to overcome the resistance provided by the electrically stimulated antagonist. In
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addition, their experiments were performed without a guidance device to control the range of motion (ROM) or to maintain a constant angular velocity to the elbow joint.
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In this study, we developed an involuntary eccentric contraction training system to enhance
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biceps brachii muscle strength. The developed system uses a motor to generate elbow joint
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movements and a commercial electrical stimulation device to stimulate the biceps brachii muscle. To evaluate the developed system, we trained seven healthy subjects and compared their elbow
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joint torques and muscle thicknesses at pre- and post-training.
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Methods
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Involuntary eccentric contraction training system
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Our involuntary eccentric contraction training system consists of two parts: (1) a continuous
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passive movement (CPM) device for the elbow joint and (2) a NMES device. The CPM device includes a brushed DC motor (GR 53x30, Ametek PMC, US) to generate elbow joint movements
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with a constant velocity of 10°/s and an exoskeleton to fix the arm. The exoskeleton was
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designed to allow the elbow joint ROM from 0° (fully extended) to 90° (flexed). The commercial NMES device (Stim Plus DP-100, Cybermedic Co., Ltd., KR) was used to stimulate the biceps
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brachii muscle only while the elbow joint was extending; thus, the biceps brachii muscle could
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perform involuntary eccentric contractions. A microcontroller (Atmega128, Atmel, US) was
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used to link the CPM device and the NMES device, controlling the elbow joint movement using the pulse width modulation function and triggering the NMES device only while the elbow joint was in extension (Figure 1).
Participants
Seven healthy male subjects (Table 1) were recruited, who had right dominant hands and no neuromusculoskeletal injury. They gave informed consent, which was approved by the Institutional Review Board of Yonsei University (#2013-10) prior to commencing the experiments.
Training session
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The participants were trained two times per week (three subjects: Mondays and Thursdays; and four subjects: Tuesdays and Fridays) for 12 weeks. Each exercise session was performed for 30
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minutes with no rest interval (Hsu et al., 2010). During the training, the subject was required to
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maintain a shoulder joint angle of 90° in the sagittal plane. The electrical stimulation (pulse
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width: 200 μs; and frequency: 20 Hz (Dreibati et al., 2010)) was delivered through a pair of 5 × 5 cm gel-coated electrodes attached to the region of the biceps brachii muscle belly. The
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magnitude of the stimulation was determined as the subject’s maximum comfortable current
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Data acquisition and analysis
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mean value was 57.00 (SD 4.28) mA.
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level, but no more than 80 mA, with complete elbow flexion from the fully extended state; the
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In order to evaluate training effects of the developed system, a dynamometer (Biodex System 3 Pro, Biodex Medical Systems, US) was used to measure the maximum isometric elbow flexion torques at pre- and post-training, 3 times each. The shoulder and elbow joint angles were fixed at 45° and 60°, respectively, using a hand-held goniometer, and assumed to be a constant for each trial. While subjects sat on the dynamometer seat for the assigned posture with the elbows flexed at 90°, the thickness of the biceps brachii muscles was measured with a B-mode ultrasound image device with 9 MHz linear transducer (SonoAce pico, Samsung Medison Co., Ltd., KR) at rest and at maximum voluntary contraction (MVC), respectively. The probe was prepared with water-soluble transmission gel and applied securely on the skin over the mid-bellies of the biceps brachii muscles (Ohata et al., 2006; Pillen, 2010). The captured images were imported into a custom-made software, which was developed in the MATLAB GUI environment (R2010a, Mathworks Inc., US) (Figure 2) (Kim et al., 2013) to calculate the muscle thickness. The muscle 7
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thickness was determined as the greatest distance from the adipose tissue-muscle interface to the muscle-bone interface (Ohata et al., 2006; Akagi et al., 2009).
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Statistical analysis
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Because of the given inter-individual differences in torque-generating capacity and muscle
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thickness, training effects were expressed relative to the baseline, i.e., values at pre-training, for each subject. Then, in order to assess assumptions of the normality and homogeneity of variances,
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Kolmogorov-Smirnov and Levene tests were performed for the normalized torque and muscle
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thickness data, respectively. Since all data did not satisfy the assumptions, Wilcoxon’s signedranks test was performed to evaluate paired difference for the data. All statistical analyses were
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performed with IBM SPSS Statistics (Version 20, IBM, US), and the significance level (p) was
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set to 0.05.
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Results
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Involuntary eccentric contraction training showed significant effects on the maximum isometric
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flexion torque (expressed relative to the body weight, Figure 3A, and the initial performance,
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Figure 3B, in each subject). The maximum isometric flexion torque of the trained side was 0.63 (SD 0.13) N-m/kg at the baseline (Pre) and 0.76 (SD 0.14) N-m/kg at the completion of the 12-
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week training (Post). After the 12-week training, the maximum isometric flexion torque
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increased by approximately 23% compared to the initial performance. These results show a significant enhancement in the maximum isometric contraction torque of the trained side after
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the 12-week involuntary eccentric contraction training (p < 0.01). However, although the
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maximum isometric flexion torque of the untrained side was 0.64 (SD 0.14) N-m/kg at the
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baseline and 0.64 (SD 0.14) N-m/kg at completion of the 12-week training, the change was not statistically significant (p = 0.862). During the 12-week training, the biceps brachii muscle thickness of the trained side was changed from 15.97 (SD 4.86) mm to 16.23 (SD 5.56) mm at rest, and from 21.37 (SD 9.67) mm to 24.85 (SD 11.32) mm at MVC (Figure 4A, and Figure 4B expressed relative to initial thickness at rest in each subject). The thickness increased by approximately 8% at rest and 16% at MVC. These results show a significant increase in muscle thickness of the trained side after the 12-week involuntary eccentric contraction training (p < 0.01).
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Discussion
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The objective of this study was to investigate the effects of an involuntary eccentric contraction
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training on the enhancement of muscle strength. Seven subjects participated in the 12-week
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training. During the training, the subjects were required not to do any strenuous exercise. This request seemed to be accepted since the results of the untrained side showed no significant
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change. Although the numbers of subjects and treated muscles were limited, our findings are
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promising for increasing the maximum isometric flexion torque and the muscle thickness. The concept of this study arose from two points of view. First, the principle of overload is
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generally recognized as fundamental to the strengthening process, meaning that when an
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unaccustomed load, i.e., overload, is applied to the body, the body will adapt to become able to
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handle the load by involving physiological changes or neural adaptations (Hellebrandt and Houtz, 1956; Baechel and Earle, 2008). Indeed, although NMES has been widely used to strengthen muscles, its clinical value and optimal application are equivocal (Yanagi et al., 2003). According to a systematic review of the randomized controlled trials by Bax et al. (2005), NMES can constitute an effective way to strengthen the quadriceps femoris muscles in normal individuals and in patients who are not exercising; however, some researchers have concluded that NMES does not result in significant strength improvement compared with those who do not exercise. These discrepancies might come from whether the experimental conditions, i.e., the various forms of muscle contraction and intensity of NMES, satisfy the principle of overload. Since muscles basically tend to shorten when stimulated, they generally work as forms of concentric contraction; however, an unaccustomed load is essential to increasing strength, according to the principle of overload. Thus, eccentric contraction could be more favorable than concentric 10
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contraction, based on the force–velocity relationship (Hill, 1938; Katz, 1939). Second, a number of studies have demonstrated that active, voluntary training with individuals’ efforts is better for
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improvements of motor functionality than passive, involuntary training. For example, Lum et al.
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(2002) compared the effects of robot-assisted movement training with conventional techniques
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for the rehabilitation of upper arm motor function after stroke, and suggested that the greater strength gains in the robot group could be due to the active-constrained mode they employed,
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which is a form of maximal-effort resistance exercise. However, all patients do not perform
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active training, because the strength generated by their own muscle contractions is not always enough for movements to occur; in this case, passive training is needed to avoid functional
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degeneration of muscles and joints. Fortunately, passive training has the potential to facilitate
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brain activity in the primary sensory and motor cortices (Guzzetta et al., 2007; Formaggio et al.,
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2013; Perrey, 2013). Weiller et al. (1996) measured the regional cerebral blood flow (rCBF) during repetitive active and passive flexion and extension of the right elbow in six healthy males using positron emission tomography and a standard H215O injection technique. The results showed that there were strong increases in rCBF, identical in location, amount, and extent to those in the contralateral sensorimotor cortex during both types of movement. Saitou et al. (2000) investigated the effects of 13 rehabilitation tasks on cerebral blood volume (CBV) and cerebral oxygen volume (COV) in the prefrontal region among 44 stroke patients using a near-infrared spectroscopy. In the study, passive movements of 13 tasks were involved: cycling, repeated wrist and finger extensions, and movement of affected upper limbs using a pulley. At the end of each task, CBV increased by 92.3%, 6.3% and 27.8%, respectively, and COV increased by 92.3%, 37.5% and 50.0%, respectively, compared to the baseline. These results imply that the repetitive
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element is of particular value in motor learning and rehabilitation, in spite of its being a passive type of training (Bütefisch et al., 1995).
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Our involuntary eccentric contraction training system yielded promising results, showing
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increases in the maximum isometric flexion torque by an average of 23%. These results were
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similar to those in previous studies. For example, Westing et al. (1990) presented that eccentric torque could be significantly increased by an average of 21–24% above the voluntary level by
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superimposing electrical stimulation. In addition, Hortobágyi et al. (1999) compared the
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effectiveness of voluntary and stimulated eccentric contractions in eliciting strength gains, and reported that voluntary and stimulated training resulted in 54 and 177% strength gains,
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respectively, suggesting that stimulation may be a better means of conditioning. Indeed,
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eccentric contractions are associated with the activation of large motor units which are
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preferentially recruited during electrical stimulation (Phillips and Petrofsky, 1980; Hortobágyi et al., 1999). These findings imply that stimulated eccentric contractions cause large motor units to activate unusually highly, which could account for the extreme ipsilateral adaptations (Westing et al., 1990).
The muscle thickness at MVC also increased by an average of 16%. Generally, muscle strength is related to its cross-sectional area (CSA) (Maughan et al., 1983; Starkey et al., 1996). Some researchers have reported that isometric contractions increase the thickness of parallel-fibered muscles, such as the biceps brachii and brachialis (Hodges et al., 2003; Akagi et al., 2008). Therefore, the increase in muscle thickness and so of its CSA developed through contractions of parallel-fibered muscles is likely to increase muscle force production (Hodges et al., 2003). Indeed, Akagi et al. (2008) investigated the linear relationship between muscle strength and indices of CSA for elbow flexors during MVC. They chose the product of muscle thickness and 12
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circumference (MT×C) and the square of muscle thickness (MT2) as the indices of CSA. They found that the correlation coefficient during MVC was 0.905 (p < 0.001) for the relationship
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between muscle strength of elbow flexors and the MT×C index, and it was 0.896 (p < 0.001) for
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the relationship between the strength and the MT2 index. We did not measure the circumference
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and strength of the biceps brachii muscles, but rather we performed a linear regression analysis of the relationship between the MT2 index and elbow flexion torque. The correlation coefficient
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was 0.806 (p < 0.05) in our result (Figure 5), and this indicates that the enhancement of elbow
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flexion torque results from the increased thickness of the trained biceps brachii muscles. There are some issues to consider in this study. First, this study did not compare the involuntary
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eccentric contraction group with a control group undergoing either a sham therapy or a
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conventional treatment. Our results show a significant enhancement in the trained arm and not in
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the untrained arm. Despite the lack of control group comparison, this result leads us to expect that involuntary eccentric contraction training is at least more beneficial to enhancing muscle strength than doing no exercise. Second, this study does not answer the highly relevant clinical question of whether our training could be beneficial to enhance muscle strengths in acute, subacute, or chronic neuromuscular patients, and if so what amount of recovery could be expected. Moreover, the optimum therapy protocol such as stimulation intensity or treatment intensity is important, but unknown. In addition, it is yet to be determined whether involuntary eccentric contraction training can yield promising results on other muscles. We plan to perform further studies of the short- and long-term effects to answer to these questions.
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Conclusion
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In this study, we developed an involuntary eccentric contraction training system and evaluated
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the effects of the training on the enhancement of biceps brachii muscle strength in seven normal
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adult men. The results showed that maximum isometric flexion torque and muscle thickness on the trained side significantly increased by 23% and 16% respectively after a 12-week training
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program. The developed system and the technique show promising results, suggesting that it has
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the potential to be used to increase the muscle strength in patients with neuromuscular disease
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Acknowledgments
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and to be implemented in design rehabilitative protocols.
This work was supported by the Technology Development Program with Association of Industry, Academy and Research Institute (1030050032) funded by the Small and Medium Business Administration (SMBA, Korea), and this research was also financially supported by the Ministry of Knowledge Economy (MKE) and Korea Institute for Advancement of Technology (KIAT) through the Research and Development for Regional Industry (70011192).
Conflicts of interest
We have no conflict of interest with this work. 14
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Table 1. Subject information (N = 7) Age (years)
Height (cm)
1
26
180
2
25
172
3
24
171
4
25
5
27
6
27
7
29
Mean (SD)
26.1 (1.7)
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Subject No.
88 70 64 56
175
72
179
62
165
82
173.4 (5.1)
70.6 (11.3)
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172
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Weight (kg)
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Figure legends
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Figure 1. Apparatus for involuntary eccentric contraction training and its application.
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Figure 2. Custom-made software that can measure the fiber length, the pennation angle and the
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muscle thickness from an ultrasound image. (A) Original ultrasound image: a, line to define the number of pixels corresponding to 1 cm; and b, rectangle to define the region of interest (ROI).
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(B) Magnified image in ROI: a, biceps brachii muscle; b, brachialis muscle; c, humerus; d,
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biceps brachii muscle fascia to subcutaneous tissue; e, biceps brachii muscle thickness; and f,
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biceps brachii muscle fascia to brachialis muscle.
Figure 3. Effects of 12-week involuntary eccentric contraction training on maximum isometric elbow flexion torque. (A) The individual subjects’ torques of the trained and untrained sides are shown at baseline (Pre) and after the training (Post). The torque data were normalized by the individual subjects’ weight. The torque of the trained side increased, but that of the untrained side showed an irregular tendency. (B) The group changes in torque are shown at Pre and Post. The changes in torque are expressed as a post/pre ratio for the trained and untrained sides. The change in torque was statistically significant on the trained side only.
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Figure 4. Effects of 12-week involuntary eccentric contraction training on biceps brachii muscle thickness of the trained side. (A) The individual subjects’ muscle thicknesses at rest and at
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maximum voluntary contraction (MVC) are shown at baseline (Pre) and after the training (Post).
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The thickness increased both at rest and at MVC. (B) The group changes in thickness at rest and
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at MVC are shown at Pre and Post. The changes in thickness are expressed relative to the initial thickness at Pre. The changes in muscle thickness are statistically significant at both rest and
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MVC.
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Figure 5. Performance enhancements in maximum isometric flexion torque as a function of
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changes in the square of the muscle thickness. The abscissa indicates the biceps brachii muscle
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thickness at MVC; the ordinate shows the maximum isometric flexion torque. Based on the good linear relationship between the two variables, the strength gains of the biceps brachii muscles appear to result in enhancements of the torque performance.
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Highlights
An involuntary eccentric contraction system was designed with NMES.
The system was applied to biceps brachii of 7 healthy men for 12-week training.
Isometric elbow flexion torques of trained side significantly increased around 23%.
Isometric elbow flexion torques of untrained side showed no significant changes.
The muscle thickness significantly increased around 16% at MVC.
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S0268-0033(14)00134-X doi: 10.1016/j.clinbiomech.2014.06.003 JCLB 3803
To appear in:
Clinical Biomechanics
Received date: Revised date: Accepted date:
2 January 2014 2 June 2014 2 June 2014
Please cite this article as: Son, Jongsang, Lee, Dongyeop, Kim, Youngho, Effects of an involuntary eccentric contraction training by neuromuscular electrical stimulation on the enhancement of muscle strength, Clinical Biomechanics (2014), doi: 10.1016/j.clinbiomech.2014.06.003
This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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Effects of an involuntary eccentric contraction training by neuromuscular electrical
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stimulation on the enhancement of muscle strength
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Jongsang Son, Ph.D., Dongyeop Lee, M.S., and *Youngho Kim, Ph.D.
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Department of Biomedical Engineering and Institute of Medical Engineering, Yonsei University (Wonju Campus), Maeji-ri, Heungeop-myeon, Wonju-si, Gangwon-do, 220-710 Republic of
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Korea
*Corresponding author
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Email: [email protected] or [email protected]
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Fax: +82-33-760-2806
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Phone: +82-33-760-2492
Abstract: 245 words
Main text: 2815 words 5 figures and 1 table
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Abstract
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Background: Neuromuscular electrical stimulation is well known as a modality to improve the
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performance of neuromuscular system, but its clinical value on muscle strengthening remains
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equivocal. In this study, we designed a system for an involuntary eccentric contraction of biceps brachii muscles using a continuous passive movement and a commercial functional electrical
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stimulation devices.
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Methods: To investigate the effects of an involuntary eccentric contraction training by neuromuscular electrical stimulation on the enhancement of muscle strength, seven healthy men
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between the ages of 24 and 29 years participated in this study. Participants were trained two
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times per week for 12 weeks. Each exercise session was performed for 30 minutes with no rest
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intervals. Isometric elbow flexion torque and biceps brachii muscle thickness were chosen as evaluation indices, and were measured at pre-/post-training. Findings: After the 12-week training, the isometric elbow flexion torque of the trained side significantly increased by approximately 23% compared to the initial performance (p < 0.01). Meanwhile, the torque of the untrained side showed no significant change (p = 0.862). During the 12-week training period, the biceps brachii muscle thickness of the trained side significantly increased by around 8% at rest and 16% at maximum voluntary contraction (p < 0.01). Interpretation: The developed system and the technique show promising results, suggesting that it has the potential to be used to increase the muscle strength in patients with neuromuscular disease and to be implemented in design rehabilitative protocols. Keywords: Electromyostimulation, Strength training, Rehabilitation
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Introduction
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Neuromuscular electrical stimulation (NMES) is well known as a modality to improve
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performance of the neuromuscular system by reducing immobilization-associated muscle
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weakness, strengthening muscles, and improving impaired muscle function (Vanderthommen and Duchateau, 2007; Hortobágyi and Maffiuletti, 2011). Balogun et al. (1993) showed that the
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quadriceps femoris muscle strength of healthy subjects can be increased by 10% to 20% with 3
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to 6 weeks of high-intensity stimulation. Babault et al. (2007) reported that NMES application on quadriceps for strengthening muscles in athletes is effective after 12 weeks. These positive
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effects can be also found in clinical studies with neuromuscular or musculoskeletal patients.
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Snyder-Mackler et al. (1995) found that NMES is effective in strengthening the quadriceps
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femoris muscle and enhancing functional recovery after reconstruction surgery of the anterior cruciate ligament. Stevens et al. (2004) investigated the effect of high-intensity NMES on quadriceps strength and voluntary activation following total knee arthroplasty, and reported that the weak NMES-treated legs of 4 of the 5 patients had surpassed the strength of the contralateral leg at 6 months. Hu et al. (2012) developed an electromyography-driven electromechanical robot system integrated with NMES for wrist training after stroke, and suggested that assistance from the robot helped to improve movement accuracy and that the NMES helped increase muscle activation for the wrist joint and suppress excessive muscular activities from the elbow joint. These studies provide evidence that direct electrical stimulation can be used in the development of motor treatments for muscles and the enhancement of muscle strength. NMES research has typically focused on isometric or concentric contraction of the muscles to be treated. A number of studies have demonstrated that eccentric training has advantages over 3
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concentric training. For example, Colliander and Tesch (1990) compared the adaptive responses to two different resistance trainings, i.e. 12 maximum bilateral concentric or six pairs of
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maximum bilateral eccentric and concentric quadriceps muscle actions, and suggested that
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increases in peak torque and strength-related performance parameters, such as vertical jump
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height and three-repetition maximum half-squat, were greater following the maximum concentric and eccentric training than the resistance training using concentric muscle actions only. Dudley
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et al. (1991) also emphasized the importance of eccentric actions in performance adaptations to
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resistance training, showing similar results by Colliander and Tesch (1990). These results could be regarded as an outcome from neural adaptations produced by eccentric muscle actions, and
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those adaptations seem to be related to more efficient motor unit recruitment patterns after
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eccentric training than concentric training (Gabriel et al., 2006; Hortobágyi and Maffiuletti, 2011;
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de Souza-Teixeira and de Paz, 2012).
In order to improve the effects of each NMES and eccentric training on muscle strength, Yanagi et al. (2003) developed a hybrid strengthening technique, by combining NMES and eccentric contraction, in which an agonist performs a volitional concentric contraction against an electrically stimulated antagonist. They applied this hybrid exercise to the elbow flexors and extensors of twelve healthy men, training the participants 3 times per week for 12 weeks. After the training, elbow extension torques increased significantly, and cross-sectional areas increased in all muscles. They proposed a novel modality for muscle strengthening definitely, but there are some limitations in the technique. First, the hybrid exercise might not be adequate for patients severely affected with neuromuscular disease because they need to be able to generate agonist muscle forces to overcome the resistance provided by the electrically stimulated antagonist. In
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addition, their experiments were performed without a guidance device to control the range of motion (ROM) or to maintain a constant angular velocity to the elbow joint.
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In this study, we developed an involuntary eccentric contraction training system to enhance
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biceps brachii muscle strength. The developed system uses a motor to generate elbow joint
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movements and a commercial electrical stimulation device to stimulate the biceps brachii muscle. To evaluate the developed system, we trained seven healthy subjects and compared their elbow
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joint torques and muscle thicknesses at pre- and post-training.
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Methods
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Involuntary eccentric contraction training system
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Our involuntary eccentric contraction training system consists of two parts: (1) a continuous
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passive movement (CPM) device for the elbow joint and (2) a NMES device. The CPM device includes a brushed DC motor (GR 53x30, Ametek PMC, US) to generate elbow joint movements
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with a constant velocity of 10°/s and an exoskeleton to fix the arm. The exoskeleton was
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designed to allow the elbow joint ROM from 0° (fully extended) to 90° (flexed). The commercial NMES device (Stim Plus DP-100, Cybermedic Co., Ltd., KR) was used to stimulate the biceps
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brachii muscle only while the elbow joint was extending; thus, the biceps brachii muscle could
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perform involuntary eccentric contractions. A microcontroller (Atmega128, Atmel, US) was
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used to link the CPM device and the NMES device, controlling the elbow joint movement using the pulse width modulation function and triggering the NMES device only while the elbow joint was in extension (Figure 1).
Participants
Seven healthy male subjects (Table 1) were recruited, who had right dominant hands and no neuromusculoskeletal injury. They gave informed consent, which was approved by the Institutional Review Board of Yonsei University (#2013-10) prior to commencing the experiments.
Training session
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The participants were trained two times per week (three subjects: Mondays and Thursdays; and four subjects: Tuesdays and Fridays) for 12 weeks. Each exercise session was performed for 30
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minutes with no rest interval (Hsu et al., 2010). During the training, the subject was required to
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maintain a shoulder joint angle of 90° in the sagittal plane. The electrical stimulation (pulse
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width: 200 μs; and frequency: 20 Hz (Dreibati et al., 2010)) was delivered through a pair of 5 × 5 cm gel-coated electrodes attached to the region of the biceps brachii muscle belly. The
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magnitude of the stimulation was determined as the subject’s maximum comfortable current
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Data acquisition and analysis
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mean value was 57.00 (SD 4.28) mA.
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level, but no more than 80 mA, with complete elbow flexion from the fully extended state; the
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In order to evaluate training effects of the developed system, a dynamometer (Biodex System 3 Pro, Biodex Medical Systems, US) was used to measure the maximum isometric elbow flexion torques at pre- and post-training, 3 times each. The shoulder and elbow joint angles were fixed at 45° and 60°, respectively, using a hand-held goniometer, and assumed to be a constant for each trial. While subjects sat on the dynamometer seat for the assigned posture with the elbows flexed at 90°, the thickness of the biceps brachii muscles was measured with a B-mode ultrasound image device with 9 MHz linear transducer (SonoAce pico, Samsung Medison Co., Ltd., KR) at rest and at maximum voluntary contraction (MVC), respectively. The probe was prepared with water-soluble transmission gel and applied securely on the skin over the mid-bellies of the biceps brachii muscles (Ohata et al., 2006; Pillen, 2010). The captured images were imported into a custom-made software, which was developed in the MATLAB GUI environment (R2010a, Mathworks Inc., US) (Figure 2) (Kim et al., 2013) to calculate the muscle thickness. The muscle 7
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thickness was determined as the greatest distance from the adipose tissue-muscle interface to the muscle-bone interface (Ohata et al., 2006; Akagi et al., 2009).
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Statistical analysis
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Because of the given inter-individual differences in torque-generating capacity and muscle
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thickness, training effects were expressed relative to the baseline, i.e., values at pre-training, for each subject. Then, in order to assess assumptions of the normality and homogeneity of variances,
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Kolmogorov-Smirnov and Levene tests were performed for the normalized torque and muscle
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thickness data, respectively. Since all data did not satisfy the assumptions, Wilcoxon’s signedranks test was performed to evaluate paired difference for the data. All statistical analyses were
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performed with IBM SPSS Statistics (Version 20, IBM, US), and the significance level (p) was
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set to 0.05.
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Results
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Involuntary eccentric contraction training showed significant effects on the maximum isometric
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flexion torque (expressed relative to the body weight, Figure 3A, and the initial performance,
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Figure 3B, in each subject). The maximum isometric flexion torque of the trained side was 0.63 (SD 0.13) N-m/kg at the baseline (Pre) and 0.76 (SD 0.14) N-m/kg at the completion of the 12-
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week training (Post). After the 12-week training, the maximum isometric flexion torque
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increased by approximately 23% compared to the initial performance. These results show a significant enhancement in the maximum isometric contraction torque of the trained side after
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the 12-week involuntary eccentric contraction training (p < 0.01). However, although the
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maximum isometric flexion torque of the untrained side was 0.64 (SD 0.14) N-m/kg at the
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baseline and 0.64 (SD 0.14) N-m/kg at completion of the 12-week training, the change was not statistically significant (p = 0.862). During the 12-week training, the biceps brachii muscle thickness of the trained side was changed from 15.97 (SD 4.86) mm to 16.23 (SD 5.56) mm at rest, and from 21.37 (SD 9.67) mm to 24.85 (SD 11.32) mm at MVC (Figure 4A, and Figure 4B expressed relative to initial thickness at rest in each subject). The thickness increased by approximately 8% at rest and 16% at MVC. These results show a significant increase in muscle thickness of the trained side after the 12-week involuntary eccentric contraction training (p < 0.01).
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Discussion
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The objective of this study was to investigate the effects of an involuntary eccentric contraction
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training on the enhancement of muscle strength. Seven subjects participated in the 12-week
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training. During the training, the subjects were required not to do any strenuous exercise. This request seemed to be accepted since the results of the untrained side showed no significant
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change. Although the numbers of subjects and treated muscles were limited, our findings are
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promising for increasing the maximum isometric flexion torque and the muscle thickness. The concept of this study arose from two points of view. First, the principle of overload is
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generally recognized as fundamental to the strengthening process, meaning that when an
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unaccustomed load, i.e., overload, is applied to the body, the body will adapt to become able to
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handle the load by involving physiological changes or neural adaptations (Hellebrandt and Houtz, 1956; Baechel and Earle, 2008). Indeed, although NMES has been widely used to strengthen muscles, its clinical value and optimal application are equivocal (Yanagi et al., 2003). According to a systematic review of the randomized controlled trials by Bax et al. (2005), NMES can constitute an effective way to strengthen the quadriceps femoris muscles in normal individuals and in patients who are not exercising; however, some researchers have concluded that NMES does not result in significant strength improvement compared with those who do not exercise. These discrepancies might come from whether the experimental conditions, i.e., the various forms of muscle contraction and intensity of NMES, satisfy the principle of overload. Since muscles basically tend to shorten when stimulated, they generally work as forms of concentric contraction; however, an unaccustomed load is essential to increasing strength, according to the principle of overload. Thus, eccentric contraction could be more favorable than concentric 10
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contraction, based on the force–velocity relationship (Hill, 1938; Katz, 1939). Second, a number of studies have demonstrated that active, voluntary training with individuals’ efforts is better for
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improvements of motor functionality than passive, involuntary training. For example, Lum et al.
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(2002) compared the effects of robot-assisted movement training with conventional techniques
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for the rehabilitation of upper arm motor function after stroke, and suggested that the greater strength gains in the robot group could be due to the active-constrained mode they employed,
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which is a form of maximal-effort resistance exercise. However, all patients do not perform
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active training, because the strength generated by their own muscle contractions is not always enough for movements to occur; in this case, passive training is needed to avoid functional
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degeneration of muscles and joints. Fortunately, passive training has the potential to facilitate
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brain activity in the primary sensory and motor cortices (Guzzetta et al., 2007; Formaggio et al.,
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2013; Perrey, 2013). Weiller et al. (1996) measured the regional cerebral blood flow (rCBF) during repetitive active and passive flexion and extension of the right elbow in six healthy males using positron emission tomography and a standard H215O injection technique. The results showed that there were strong increases in rCBF, identical in location, amount, and extent to those in the contralateral sensorimotor cortex during both types of movement. Saitou et al. (2000) investigated the effects of 13 rehabilitation tasks on cerebral blood volume (CBV) and cerebral oxygen volume (COV) in the prefrontal region among 44 stroke patients using a near-infrared spectroscopy. In the study, passive movements of 13 tasks were involved: cycling, repeated wrist and finger extensions, and movement of affected upper limbs using a pulley. At the end of each task, CBV increased by 92.3%, 6.3% and 27.8%, respectively, and COV increased by 92.3%, 37.5% and 50.0%, respectively, compared to the baseline. These results imply that the repetitive
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element is of particular value in motor learning and rehabilitation, in spite of its being a passive type of training (Bütefisch et al., 1995).
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Our involuntary eccentric contraction training system yielded promising results, showing
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increases in the maximum isometric flexion torque by an average of 23%. These results were
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similar to those in previous studies. For example, Westing et al. (1990) presented that eccentric torque could be significantly increased by an average of 21–24% above the voluntary level by
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superimposing electrical stimulation. In addition, Hortobágyi et al. (1999) compared the
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effectiveness of voluntary and stimulated eccentric contractions in eliciting strength gains, and reported that voluntary and stimulated training resulted in 54 and 177% strength gains,
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respectively, suggesting that stimulation may be a better means of conditioning. Indeed,
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eccentric contractions are associated with the activation of large motor units which are
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preferentially recruited during electrical stimulation (Phillips and Petrofsky, 1980; Hortobágyi et al., 1999). These findings imply that stimulated eccentric contractions cause large motor units to activate unusually highly, which could account for the extreme ipsilateral adaptations (Westing et al., 1990).
The muscle thickness at MVC also increased by an average of 16%. Generally, muscle strength is related to its cross-sectional area (CSA) (Maughan et al., 1983; Starkey et al., 1996). Some researchers have reported that isometric contractions increase the thickness of parallel-fibered muscles, such as the biceps brachii and brachialis (Hodges et al., 2003; Akagi et al., 2008). Therefore, the increase in muscle thickness and so of its CSA developed through contractions of parallel-fibered muscles is likely to increase muscle force production (Hodges et al., 2003). Indeed, Akagi et al. (2008) investigated the linear relationship between muscle strength and indices of CSA for elbow flexors during MVC. They chose the product of muscle thickness and 12
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circumference (MT×C) and the square of muscle thickness (MT2) as the indices of CSA. They found that the correlation coefficient during MVC was 0.905 (p < 0.001) for the relationship
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between muscle strength of elbow flexors and the MT×C index, and it was 0.896 (p < 0.001) for
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the relationship between the strength and the MT2 index. We did not measure the circumference
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and strength of the biceps brachii muscles, but rather we performed a linear regression analysis of the relationship between the MT2 index and elbow flexion torque. The correlation coefficient
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was 0.806 (p < 0.05) in our result (Figure 5), and this indicates that the enhancement of elbow
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flexion torque results from the increased thickness of the trained biceps brachii muscles. There are some issues to consider in this study. First, this study did not compare the involuntary
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eccentric contraction group with a control group undergoing either a sham therapy or a
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conventional treatment. Our results show a significant enhancement in the trained arm and not in
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the untrained arm. Despite the lack of control group comparison, this result leads us to expect that involuntary eccentric contraction training is at least more beneficial to enhancing muscle strength than doing no exercise. Second, this study does not answer the highly relevant clinical question of whether our training could be beneficial to enhance muscle strengths in acute, subacute, or chronic neuromuscular patients, and if so what amount of recovery could be expected. Moreover, the optimum therapy protocol such as stimulation intensity or treatment intensity is important, but unknown. In addition, it is yet to be determined whether involuntary eccentric contraction training can yield promising results on other muscles. We plan to perform further studies of the short- and long-term effects to answer to these questions.
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Conclusion
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In this study, we developed an involuntary eccentric contraction training system and evaluated
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the effects of the training on the enhancement of biceps brachii muscle strength in seven normal
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adult men. The results showed that maximum isometric flexion torque and muscle thickness on the trained side significantly increased by 23% and 16% respectively after a 12-week training
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program. The developed system and the technique show promising results, suggesting that it has
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the potential to be used to increase the muscle strength in patients with neuromuscular disease
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Acknowledgments
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and to be implemented in design rehabilitative protocols.
This work was supported by the Technology Development Program with Association of Industry, Academy and Research Institute (1030050032) funded by the Small and Medium Business Administration (SMBA, Korea), and this research was also financially supported by the Ministry of Knowledge Economy (MKE) and Korea Institute for Advancement of Technology (KIAT) through the Research and Development for Regional Industry (70011192).
Conflicts of interest
We have no conflict of interest with this work. 14
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Vanderthommen, M., Duchateau, J., 2007. Electrical stimulation as a modality to improve performance of the neuromuscular system. Exerc. Sport Sci. Rev. 35 (4), 180-185. Weiller, C., Jüptner, M., Fellows, S., Rijntjes, M., Leonhardt, G., Kiebel, S. et al., 1996. Brain representation of active and passive movements. Neuroimage 4 (2), 105-110. Westing, S.H., Y., S.J., A., T., 1990. Effects of electrical stimulation on eccentric and concentric torque‐velocity relationships during knee extension in man. Acta Physiol. Scand. 140 (1), 1722. Yanagi, T., Shiba, N., Maeda, T., Iwasa, K., Umezu, Y., Tagawa, Y. et al., 2003. Agonist contractions against electrically stimulated antagonists. Arch. Phys. Med. Rehabil. 84 (6), 843-848.
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Table 1. Subject information (N = 7) Age (years)
Height (cm)
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26
180
2
25
172
3
24
171
4
25
5
27
6
27
7
29
Mean (SD)
26.1 (1.7)
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Subject No.
88 70 64 56
175
72
179
62
165
82
173.4 (5.1)
70.6 (11.3)
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172
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Weight (kg)
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Figure legends
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Figure 1. Apparatus for involuntary eccentric contraction training and its application.
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Figure 2. Custom-made software that can measure the fiber length, the pennation angle and the
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muscle thickness from an ultrasound image. (A) Original ultrasound image: a, line to define the number of pixels corresponding to 1 cm; and b, rectangle to define the region of interest (ROI).
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(B) Magnified image in ROI: a, biceps brachii muscle; b, brachialis muscle; c, humerus; d,
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biceps brachii muscle fascia to subcutaneous tissue; e, biceps brachii muscle thickness; and f,
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biceps brachii muscle fascia to brachialis muscle.
Figure 3. Effects of 12-week involuntary eccentric contraction training on maximum isometric elbow flexion torque. (A) The individual subjects’ torques of the trained and untrained sides are shown at baseline (Pre) and after the training (Post). The torque data were normalized by the individual subjects’ weight. The torque of the trained side increased, but that of the untrained side showed an irregular tendency. (B) The group changes in torque are shown at Pre and Post. The changes in torque are expressed as a post/pre ratio for the trained and untrained sides. The change in torque was statistically significant on the trained side only.
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Figure 4. Effects of 12-week involuntary eccentric contraction training on biceps brachii muscle thickness of the trained side. (A) The individual subjects’ muscle thicknesses at rest and at
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maximum voluntary contraction (MVC) are shown at baseline (Pre) and after the training (Post).
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The thickness increased both at rest and at MVC. (B) The group changes in thickness at rest and
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at MVC are shown at Pre and Post. The changes in thickness are expressed relative to the initial thickness at Pre. The changes in muscle thickness are statistically significant at both rest and
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MVC.
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Figure 5. Performance enhancements in maximum isometric flexion torque as a function of
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changes in the square of the muscle thickness. The abscissa indicates the biceps brachii muscle
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thickness at MVC; the ordinate shows the maximum isometric flexion torque. Based on the good linear relationship between the two variables, the strength gains of the biceps brachii muscles appear to result in enhancements of the torque performance.
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Figure 1
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Figure 2
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Figure 4
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Figure 3
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Figure 5
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Highlights
An involuntary eccentric contraction system was designed with NMES.
The system was applied to biceps brachii of 7 healthy men for 12-week training.
Isometric elbow flexion torques of trained side significantly increased around 23%.
Isometric elbow flexion torques of untrained side showed no significant changes.
The muscle thickness significantly increased around 16% at MVC.
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