Abstract
BACKGROUND:
Wearable technologies have been developed for healthy aging. The technology for electromyography (EMG)-controlled functional electrical stimulation (FES) systems has been developed, but research on how helpful it is in daily life has been insufficient.
OBJECTIVE:
The purpose of this study was to investigate the effect of the EMG-controlled FES system on muscle morphology, balance, and gait in older adults.
METHODS:
Twenty-nine older adults were evaluated under two randomly assigned conditions (non-FES and FES assists). Muscle morphology, balance, gait function, and muscle effort during gait were measured using ultrasonography, a physical test, a gait analysis system, and EMG.
RESULTS:
The EMG-controlled FES system improved gait speed by 11.1% and cadence by 15.6% (
CONCLUSION:
The EMG-controlled FES system is useful for balance and gait function by increasing muscle symmetry and decreasing muscle coactivation during walking in older adults.
Introduction
As the population of older adults grows, seniors are increasingly interested in pursuing higher physical functions and improving their quality of life, that is, healthy aging, rather than simply extending their lives [1]. Healthy aging is defined as the process by which older adults improve and maintain their functional ability for well-being [2]. Therefore, older adults have complex care demands for healthy aging through independent life [3]. To meet these demands, wearable technology has been developed for simply detecting an emergency situation and preventing accidents, and recently, for the purpose of helping movement using real-time feedback [4, 5, 6]. However, most wearable devices made to help human movement have used mechanical support such as exoskeleton and orthoses type, which required an electric power supply [7, 8]. This type of device has the disadvantages of requiring customization for weight, battery capacity, noise, and cost [9]. Therefore, to overcome the shortcomings of exoskeleton-like equipment, a wearable technology using functional electrical stimulation (FES) has been developed [9, 10].
FES has been used to recover motor function in neurological conditions such as stroke or spinal cord injury, and has been widely used in the field of rehabilitation to improve the decreased muscle strength and performance of the elderly [11, 12]. The repetitive and continuous pattern of FES can lead to changes in the spinal cord synapse between the upper motor neurons and
Therefore, the purpose of this study was to investigate the immediate effects of wearable EMG-controlled FES on the lower limb muscle morphology, balance, and gait in older adults.
Methods
Participants
Twenty-nine individuals (10 men and 19 women), aged 65–84 years, with no history of central nervous system disease or abnormality were recruited for the study. The sample size was calculated using the G-Power program (IBM Inc., USA). On the basis of previous studies, when the effect size was set to 0.56, the power was set to 0.8, and the alpha error was set to 0.05, the minimum sample size was 28 people [16]. The exclusion criteria were as follows: (1) difficulty walking independently owing to problems such as visual field defect, fracture, severe muscle paralysis; (2) poorly controlled hypertension and diabetes; (3) severe dizziness; (4) serious cognitive problems; and (5) other reasons deemed inappropriate by researcher’s judgement. The study was approved by the institutional review board of the University of Sahmyook (2-7001793-AB-N-0120180861HR). All participants provided written informed consent.
Procedures
This study was designed as a crossover study to measure the test conditions. The measurement conditions were EMG-controlled FES with and without assist. All the participants went through the assessment for muscle morphology measurement, balance test, and gait with FES assist (FA) and non-FES assist (NFA) in random order. The participants had sufficient rest between the two tests conditions. EMG-controlled FES electrodes were attached bilaterally to the following lower extremity muscles: the rectus femoris (RF), biceps femoris (BF), tibialis anterior (TA), and medial part of gastrocnemius (GCM). To attach the FES electrodes, we used STIMPLUS (DP-200, CyberMedic, Iksan, Korea) to find the optimal motor point for each muscle. By using a pen-electrode, the skin of the target muscle was pressed gently for around 5 s to find the area where the twitching reaction appeared; the frequency of stimulation was set to 2 Hz using a monophasic wave with a pulse width of 100
EMG and FES electronode attachment locations (A), EMG-controlled FES system (B), and diagram of EMG-controlled FES system (C). vEMG indicates volitional electromyography.
The EMG-controlled FES system (Electronics and Telecommunications Research Institute, ETRI, Deajeon, Republic of Korea) was designed as a gait assistance strategy for older adults (Fig. 1B) and is controlled using a MATLAB-based custom graphical user interface program installed in a personal computer. It is a biofeedback device that extracts volitional EMG (vEMG) signals through dual-channel EMG signal processing algorithms and adjusts the FES intensity based on the signal of pure muscle origin regardless of FES signal interference (Fig. 1C) [18]. The system consists of one FES channel and two EMG channels for each muscle and is attached to a total of eight muscles. The signal received by each EMG channel is expressed as follows:
EMG signals were recorded using custom-developed hardware from the ECG/EEG analog front-end system (ADS-1299, Texas Instruments, Texas, USA). The common mode rejection rate was 110 dB, and the resolution of the signal was 24 bits. The sampling data were collected at 1000 Hz. Raw data were band-pass (10–200 Hz) filtered, and a 300-ms root mean square sliding window function was used for smoothing.
The vEMG raw data measured by the algorithm were automatically filtered and displayed as %MVC and delivered to the connected FES unit to adjust the stimulation pulse in proportion to %MVC in real time. FES stimulation was provided from the point when %MVC exceeded 0, and as %MVC increased, it approached the maximum intensity. The maximum intensity of FES was set to a maximum tolerable level within 10–40 mA of the subject’s painless range. The frequency of FES was fixed at 40 Hz and at a pulse width of 250
The FES unit consists of Rehastim I (Hasomed GmbH, Magdeburg, Germany) and has eight stimulation channels. Rehastim I is a biphasic rectangle pulse with a frequency range of 1–140 Hz, a pulse width range of 20–500
Measurements
Muscle effort
Muscle effort was defined as the mean normalized EMG activity of the lower extremities during the stance and swing phases during gait [8]. It was measured with an EMG-controlled FES system during 5-m walking by dividing the stance and swing phases. The measurements were averaged three times each in accordance with the EMG-controlled FES condition. The stance phase and swing phase events were specified using foot switches located on both heels and the first metatarsal heads. A foot switch is a simple mechanical sensor that can only be turned on/off and detects from heel contact to toe-off.
Muscle morphology
The quadriceps muscle thickness (QMT) is the sum of the thicknesses of the rectus femoris and vastus intermedius [27]. The dual-probe personal-computer-based muscle viewer (DPC-BMW) was used to measure bilateral QMTs simultaneously. The DPC-BMW (MicrUS-duo, TELEMED, Vilnius, Lithuania) linear probe frequency range is 6–14 MHz, with a depth of 4–10 cm, and was preset for optimal muscle image measurement in B-mode [28, 29]. The probe was positioned perpendicular to the longitudinal quadriceps femoris axis midway between the anterior superior iliac spine and the proximal end of the patella [27, 30].
All measurements were performed at rest and maximal voluntary contraction (MVC), and three measurements were taken to calculate the average value. The ultrasonographic measurement protocol for rest and MVC was used based on previous studies [31]. To measure the resting image, the participant rested with the knee slightly flexed with a towel under the knee in a long sitting position on the bed. For MVC images, the isometric contraction was achieved by pressing as much as possible against the towel under the knee. To improve acoustic coupling and image quality, a water-soluble transmission gel was placed on the probe, and the probe’s angle was adjusted slightly [27, 30]. To reduce bias, all measurements were performed by a trained operator [32]. Muscle thickness was calculated using Echo Wave II software, ver. 3.5 (version). DPC-BMW had very good to excellent reliability (ICC
Balance
A short physical performance battery (SPPB) was used to measure the physical function and strength of older adults [34]. The SPPB included the following three tasks: standing balance, 4-m walking, and sit-to-stand. For the standing balance test, the participants held their feet side-by-side for 10 s. We evaluated whether this position could be maintained at the semi-tandem and tandem positions. The 4-m walking test started in the standing position, and we measured the time it took the participants to walk 4 m at a normal pace. The sit-to-stand test measured the time from sitting on a chair to standing five times. Each of the three tasks was rated as 0 (unable to complete) to 4. The total scores ranged from 0 to 12, with higher scores indicating better function and leg strength [35]. The SPPB indicated excellent test-retest reliability (ICC
The timed up-and-go (TUG) test was used to measure the participants’ functional mobility and dynamic balance [37]. The TUG test has good inter-rater reliability (ICC
The four-square step test (FSST) is an effective tool for quickly measuring dynamic standing balance and mobility, and has moderate to strong correlations (
Gait function
The GAITRite system (CIR System Inc., New Jersey, USA) was used to measure the gait function. GAITRite measures temporal and spatial gait parameters on an electronic walkway that is 5 m long, 0.6 m wide, and 0.6 cm high, with 16,128 pressure activated sensors 1 cm in diameter arranged vertically every 1.27 cm. This instrument has an excellent agreement (ICC
The measurement protocol was modified based on previous studies [45]. Older adults walked three times each with the EMG-controlled FES system on and off (six trials in total). Participants walked at a self-selected speed according to the examiner’ s verbal instructions. Each walk was approximately 9 m long: 5 m GAITRite mat and 2 m acceleration and deceleration periods.
Data analysis
EMG data calculation
To compare individual muscle activation patterns during gait, EMG data were normalized to the percentage of MVC (%MVC). As a result, %MVC means muscle effort. To determine the symmetry of bilateral leg muscles in the stance and swing phases during gait, %MVC data were calculated as weakest/strongest, which was defined as the symmetry ratio (SR) [46]. As SR approaches 1, both muscles are symmetrical. Finally, the co-activation index (CI) was calculated to compare the degree of co-activation between agonist and antagonist (RF: BF, TA: GCM) during the gait process [24, 47]:
CI was calculated as the average of 20 strides in each condition.
Ultrasound-image-based calculation
QMT was measured as the distance between the superior border of the subcutaneous fascia and the superior border of the femur [48]. The SR equation was used to compare the symmetry of both QMTs and was defined as the quadriceps symmetry ratio (QSR) [46].
Statistical analysis
PASW Statistics 18 (SPSS Inc., Quarry Bay, Hong Kong) was used for all statistical analyses. The Shapiro-Wilk test was performed to confirm the normality of the subject characteristics. All data are expressed as the mean (SD). A paired
Results
Baseline participant characteristics
The baseline characteristics of the 29 older adults are summarized in Table 1.
Participant characteristics
Participant characteristics
Abbreviations: BMI, Body mass index.
FA gait significantly lowered muscle effort in the right RF and both GCM in the stance phase compared to the NFA gait (
Muscle effort, muscle thickness, physical function and gait function
Muscle effort, muscle thickness, physical function and gait function
Abbreviations: NFA, non-FES assist; FA, FES assist; RF, rectus femoris; BF, biceps femoris; TA, tibialis anterior; GCM, gastrocnemius; QMT, quadriceps muscle thickness; QSR, quadriceps symmetry ratio; SPPB, short physical performance battery; TUG, time up and go test; FSST, four square step test.
Mean (standard deviation) muscle effort (%MVC) of swing phase (A) and stance phase (B), according to each muscle. 
Left and right QMT in FA or NFA gaits were not statistically significant (
Balance
The SPPB showed a statistically significant improvement in the FA condition compared to the NFA condition (
Gait function
Gait speed was significantly faster in the FA condition than in the NFA condition (
Discussion
The purpose of our study was to investigate the effects of EMG-controlled FES on muscle effort, muscle morphology, balance, and gait in older adults.
The results showed that the application of EMG-controlled FES reduced muscle effort during gait in older adults. In particular, bilateral GCM muscle effort was significantly reduced in the stance phase (right 18.18%, left 10.17%). There was no significant difference in the other muscles assessed, but most of them showed a decreasing pattern during the FA gait. This is similar to previous research findings that it is possible to move efficiently by using less energy during trunk forward progression at terminal stance by reducing the muscle consumption rate of GCM through a gait assistance device [8]. Another study found that when performing functional movements such as arm movement, the effort of the muscles used increased in older adults compared to that in young adults [49]. Therefore, in order to use muscles efficiently for gait performance in older adults, muscle effort of the GCM should be set as an important factor. The SR of bilateral GCM muscle effort was significantly improved during FA gait (stance phase, 9%; swing phase, 10.53%). These results are similar to previous studies that single session gait training using FES improved ankle moment symmetry [50]. The degree of co-activation increases with the decrease of strength and neurological function with aging, which means that older adults make joints stiff for stability compared to young adults even if they perform the same task [47]. We confirmed a significant decrease in co-activation in both the thigh (31.06%) and shank (33.58%) during FA gait. Consequently, our results showed that the FA gait was more efficient in muscle effort, and the stiffness of the lower limb joints was reduced, resulting in smooth motion.
In this study, there was no difference in muscle thickness during the MVC of the quadriceps muscle, FA or NFA. The reason for this result is similar to that of a previous study, in which single sessions tended not to elicit morphologic changes such as muscle mass alterations in older adults [51]. However, QSR showed a significant improvement in the FA condition (5.15%). According to previous studies, the increase in knee extensor muscle asymmetry is related to gait asymmetry, and unilateral movement is important during training [52]. Similarly, in this study, the use of EMG-controlled FES led to symmetrical contraction of the quadriceps muscles in the elderly and to a symmetrical pattern of muscle activation during gait. Therefore, the EMG-controlled FES system assists in symmetrical muscle activity.
EMG-controlled FES affected the physical function of older adults. After wearing the EMG-controlled FES equipment, scores improved in the SPPB (5.65%) and FSST (9.68%), indicating that EMG-controlled FES was effective in improving physical performance and balance. This was consistent with the findings of previous studies that reported better gait and balance performance, as well as improved muscle physiology and function in older adults with FES-based training [11].
The gait parameter is an objective evaluation method and is used as an important biomarker in aging and pathological studies [3]. Our results show that FA gait has a positive effect on gait speed (10.9%) and cadence (13.55%) in the elderly. In previous studies, it was reported that when FES was applied, for voluntary muscle contraction, the gait performance of older adults improved higher than when only passive FES was applied [11]. Therefore, it is necessary to compare the difference in the level of balance or gait parameters after training in which the FES intensity is adjusted in real time through EMG-controlled FES and the existing voluntary muscle contraction FES training, in a follow-up study. In another previous study, it was reported that gait speed decreased with increasing co-activation of the agonist and antagonist muscles in the stance and swing phases [24]. Similarly, in our study, gait speed increased and co-activation of the lower limb muscles decreased according to FA in older adults.
Finally, our results demonstrate that the EMG-controlled FES system is a potentially useful gait assist system for improving gait function by increasing the muscle symmetry of the lower limbs and by decreasing muscle co-activation during walking in elderly adults.
The limitation of this study is the small sample size used to support the cross-sectional study design. In addition, it was difficult to accurately determine the effect of EMG-controlled FES because it was aimed at healthy elderly people without gait problems. Therefore, in future research, it will be necessary to proceed with a larger sample size and various groups.
Conclusion
The EMG-controlled FES not only improved balance, walking speed, and muscle morphological ability, but also positively altered the asymmetrical walking pattern in older adults. The proper timing of electrical stimulation also had an effect on the reduction of joint muscle contraction.
This study verified the supplementary effects of electrical stimulation in older adults, and future studies are needed to verify the effects in the long-term, in various groups, and training methods using EMG-controlled FES equipment.
Footnotes
Acknowledgments
This study was supported by the Institute for Information and Communications Technology Promotion (IITP) grant funded by the Korean government (MSIT) (2017-0-00050, Development of Human Enhancement Technology for auditory and muscle support) and by a grant from the NRF (NRF-2016R1A6A3A11930931 and NRF-2018R1D1A1B07042870), which is funded by the Korean government.
Conflict of interest
The authors declare no conflicts of interest.
