Gait training with auditory feedback improves trunk control,muscle activation and dynamic balance in patients with hemiparetic stroke: A randomized controlled pilot study

Abstract

BACKGROUND:

Auditory feedback enables an individual to identify and modify the differences between actual and intended movement during the motor learning process.

OBJECTIVE:

We investigated the effects of gait training with auditory feedback on trunk control, muscle activation, and dynamic balance in patients with hemiparetic stroke.

METHODS:

Twenty participants with hemiparetic stroke were recruited in this study and randomly assigned to the experimental ( $n=$ 10) or control ( $n=$ 10) group. The subjects in the experimental group participated in gait training with auditory feedback for 30 minutes, 5 times a week, for 4 weeks, whereas those in the control group received conventional gait training for 30 minutes, 5 times a week, for 4 weeks. During auditory feedback training, a beeping sound is produced every time a patient loaded weight that was higher than the preset threshold on the cane. Activation of the erector spinae muscle was measured using surface electromyography, and trunk control was evaluated using the Trunk Impairment Scale (TIS). Dynamic balance was measured using the Timed Up and Go (TUG) test.

RESULTS:

Muscle activation was significantly higher in the experimental group than in the control group (6.6 $\pm$ 9.2% vs 1.4 $\pm$ 5.4% nonparetic peak activity). No significant difference was found in the TIS score between the experimental and control groups. Based on the TUG test, a significant improvement was observed in the experimental group compared to the control group (12.1 $\pm$ 11.4 vs 3.8 $\pm$ 4.7 s).

CONCLUSION:

Our findings indicate that gait training with auditory feedback was beneficial for improving trunk control and muscle activation in patients with hemiparetic stroke.

Keywords

Biofeedback cane stroke trunk control

1. Introduction

A survey conducted among stroke patients regarding their use of walking aids 6 months after stroke revealed that more than 30% of patients can hardly walk without walking aids [1, 2, 3]. A cane provides stability to patients with decreased muscle strength, such as patients with stroke or those with unstable gait, by increasing the base of support [4, 5]. Kuan et al. [6] have assessed the effects of using a cane on walking and reported a significant increase in stride length, step length of the affected side, and walking speed and improved gait with decreased circumduction gait as hip adduction, knee flexion, and ankle dorsiflexion angles increased during the swing phase.

The use of a cane is believed to encourage a patient to lean over to the non-affected side, which reduces weight bearing on the affected side. In addition, a significant relationship was observed between asymmetric trunk movement and walking ability [7]. The function of the erector spinae is to decelerate the contralateral pelvic drop during the terminal stance and maintain normal trunk alignment during walking with lumbar extension [8]. Buurke et al. [9] reported that the use of a cane decreases the muscle activity and burst duration of the erector spinae in patients with stroke.

Auditory feedback mediated by a pressure sensor can provide additional information about posture regulation in patients with disrupted senses and can repeatedly stimulate the affected side via goal-oriented training [10]. Furthermore, it is an effective measure that prevents secondary impairment caused by disuse.

A study that provided auditory feedback for weight support on the affected foot and single-limb support time has revealed a significant improvement in walking speed and symmetry [11]. Another cross-sectional study has reported that limiting dependency on a cane results in improved pelvic stability caused by increased muscle activation [12]. Furthermore, Jung et al. [13] have reported a significant increase in the activity of the gluteus and vastus medialis oblique and single-limb support time of the affected leg after providing auditory feedback correlated to weight bearing on the cane. However, trunk control was not assessed.

Research on gait training using a cane and auditory feedback in patients with stroke has not been conducted, and whether such training can improve trunk control has not been investigated in previous studies. Therefore, this study aimed to assess the effects of gait training with a cane and augmented pressure sensor on trunk control, muscle activation, and balance in patients with hemiparetic stroke.

2. Methods

2.1 Subjects

Twenty patients with hemiparetic stroke were recruited in this study and were assigned to either the experimental ( $n=$ 10) or control ( $n=$ 10) group. The inclusion criteria were as follows: diagnosis of first unilateral hemispheric stroke; ability to walk with a cane (functional ambulation classification, 2–3); ability to understand and follow simple verbal instructions; no impaired touch and pressure sensation on the unaffected hand; no hemineglect; and no orthopedic disease influencing gait. Table 1 shows the general characteristics of the experimental and control groups. After being informed about the study, all subjects agreed to participate and signed a consent form. The study was approved by the institutional review board of Sahmyook University.

Table 1
Demographic and clinical characteristics of the participants

Variable	Experimental group ( $n=$ 10)	Control group ( $n=$ 10)	$p$
Gender
Male, $n$ (%)	7 (70%)	7 (70%)
Female, $n$ (%)	3 (30%)	3 (30%)	0.999 ${}^{\text{a}}$
Age (years)	57.1 $\pm$ 11.4	56.3 $\pm$ 17.1	0.981 ${}^{\text{b}}$
Weight (kg)	67.7 $\pm$ 11.0	61.6 $\pm$ 7.1	0.157 ${}^{\text{b}}$
Height (cm)	164.1 $\pm$ 8.5	165.7 $\pm$ 6.3	0.639 ${}^{\text{b}}$
Stroke type
Ischemic, $n$ (%)	7 (70%)	8 (80%)	0.606 ${}^{\text{a}}$
Hemorrhagic, $n$ (%)	3 (30%)	2 (20%)
Affected side
Right, $n$ (%)	3 (30%)	3 (30%)
Left, $n$ (%)	7 (70%)	7 (70%)	0.999 ${}^{\text{a}}$
Post-stroke duration (months)	6.3 $\pm$ 2.6	7.0 $\pm$ 2.5	0.552 ${}^{\text{b}}$
MMSE	26.9 $\pm$ 2.0	27.3 $\pm$ 2.4	0.689 ${}^{\text{b}}$
FAC	1 $\sim$ 2	1 $\sim$ 2	0.999 ${}^{\text{a}}$

MMSE, Mini-Mental State Examination; FAC, Functional ambulation classification. Unless otherwise stated, data are mean $\pm$ SD. ${}^{\text{a}}$ chi-squared test. ${}^{\text{b}}$ independent $t$ -test.

2.2 Procedures

This was a pilot, assessor-blinded, randomized controlled trial (RCT). The patients included in the study were randomly assigned to either the experimental or control group using a selection envelope. The participants in the experimental group participated in gait training with auditory feedback for 30 minutes, 5 times a week, for 4 weeks, whereas those in the control group engaged in conventional gait training without auditory feedback for 30 minutes, 5 times a week, for 4 weeks. All participants underwent a conventional exercise program provided by the rehabilitation hospital for 30 minutes, 5 times a week, for 4 weeks. Subjects in the experimental group underwent gait training with auditory feedback. Subjects in the control group received conventional gait training without auditory feedback.

2.3 Interventions

The cane was designed to provide auditory feedback, and it had a pressure sensor and portable indicator. The pressure sensor was used to measure the peak vertical force on the cane, and the portable indicator produced a beeping sound whenever the participants pressed the cane with a higher force than the threshold. The participants were instructed to avoid triggering the beeping sound during gait training and to hold the cane using the nonparetic hand, and the height of the cane was adjusted at the level of the participants’ greater trochanter. To ensure safety, two therapists walked alongside each participant during training.

Prior to the training, the threshold was set every week for each participant based on the level of dependency, which was calculated using the following formula: peak vertical force/body weight $\times$ 100 [14]. The initial threshold was set at 60% of the level of dependency and was decreased by 10% every week. The number of steps was measured using a counter application, developed for a smartphone, during each session of gait training. The threshold was decreased once the participants could walk without producing a beeping sound for more than 80% of the total number of steps on the paretic side.

2.4 Outcome measurements

Two physical therapists who were not involved in the study evaluated the participants.

Data about peak vertical force on the cane, trunk muscle activation, TIS score, and TUG score before and after the training were collected. All participants were instructed to walk 7 meters at a usual pace. The instrumented cane was used to measure the amount of peak vertical force on the cane whenever a participant pushed the cane. Data about force were collected simultaneously at a sampling rate of 100 Hz and were recorded using a cable connecting the indicator to a computer. The average force data from 10 gait cycles and the percentage of body weight were calculated.

In terms of gait, the activity of the erector spinae was measured using surface electromyography (EMG) (Telemyo 2400 G2, Noraxon, USA, 2007). To minimize skin resistance, hair was removed, and the skin was cleaned with alcohol before the electrodes were attached. The electrodes were placed parallel to the spine, 2 cm apart from the spine [15]. The sampling rate for EMG was set at 1500 Hz, and the band-pass filter was set to a bandwidth of 16–500 Hz. After performing full-wave rectification on the EMG signals of the measured muscle activity, the root mean square (RMS) values were recorded. The EMG data were normalized to the peak activity of the same muscles on the nonparetic side [16]. To measure the peak activity of the erector spinae, the participants were asked to lie face down and lift the upper body against resistance. A foot switch was attached to the heel and the first metatarsal bone to record gait cycle. The activity of the erector spinae muscle during the paretic stance phase of the gait cycle was analyzed. An average of 10 gait cycles during a 7-meter walk was used as the mean value (%) of nonparetic peak activity.

The TIS comprises the following subscales: static sitting balance, dynamic sitting balance, and coordination. The TIS scores range from 0 to 23. Higher scores indicate better trunk performance. The TIS is a reliable tool for measurement, with an ICC (r) of 0.96 for test-retest reliability and inter-rater reliability of 0.99 [17, 18].

The TUG test is used to examine the dynamic balance associated with rising from a chair, turning, and sitting down [19], and it has high intra-rater ( $r=$ 0.99) and inter-rater ( $r=$ 0.98) reliabilities [20].

Table 2
Changes in the functional scores in the experimental and control groups

Variables	Experimental group				Control group				Time x group	Between group
	( $n=$ 10)				( $n=$ 10)				interaction	effects
	Pre-test		Post-test		Pre-test		Post-test		$p$	$p$
Peak vertical force on cane (% BW)	10.05	$\pm$ 3.11	3.01	$\pm$ 2.29 ${}^{*,\text{a}}$	10.28	$\pm$ 4.93	5.83	$\pm$ 3.94 ${}^{*,\text{b}}$	0.017	0.023 ${}^{\text{c}}$
Muscle activation (% peak activity)	17.97	$\pm$ 5.61	24.60	$\pm$ 9.85 ${}^{*,\text{b}}$	22.59	$\pm$ 14.30	21.17	$\pm$ 13.65 ${}^{\text{a}}$	0.028	0.035 ${}^{\text{c}}$
Trunk impairment scale (score)
Static	5.90	$\pm$ 0.88	6.50	$\pm$ 0.71 ${}^{*,\text{b}}$	5.60	$\pm$ 1.35	6.00	$\pm$ 1.25 ${}^{\text{a}}$	0.530
Dynamic	4.10	$\pm$ 1.20	5.70	$\pm$ 2.26 ${}^{*,\text{a}}$	4.60	$\pm$ 0.70	6.10	$\pm$ 1.37 ${}^{*,\text{b}}$	0.898
Coordination	2.50	$\pm$ 1.27	3.0	$\pm$ 0.94 ${}^{*,\text{a}}$	2.6	$\pm$ 1.17	2.8	$\pm$ 1.32 ${}^{\text{b}}$	0.177
Total	12.50	$\pm$ 2.17	15.2	$\pm$ 2.97 ${}^{*,\text{a}}$	12.8	$\pm$ 1.75	14.9	$\pm$ 2.38 ${}^{*,\text{a}}$	0.476
TUG (s)	33.66	$\pm$ 22.99	21.52	$\pm$ 12.34 ${}^{*,\text{b}}$	33.88	$\pm$ 18.08	30.11	$\pm$ 13.92 ${}^{*,\text{b}}$	0.046	0.015 ${}^{\text{c}}$

BW, Body weight; TUG, Timed Up and Go test. ${}^{*}$ Significant difference between pre- and post-test. ${}^{\text{a}}$ Paired $t$ test. ${}^{\text{b}}$ Wilcoxon signed-rank test. ${}^{\text{c}}$ Mann-Whiney U test.

2.5 Statistical analysis

The Statistical Package for the Social Sciences software for Windows version 23.0 (SPSS Inc., Chicago, IL, USA) was used for data analysis. The normality of variables was assessed using the Shapiro-Wilk test. The independent $t$ -test (for continuous variables) and chi-squared test (for categorical variables) were used for the comparison of baseline characteristics between the experimental and control groups. Two-by-two mixed factorial analysis of variance (ANOVA) was conducted to compare pre- and post-test time with respect to the effect of gait training with auditory feedback on peak vertical force on the cane, muscle activation, TIS score, and TUG test score. The paired $t$ -test and Wilcoxon signed-rank test were used as a simple effects analysis in each group when a significant interaction was observed between auditory feedback and time. The Mann-Whitney U test was also used to compare pre- to post-test changes between the groups. The significance level was set at $p<$ 0.05.

3. Results

A two-by-two mixed factorial ANOVA yielded a significant interaction between auditory feedback (experimental vs. control group) and time (pre- and post-test) in terms of peak vertical force on the cane (F (1, 18) $=$ 6.955, $p=$ 0.017). These results indicated a significant decrease from pre- to post-exercise in the experimental and control groups. A simple effects analysis of the intervention indicated that the means between the pre- and post-test significantly decreased in both the experimental group (10.05 $\pm$ 3.11 vs. 3.01 $\pm$ 2.29, $p<$ 0.001) and the control group (10.28 $\pm$ 4.93 vs. 5.83 $\pm$ 3.94, $p=$ 0.005). In addition, a significant difference was observed in the mean changes from pre- to post-test between the two groups ( $p=$ 0.023, Table 2).

A significant relationship was found between auditory feedback and time in terms of muscle activation (F (1, 18) $=$ 5.687, $p=$ 0.028). These results indicated a significant increase from pre- to post-exercise in the experimental and control groups. Muscle activation between pre- and post-test significantly increased in the experimental group (17.97 $\pm$ 5.61 vs. 24.60 $\pm$ 9.85, $p=$ 0.028), but not in the control group (22.59 $\pm$ 14.30 vs. 21.17 $\pm$ 13.65, $p=$ 0.423). In addition, the experimental group had a significantly higher change in mean muscle activation between pre- and post-test than the control group ( $p=$ 0.035, Table 2).

Similarly, a significant relationship was observed between auditory feedback and time in terms of TUG test score (F (1, 18) $=$ 4.613, $p=$ 0.046). These results indicated a significant decrease from pre- to post-exercise in the experimental and control groups. A simple effects analysis of the intervention showed a significant decrease in TUG test score in both the experimental group (33.66 $\pm$ 22.99 vs. 21.52 $\pm$ 12.34, $p=$ 0.005) and the control group (33.88 $\pm$ 18.1 vs. 30.11 $\pm$ 13.92, $p=$ 0.028) and a significant between-group effect ( $p=$ 0.015, Table 2).

The TIS static, and dynamic balance, coordination, and total score improved in the experimental and control groups between pre- and post-test. The relationship between auditory feedback and time was not significantly different in terms of TIS static, and dynamic balance, coordination, and total score.

4. Discussion

This study revealed a significant improvement in the activity of the erector spinae during walking based on the assessment of the effects of gait training with the use of a cane along with auditory feedback on the activity of trunk muscles in patients with hemiparetic stroke. Walking involves adjusting to continuous imbalance and moving forward during the stance phase [21].

Displacement of the center of gravity should be minimized to reduce energy consumption, and appropriate muscle activation is required. Buurke et al. [9] have compared the muscle activity pattern in patients with stroke with and without the use of a cane and reported that the activity and contraction duration of the erector spinae decreased during walking with a cane. The outcome was attributed to a decreased need to generate muscle force owing to weight-bearing on the cane [22]. In this study, the activity of the erector spinae significantly increased after training, which might be attributed to training with auditory feedback as it reduces weight bearing against the cane, thereby facilitating walking in the upright position. Batavia et al. [23] have indicated that the use of auditory feedback improves postural control through constant auditory stimulus to remind the patient to maintain midline. Auditory feedback is mainly applied during the single-limb support phase of the affected side, where the non-affected foot is lifted from the ground surface. This action facilitates symmetric posture and activates the antigravity muscle activity of the affected side by moving the weight supported by the cane to the affected side [12].

In addition, we assessed the effect of training on the improvement of trunk control. However, the result was not significant. The TIS is a tool used for evaluating trunk control ability in sitting position. In this study, the tool was not considered effective since the training was performed in standing rather than sitting position. Therefore, further study must be conducted to evaluate the effect on improving trunk control during walking via a movement analysis.

Balance control during walking in patients with stroke is not automatically regulated at the level of the spinal cord and brainstem. However, it is significantly affected by conscious cortical regulation [24, 25]. Wulf et al. [26] have reported that augmented feedback stimulates movement control in a more automatic manner by repeatedly reminding the patient of the movement goal during training. In addition, to maintain balance in a situation where the center of gravity and base of support are continuously changing, such as during walking, coordinated activity of the limb and trunk muscles is required [27]. In this study, we observed a significant decrease in the TUG test score after training, which is attributed to the improvement in trunk stability during the stance phase after the increase in the activity of the erector spinae during walking. The relationship between trunk control and walking ability has been observed in participants with stroke [28]. Boonsinsuku et al. [12] have reported improved muscle activation and pelvic stability when the vertical peak force on the cane was decreased as dependency on the cane was reduced. Furthermore, in this study, the training method, which involved repeated weight-bearing on the affected side of the body, could have improved the muscular strength of the affected leg and eventually walking speed. Jung et al. have reported that gait training with auditory feedback improves muscle activities in the affected leg.

This study validated that gait training with a cane and auditory feedback improved the activity of the erector spinae and balance in patients with hemiparetic stroke. However, the result could not be generalized due to the small number of participants and lack of follow-up. Therefore, further study must be conducted to assess the effects of gait training with a cane and auditory feedback on trunk kinematics during walking in patients with stroke.

Footnotes

Acknowledgments

This work was supported by the Gimcheon University Research Grant.

Conflict of interest

The authors have no conflict of interest to declare.

References

Jorgensen

Nakayama

Raaschou

Olsen

. Recovery of walking function in stroke patients: the Copenhagen Stroke Study. Arch Phys Med Rehabil 1995; 76: 27-32.

Mayo

Wood-Dauphinee

Cote

Durcan

Carlton

. Activity, participation, and quality of life 6 months poststroke. Arch Phys Med Rehabil 2002; 83: 1035-42.

Patel

Duncan

Lai

Studenski

. The relation between impairments and functional outcomes poststroke. Arch Phys Med Rehabil 2000; 81: 135-63.

Laufer

. Effects of one-point and four-point canes on balance and weight distribution in patients with hemiparesis. Clin Rehabil 2002; 16: 141-8.

Laufer

. The effect of walking aids on balance and weight-bearing patterns of patients with hemiparesis in various stance positions. Phys Ther 2003; 83: 112-22.

Kuan

Tsou

. Hemiplegic gait of stroke patients: the effect of using a cane. Arch Phys Med Rehabil 1999; 80: 777-84.

Tyson

. Trunk kinematics in hemiplegic gait and the effect of walking aids. Clin Rehabil 1999; 13: 295-300.

Perry

. Gait analysis. normal and pathological function. Slack New Jersey. 1992.

Buurke

Hermens

Erren-Wolters

Nene

. The effect of walking aids on muscle activation patterns during walking in stroke patients. Gait Posture 2005; 22: 164-70.

10.

Oscari

Secoli

Avanzini

Rosati

Reinkensmeyer

. Substituting auditory for visual feedback to adapt to altered dynamic and kinematic environments during reaching. Exp Brain Res 2012; 221: 33-41.

11.

Sungkarat

Fisher

Kovindha

. Efficacy of an insole shoe wedge and augmented pressure sensor for gait training in individuals with stroke: a randomized controlled trial. Clin Rehabil 2011; 25: 360-9.

12.

Boonsinsukh

Panichareon

Phansuwan-Pujito

. Light touch cue through a cane improves pelvic stability during walking in stroke. Arch Phys Med Rehabil 2009; 90: 919-26.

13.

Jung

Kim

Cha

, et al. Effects of gait training with a cane and an augmented pressure sensor for enhancement of weight bearing over the affected lower limb in patients with stroke: a randomized controlled pilot study. Clin Rehabil 2015; 29: 135-42.

14.

Chen

Wong

, et al. Temporal stride and force analysis of cane-assisted gait in people with hemiplegic stroke. Arch Phys Med Rehabil 2001; 82: 43-48.

15.

Cram

Kasman

, Holtz. Introduction to surface electromyography. 1993. Washington. Aspen publisheres.

16.

Maguire

Sieben

Erzer

, et al. How to improve walking, balance and social participation following stroke: a comparison of the long term effects of two walking aids canes and an orthosis TheraTogs on the recovery of gait following acute stroke. A study protocol for a multi-centre, single blind, randomised control trial. BMC Neurol 2012; 12: 18.

17.

Verheyden

Kersten

. Investigating the internal validity of the Trunk Impairment Scale (TIS) using Rasch analysis: the TIS 2.0. Disabil Rehabil 2010; 32: 2127-37.

18.

Verheyden

Nieuwboer

Mertin

, et al. The Trunk Impairment Scale: a new tool to measure motor impairment of the trunk after stroke. Clin Rehabil 2004; 18: 326-34.

19.

Podsiadlo

Richardson

. The timed “Up & Go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc 1991; 39: 142-8.

20.

Hui-Chan

. The timed up & go test: its reliability and association with lower-imb impairments and locomotor capacities in people with chronic stroke. Arch Phys Med Rehabil 2005; 86: 1641-7.

21.

MacKinnon

Winter

. Control of whole body balance in the frontal plane during human walking. J Biomech 1993; 26: 633-44.

22.

Hof

van den Berg

. Linearity between the weighted sum of the EMGs of the human triceps surae and the total torque. J Biomech 1997; 10: 529-39.

23.

Batavia

Gianutsos

Kambouris

. An augmented auditory feedback device. Arch Phys Med Rehabil 1997; 78: 1389-92.

24.

Maki

McIlroy

. Cognitive demands and cortical control of human balance-recovery reactions. J Neural Transm 2007; 114: 1279-96.

25.

Mochizuki

Sibley

Cheung

Camilleri

McIlroy

. Generalizability of perturbation evoked cortical potentials: independence from sensory, motor and overall postural state. Neurosci Lett 2009; 451: 40-4.

26.

Wulf

McConnel

Gartner

Schwarz

. Enhancing the learning of sport skills through external-focus feedback. J Mot Behav 2002; 34: 171-82.

27.

Karatas

Cetin

Bayramoglu

Dilek

. Trunk muscle strength in relation to balance and functional disability in unihemispheric stroke patients. Am J Phys Med Rehabil 2004; 83: 81-7.

28.

Verheyden

Vereeck

Truijen

, et al. Trunk performance after stroke and the relationship with balance, gait and functional ability. Clin Rehabil 2006; 20: 451-8.

Gait training with auditory feedback improves trunk control,muscle activation and dynamic balance in patients with hemiparetic stroke: A randomized controlled pilot study

Abstract

BACKGROUND:

OBJECTIVE:

METHODS:

RESULTS:

CONCLUSION:

Keywords

1. Introduction

2. Methods

2.1 Subjects

Table 1 Demographic and clinical characteristics of the participants

2.3 Interventions

2.4 Outcome measurements

Table 2 Changes in the functional scores in the experimental and control groups

3. Results

4. Discussion

Footnotes

Acknowledgments

Conflict of interest

References

Table 1
Demographic and clinical characteristics of the participants

Table 2
Changes in the functional scores in the experimental and control groups