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NeuroRehabilitation 35 (2014) 681–688 DOI:10.3233/NRE-141182 IOS Press

Intensive gait training with rhythmic auditory stimulation in individuals with chronic hemiparetic stroke: A pilot randomized controlled study Yuri Chaa , Young Kima , Sujin Hwangb and Yijung Chungc,∗ a Department

of Physical Therapy, The Graduate School, Sahmyook University, Seoul, Republic of Korea of Physical Therapy, Division of Health Science, Baekseok University, Cheonan, Republic of Korea c Department of Physical Therapy, College of Health and Welfare, Sahmyook University, Seoul, Republic of Korea b Department

Abstract. BACKGROUND: Motor relearning protocols should involve task-oriented movement, focused attention, and repetition of desired movements. OBJECTIVES: To investigate the effect of intensive gait training with rhythmic auditory stimulation on postural control and gait performance in individuals with chronic hemiparetic stroke. METHODS: Twenty patients with chronic hemiparetic stroke participated in this study. Subjects in the Rhythmic auditory stimulation training group (10 subjects) underwent intensive gait training with rhythmic auditory stimulation for a period of 6 weeks (30 min/day, five days/week), while those in the control group (10 subjects) underwent intensive gait training for the same duration. Two clinical measures, Berg balance scale and stroke specific quality of life scale, and a 2-demensional gait analysis system, were used as outcome measure. To provide rhythmic auditory stimulation during gait training, the MIDI Cuebase musical instrument digital interface program and a KM Player version 3.3 was utilized for this study. RESULTS: Intensive gait training with rhythmic auditory stimulation resulted in significant improvement in scores on the Berg balance scale, gait velocity, cadence, stride length and double support period in affected side, and stroke specific quality of life scale compared with the control group after training. CONCLUSIONS: Findings of this study suggest that intensive gait training with rhythmic auditory stimulation improves balance and gait performance as well as quality of life, in individuals with chronic hemiparetic stroke. Keywords: Gait, rhythmic auditory stimulation, stroke

1. Introduction In most stroke survivors, weakness of one side of the body, hemiparesis or hemiplegia, following stroke, has been demonstrated. These impairments give rise to serious problems related to postural control and gait performance, such as postural instabilities, postu∗ Address

for correspondence: Yijung Chung, P.T., Ph.D., Department of Physical Therapy, College of Health and Welfare, Sahmyook University, P.O.Box. Hwarangro 815, Nowon-gu, Seoul 139-800, Republic of Korea. Tel.: +82 2 3399 1637; Fax: +82 3399 1639; E-mail: [email protected].

ral asymmetry, walking speed, cadence, stride length, increased double support period, reduced single support period, and so forth (Dobkin, 2003). In research and clinical fields, protocols for restoration or remediation for improvement of these abnormalities have been suggested. In particular, motor relearning protocols should involve task-oriented movement, focused attention, and repetition of desired movements (Daly & Ruff 2007; Schmid et al., 2007). Intensive training with desired movement has been used to produce functional gains after spontaneous neurological recovery. For repetition of desired

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Y. Cha et al. / Intensive gait training with rhythmic auditory stimulation in individuals

movements, rhythmic auditory stimulation training is a typical therapeutic approach. Rhythmic auditory stimulation involves external rhythmic cueing to facilitate intrinsically and biologically rhythmic movements using a therapeutic approach, and planning of motor programming and execution through a strong synchronization effect of repetitive rhythmic sensory signal on the motor system (Conesa et al., 2012; Fritz et al., 2011). The pattern of movement can be regulated and influenced by the repeating cue of a rhythmic auditory stimulation, and the reticulospinal tract plays a role for optimal coordination and pattern of movement in human (Thaut 2003). One of main possible explanation is that the spinal motor neurons become excitable with repetitive rhythmic sound patterns through the reticulospinal pathway, thus allowing the incorporation of coordinated axial and proximal movement upon motor command. It is also possible that subcortical neuronal loops may be activated by rhythmical auditory cues, and may subsequently augment balance control and adjust the coordination of bilateral trunk and proximal muscles driven by reactive feedback. Previous studies have examined the efficacies of motor synchronization using rhythmic auditory stimulation to improve gait deficits in several neurological populations, such as Parkinson’s disease, stroke, cerebral palsy, multiple sclerosis and traumatic brain injury (Conklyn et al., 2010; Hurt et al., 1998; Kadivar et al., 2011; Kim et al., 2012; Roerdink et al., 2007; Thaut et al., 2007). However, these research studies have used different types of therapeutic protocols involving control of step length, gait velocity, terrain, direction, and so forth. For stroke rehabilitation, rhythmic auditory stimulation has typically been used for improvement of upper and lower extremity function (Malcolm et al., 2009; Thaut et al., 2007; Whitall et al., 2000). Therefore, the necessity of gait training with rhythmic auditory stimulation for stroke patients will increase. The objective of the present study was to evaluate the efficacy of intensive gait training with rhythmic auditory stimulation on improvement of postural control, spatiotemporal gait parameters, and quality of life in individuals with chronic hemiparetic stroke. This study employed a protocol for rhythmic auditory stimulation using three different cadences in intensive gait training for patients with chronic hemiparetic stroke. It was hypothesized that intensive gait training with rhythmic auditory stimulation would be more effective in maintaining treatment effects compared to only intensive gait training. The outcome measures used in this study includes the Berg balance scale (BBS) and the Stroke

Specific Quality of Life scale (SS-QOL). For kinematic measurements, a 2-demensional gait analysis system was used.

2. Methods 2.1. Participants Twenty patients with chronic hemiparetic stroke were recruited from the H hospital, and were assigned randomly to two groups, including Rhythmic auditory stimulation (RAS) training and control groups. Criteria for inclusion of participants were (1) at least six months since a clinical diagnosis of ischemic or hemorrhagic hemiparetic stroke; (2) sufficient cognitive ability to participate, as indicated by a Mini-Mental State Examination score of 20 or higher; (3) Brunnstrom stage III or IV in the proximal and distal parts of the lower extremity; and (4) no serious auditory or visual deficits. The exclusion criteria included (1) a symptomatic cardiac failure or unstable angina, (2) uncontrolled hypertension, (3) significant orthopedic or chronic pain conditions affecting gait performance, and (4) any neurologic disease except for the initial stroke. Table 1 shows a list of the general characteristics of subjects in the RAS training and control groups. After being informed, all subjects agreed to participate in the study and signed a consent form. The study was approved by the Institutional Review Board of S University. 2.2. Protocol This study was a pretest-posttest design, and the subjects were randomly assigned to either and RAS training or control group using sealed envelopes. Subjects in the RAS training group underwent intensive gait training with rhythmic auditory stimulation for a period of six weeks; five times per week for 30 minutes per session while those in the control group underwent the intensive gait training for the same period. All participants also received general physical therapy, including Bobath approach and proprioceptive neuromuscular facilitation for 30 minutes per day, five times per week. All patients went through pre- and post-testing the day before commencement and the day after conclusion of the training. 2.3. Intervention Subjects in the RAS training group conducted the intensive gait training with rhythmic auditory

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Table 1 Common and clinical characteristics of the subjects (N = 20) RAS training group (n = 10) Gender (number) Male Female Age (yr) Height (cm) Weight (kg) Mini-Mental State Examination Post-Stroke duration (mo) Paretic side Right Left

6 4 59.8 ± 11.7 167.4 ± 5.5 67.0 ± 11.2 26.6 ± 2.1 14.5 ± 5.5 1 9

Control group (n = 10) 6 4 63.0 ± 14.1 165.8 ± 7.6 66.9 ± 10.2 26.1 ± 1.8 14.7 ± 5.4

X2 /t

p

0.220

0.639

−0.552 0.532 0.021 0.578 0.154 0.000

0.588 0.597 0.984 0.570 879 1.000

1 9

RAS, Rhythmic auditory stimulation. Value = mean ± standard deviation.

stimulation, while those in the control group underwent intensive gait training. For gait training in the RAS training group, patients used a metronome and specifically prepared music tapes. To prepare the music, we asked the participants of their preference either pop or country music. Then we asked the music specialist to play three songs emphasizing the rhythms based on selected music. For this process, a synthesizer keyboard (KURZWEIL SP88, Young Chang Co., Ltd.,) was used, along with the MIDI Cuebase musical instrument digital interface program (Cubase MIDI Program, Steinberg, German), and a KM Player version 3.3 (KMP media Inc.) was used to control the rhythmic tempo in each participant. A metronome was played over the beat of the music in order to enhance the rhythmic perception for the patient. The metronome was set up so that it matched directly with the participant’s step pattern. The playback equipment and speakers were placed in a quiet therapy room where the music was the most audible. First, subjects were asked to move around the roundtrack at a self-selected, comfortable pace for a period of two minutes to establish a baseline cadence of rhythmic auditory stimulation. Baseline cadence was measured three times per two weeks for a progressive protocol, depending on patients’ ability. The participants went through a total of 6 weeks of training and the cadence speed was reassessed every two weeks. On the third and the fifth week, the rhythm frequency was increased by 5%. Subjects in the RAS training group underwent intensive gait training with rhythmic auditory stimulation according to a three-section protocol, including intensive gait training with rhythmic auditory stimulation for two sessions, and without rhythmic auditory stimulation for one session. The protocol used for the rhythmic auditory stimulation training was as follows:

Step 1. The participants were exposed to the music to become familiar with the rhythmic auditory stimulation while moving the hands and feet onto the beat (one minute). To do fitted step easily, a participant was instructed to walk and match him/herself to the beat of the music and metronome simultaneously. Step 2. Rest while sitting on a chair (two minutes). Step 3. Repeat step 1. Step 4. Participants underwent intensive gait training with rhythmic auditory stimulation (10 minutes). Participants were instructed to walk and match with the rhythmic stimulation using music and a metronome through careful listening. Step 5. Rest while sitting on a chair (two minutes). Step 6. Repeat step 4. Step 7. The final step involved intensive gait practice without rhythmic auditory stimulation (four minutes). Two therapists stood beside and observed a participant to assist or provide feedback if necessary. Subjects in the control group trained for the same amount of time and distance with equivalent instructions regarding speed improvement, without the utilization of rhythmic auditory stimulation. 2.4. Outcome measures In this study, the BBS, GAITRite, multifunction force measuring plate, and SS-QOL were used for assessment of the effects of rhythmic auditory stimulation for patients with stroke (Blum and Korner-Bitensky 2008; Kuys et al. 2011; Williams et al. 1999). The BBS, a performance-based measure developed by Kathy Berg, is a widely used test for assessment of the ability

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Y. Cha et al. / Intensive gait training with rhythmic auditory stimulation in individuals

of subjects to maintain upright posture and to make appropriate adjustments for voluntary movement in older persons and individuals with neurological disorders (Berg et al., 1995). The BBS consists of 14 different items, including a 5-point scale, range 0 (minimum) to 4 (maximum), with a maximum possible score of 56 points. The BBS has demonstrated good test-retest and interrater reliability and good internal consistency in patients with chronic stroke (Blum & Korner-Bitensky 2008). The GAITRite is a validated measurement of the spatiotemporal parameters of footstep pattern and a pressure-sensitive electronic board consisting of a 5-meter electrical walkway-integrated containing six sensor pads encapsulated in a roll-up carpet to produce an active area measuring 24 inches (61 cm) wide with a height of 0.6 cm. The active area consists of a grid (48 sensors by 288 sensors placed on 0.5 inch [1.27] centers) totaling 16,128 sensors. The device collects the loading of the subject’s feet with a sample rate of 80 Hz per second while he walks on it, and then transmits the data to the computer through a serial interface cable. GAITRite GOLD, Version 3.2b software was used for processing of spatiotemporal data. For this study, subjects were instructed to stand in front of the gait board, and then to walk on it at a self-selected comfortable speed until they reached the end of the board. The SS-QOL was developed as a valid, reliable, and responsive stroke-specific quality of life measure. It consists of 12 different subscales, including mobility (six items), energy (three items), upper extremity function (five items), work/productivity (three items), mood (five items), self-care (five items), social roles (five items), family roles (five items), vision (five items), language (five items), thinking (three items), and personality (three items), range “total help” to “no help needed” and has a maximum possible score of 245 points. The SS-QOL has demonstrated good test-retest reliability and internal consistency in chronic stroke patients (Fernandez-Concepcion et al., 2005). 2.5. Data analysis Stride parameters of five gait cycles were used to assess improvement in gait ability with regard to velocity, stride length on the affected side, cadence, and double support period. Percentage change scores for all gait data were computed for each subject and averaged across groups for statistical analysis. KolmogorovSmirnov was used for the general property and variables

of the subjects. A paired t-test was used for comparison of changes between pretest and posttest in each group. The independent t-test was used for comparison of the difference between postural control and gait performance after training. The significance level was set to P < 0.05. The SPSS 12.0 program was used for statistical analysis.

3. Results Both the RAS training group and the control group included 6 males and 4 females with the mean age of 59.8 ± 11.7 years in the RAS training group and 63.0 ± 14.1 years in the control group. The MiniMental State Examination scores were 26.6 ± 2.1 in the RAS training group and 26.1 ± 1.8 in the control group, and the post-stroke duration was 14.5 ± 5.5 months in the RAS training group and 14.7 ± 5.4 years in the control group (Table 1). The spatiotemporal parameters were compared within the RAS training and control groups. The RAS training group revealed the following: gait velocity 37.4 ± 19.7 to 60.7 ± 27.8 (cm/sec), cadence 71.0 ± 18.2 to 87.2 ± 23.3 (step/min), stride length 61.3 ± 17.3 to 79.8 ± 18.3 (cm) and double support period 44.8 ± 13.5 to 32.6 ± 10.1 (% cycle) on the affected side, and stride length 60.9 ± 16.9 to 75.6 ± 22.9 (cm) and double support period 45.3 ± 14.7 to 32.8 ± 10.4 (% cycle) on the less affected side after training. Gait velocity 37.9 ± 18.3 to 42.0 ± 18.5 (cm/sec), cadence 72.5 ± 22.8 to 76.8 ± 25.3 (step/min), stride length on the affected side 60.9 ± 14.9 to 65.0 ± 15.1 (cm), and stride length on the less affected side 60.4 ± 14.6 to 64.8 ± 15.7 (cm) showed significant improvement in the control group after training (Fig. 1). Scores on the BBS showed significant improvement after training in both the RAS training group 43.5 ± 8.2 to 48.5 ± 7.7 and the control group 41.9 ± 6.9 to 43.6 ± 7.0. Scores of SS-QOL showed significant improvement in both groups after training. Score in the RAS training group showed a change from 158.6 ± 18.3 to 183.7 ± 21.5 and from 153.0 ± 17.1 to 159.2 ± 17.4 in the control group (Fig. 2). Comparison between the two groups showed that gait velocity, cadence, stride length on the affected side, and double support period on the affected side significantly improved in greater amount in the RAS training group than in the control group after training (p < 0.05). Stride length and double support period on the less

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Fig. 1. Comparison of spatiotemporal parameters within the Rhythmic auditory stimulation training and control groups.

affected side did not differ significantly between the two groups after training. Scores from the BBS and SS-QOL showed significantly greater improvements in the RAS training group in comparison with the control group (p < 0.05) (Table 2).

4. Discussion The results of this study demonstrated the positive effects of intensive gait training with rhythmic auditory stimulation on functional balance, locomotion, and

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Y. Cha et al. / Intensive gait training with rhythmic auditory stimulation in individuals

Fig. 2. Comparison of clinical measures within the Rhythmic auditory stimulation training and control groups. Table 2 Pre-test and post-test of clinical measures (N = 20) Variables Berg Balance Scale (score) Gait Velocity (cm/s) Cadence (steps/min) Stride length (cm) Affected side Less affected side Double stance period (% cycle) Affected side Less affected side SS-QoL (score)

RAS training group (n = 10)

Control group (n = 10)

t

p

43.6 ± 7.0 42.0 ± 18.5 76.8 ± 25.3

4.919 2.710 2.321

Intensive gait training with rhythmic auditory stimulation in individuals with chronic hemiparetic stroke: a pilot randomized controlled study.

Motor relearning protocols should involve task-oriented movement, focused attention, and repetition of desired movements...
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