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GAIPOS-4469; No. of Pages 6 Gait & Posture xxx (2015) xxx–xxx

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Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost

Treadmill gait training combined with functional electrical stimulation on hip abductor and ankle dorsiflexor muscles for chronic hemiparesis Min-Kwon Cho a, Jung-Hyun Kim a, Yijung Chung b,*, Sujin Hwang c a b c

Department of Physical Therapy, The Graduate School, Sahmyook University, Republic of Korea Department of Physical Therapy, College of Health Welfare, Sahmyook University, Republic of Korea Department of Physical Therapy, Division of Health Science, Baekseok University, Republic of Korea

A R T I C L E I N F O

A B S T R A C T

Article history: Received 15 December 2014 Received in revised form 16 April 2015 Accepted 17 April 2015

The purpose of this study was to investigate the effects of treadmill training (TT) with functional electrical stimulation (FES) applied to the gluteus medius (GM) and tibialis anterior (TA) muscles on gait and balance performance in individuals with chronic hemiparetic stroke. Thirty-six participants with chronic hemiparesis were recruited to this study and randomly distributed into three groups: TT with FES applied to the GM and TA muscles (TTFES-GM + TA group, 12 patients); TT with FES applied to the TA muscle (TTFES-TA group, 12 patients); and TT only (control group, 12 patients). All participants underwent 20 sessions of TT with a harness (30 min five times per week for 4 weeks). They also received regular physical therapy for 1 h five times per week for 4 weeks. All participants were assessed before and after training using digital muscle testing, the Medical Research Council (MRC) scale, the 6-min walk test (6MWT), and spatiotemporal parameters. After training, the TTFES-GM + TA group showed significant improvement in hip abductor strength, Berg Balance Scale score, 6MWT result, MRC scale score grade, gait velocity, and cadence compared to the TTFES-TA group and control group. These findings show that TT with FES applied to the GM and TA muscles increased lower limb muscle strength and improved balance and gait capacities. Therefore, TT with FES applied to the GM and TA could be a beneficial intervention in clinical settings for individuals with chronic hemiparetic stroke. ß 2015 Elsevier B.V. All rights reserved.

Keywords: Functional electrical stimulation Gait Stroke Treadmill training

1. Introduction A functional gait is a prerequisite for most daily activities following stroke. Recovery of gait capacity following a stroke is an important factor for good quality of life and functional independence [1]. Foot drop is a common chief complaint in stroke survivors. In addition, they have difficulty moving their body weight to the affected side and supporting the load in the midstance phase [2]. Previous studies have reported the effects of BWSTT combined with FES on gait function in individuals with hemiparetic stroke. Hesse et al. examined the use of multichannel electrical stimulation

* Corresponding author at: Department of Physical Therapy College of Health and Welfare, Sahmyook University, Cheongmyangni, P.O. Box 118, Seoul 130-650, Republic of Korea. Tel.: +82 02 3399 1637; fax: +82 02 3399 1639. E-mail address: [email protected] (Y. Chung).

applied to trunk muscles and upper and lower limb muscles with partial BWSTT for non-ambulatory hemiparetic stroke [3]. They reported that multichannel electrical stimulation with partial BWSTT improved leg muscle length, stride length, cadence, gait velocity, and gait pattern. Lindquist et al. investigated the effects of the combined use of FES applied to the common peroneal nerve and BWSTT on walking function and voluntary control of the lower limb in patients with chronic hemiparesis [4]. They reported that motor recovery and gait pattern improved with the combined use of FES and BWSTT. These previous studies used FES and BWSTT to improve the gait function in individuals following stroke. There was a single study which reported that gait speed, cadence, double support time and gait symmetry were improved when FES was applied to the gluteus medius and tibialis anterior of a walking patient while corresponding with the gait cycle [5]. Studies on training of the gluteus medius in persons with stroke, however, are insufficient in number in comparison to its

http://dx.doi.org/10.1016/j.gaitpost.2015.04.009 0966-6362/ß 2015 Elsevier B.V. All rights reserved.

Please cite this article in press as: Cho M-K, et al. Treadmill gait training combined with functional electrical stimulation on hip abductor and ankle dorsiflexor muscles for chronic hemiparesis. Gait Posture (2015), http://dx.doi.org/10.1016/j.gaitpost.2015.04.009

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importance, and studies on FES in particular have mostly been applied to tibialis anterior focusing only on improvement of gait speed. In addition, this was a cross-sectional study and therefore, there is a need to confirm whether there is a training effect to applying FES on the gluteus medius. There are studies that have studied the effects of FES applied onto the GM and TA in the experimental group and have compared with a control group [6]. However, there are currently no studies that have studied the effects of FES applied to the GM and TA in comparison with FES applied only onto the TA. Therefore, there is a need to conduct a study to confirm if there is a significant difference. This study focused on dysfunctional weight bearing in the stance phase and dysfunctional foot position in the swing phase, and aimed to improve the dynamic balance of single limb and swing limb advancement during gait. The purpose of this study was to determine the effects of treadmill training (TT) with application of FES to the gluteus medius (GM) and tibialis anterior (TA) muscles on gait and balance performance in individuals with chronic hemiparetic stroke. This study hypothesized that TT combined with FES to the GM and TA would improve the balance and gait function of participants compared to TT with FES onto the TA only. 2. Methods 2.1. Participants Thirty-six participants with chronic hemiparetic stroke were recruited for this study, and allocated randomly into three groups. Inclusion criteria for participants were as follows: (1) diagnosis of first onset of unilateral hemisphere stroke >6 months ago; (2) ability to walk at least 10 m without any assistance; (3) adequate cognitive ability to communicate and understand verbal instructions, as indicated by a mini-mental state examination score of 21; and (4) no other orthopedic or neurological problems to affect gait performance. Exclusion criteria included medical and psychological contraindications for electrical stimulation. All participants were evaluated and screened using the inclusion and exclusion criteria. Informed consent was voluntarily obtained from all patients before participation in the study, and this study was approved by the Institutional Review Board of Sahmyook University. Table 1 shows the common characteristics of participants in this study. 2.2. Equipment and data collection This study used a treadmill (Fitex5050, Fitex Inc., Seoul, Republic of Korea) and surface FES (EMG-FES 3000, Cyber Medic

Inc., Iksan, Republic of Korea) to provide TT with FES. The FES used a symmetric biphasic wave with a frequency of 40 Hz and a pulse width of 200 ms on the GM and TA muscles. GAITRite (CIR Systems Inc., Havertown, Pennsylvania, USA) was used to measure the spatiotemporal parameters. The device measures the loading of the subject’s feet with a sample rate of 80 Hz when the subject walks on it. The spatiotemporal data collected were processed using GAITRite GOLD, Version 3.2b software. For this study, the subjects were instructed to stand in front of the gait board, and then walk on it at a self-selected comfortable speed until they reached the end of the board. 6MWT (6 min walk test) is used to evaluate walking endurance. It is a method of measuring the maximum distance the patient can walk for 6 min, and exhibit high reliability for persons with stroke (ICC = .96) [7]. The Berg Balance Scale (BBS), developed by Katherine Berg, is a widely used clinical instrument used to measure static and dynamic balance. The scale consists of 14 different items, each scored from 0 (the lowest level of function) to 4 (the highest level of function), with a maximum score of 56. The BBS has been shown to have excellent inter-rater (intra-class correlation coefficient [ICC] = 0.98) and intra-rater reliability (ICC = 0.98) in individuals with hemiparetic stroke. The BBS score is considered a sound measure of balance impairment for stroke rehabilitation [8,9]. This study used a dynamometer and manual muscle testing (MMT). The dynamometer (Model 01163, Lafayette Inc., IN, USA) is a hand-held device for objectively quantifying eccentric muscle strength. The dynamometer was used to measure isometric strength in the gluteus medius and TA muscles. MMT was originally developed by Wright and Lovett, and uses an arc of motion, gravity, and resistance manually applied by the therapist to test and determine muscle grades. The scale used was the Medical Research Council (MRC) scale in this study. The MRC scale was obtained separately for five muscles (hip abductor, knee flexor, knee extensor, ankle dorsiflexor and plantarflexor) and was then added to a maximum sum score of 25 for the affected lower extremity [10,11]. 2.3. Procedures and intervention Since two persons had to be excluded for not satisfying the selection criteria, 34 participants were divided randomly into three groups, including TT with FES applied to the GM and TA muscles (TTFES-GM + TA group, 11 patients); TT with FES applied to the TA muscle (TTFES-TA group, 11 patients); and TT only (control group, 12 patients), by having each participant pick a sealed envelope before the start of the intervention. Three participants (one from each group respectively: TTFES-GM + TA group, TTFES-TA group,

Table 1 Common characteristics of the participants in this study (N = 31). Variables

TTFES-GM + TA group (n = 10)

TTFES-TA group (n = 10)

Control group (n = 11)

p

Sex (male/female) Age (yrs) Height (cm) Weight (kg) Etiology (infarction/hemorrhage) Post-stroke duration (months) Paretic side (right/left) MMSE MAS Berg balance scale Tibialis anterior strength Gluteus medius strength Medical research council

7/3 57.0  9.1* 167.4  11.0 70.8  12.7 4/6 22.5  12.6 4/6 27.1  2.0 1.1  0.7 46.7  7.5 4.4  3.7 8.9  3.2 14.0  5.2

7/3 53.3  9.2 164.0  9.4 61.9  9.3 5/5 22.5  14.1 5/5 27.1  3.0 1.1  0.7 47.8  4.3 2.7  2.4 7.5  2.4 13.2  3.7

5/6 57.8  7.9 161.6  7.9 64.1  11.0 5/6 21.6  6.7 6/5 26.3  2.8 1.0  0.9 49.3  6.0 4.0  3.7 7.3  2.4 14.1  3.7

.406 .137 .389 .882 .651 .965 .971 .710 .965 .710 .354 .341 .873

MMSE, mini-mental state examination; MAS, modified Ashworth scale; TTFES-GM + TA group, TT with FES applied on the GM and TA muscles; TTFES-TA group, TT with FES applied on the TA muscle; control group, TT only. * Mean  standard deviation.

Please cite this article in press as: Cho M-K, et al. Treadmill gait training combined with functional electrical stimulation on hip abductor and ankle dorsiflexor muscles for chronic hemiparesis. Gait Posture (2015), http://dx.doi.org/10.1016/j.gaitpost.2015.04.009

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GAIPOS-4469; No. of Pages 6 M.-K. Cho et al. / Gait & Posture xxx (2015) xxx–xxx

and control group) withdrew from this study before the post-test due to discharge. All participants being trained on a moving treadmill wore a harness and suspension device to ensure safety. This study used the same protocol as Chung et al. to decide the FES intensity for each participant before the training [6]. FES electrodes were attached over the GM and TA muscles, and a foot switch was attached to the heel of the affected lower limb. The GM muscle electrical stimulation was set to start at the initial stance phase of the affected lower limb as the foot switch touched the treadmill floor, and TA muscle electrical stimulation was set to begin at the initial swing phase as the foot switch left the treadmill floor during treadmill walking. Each muscle contraction of the GM and TA muscles was produced from a burst of patterned stimuli in which the current was ramped up and down for 0.5 and 0.5 s, respectively. Participants’ mean gait velocity was measured by analyzing the comfortable gait performance before the training. The mean speed was set as the starting speed of the treadmill, and the speed was increased by 0.1 km/h per week during the experimental period. The increased speed was reached over 20 s to allow the participants to attain stable walking on the moving treadmill [12]. Before TT, all participants had electrode pads attached over the GM and TA muscles on the affected side and a foot switch attached to the heel of the affected side. The TTFES-GM + TA group had the FES electrodes over the GM and TA muscles stimulated periodically during the stance and swing phases on a moving treadmill, while the TTFES-TA group had the FES electrode over the TA muscle only stimulated during TT. The control group underwent no FES stimulation during TT. All participants underwent TT without walking aids but with a harness. TT was carried out in a calm and well-organized therapy room for 30 min five times per week for 4 weeks. 2.4. Statistics This study measured spatiotemporal parameters, including gait velocity, cadence, stride length, double support percentage, single support percentage, temporal symmetry, and spatial symmetry. This study also used clinical measures, including the BBS score, MRC scale score, strength of the GM and TA muscles, and 6MWT result. Data analysis was performed using Predictive Analytics SoftWare (PASW) for Windows Version 18.0 (SPSS Inc., Chicago, IL, USA). For normality testing, the Shapiro–Wilk test was used. For the difference in variance among the three groups before and after the training, one-way ANOVA was used; for post hoc analysis, the

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Bonferroni test was used. The significance was set to p < 0.05 with 95% confidence limits. 3. Results After training, gait velocity and cadence were significantly different among the three groups. The gait velocity and cadence in the TTFES-GM + TA group (change values, 19.8 cm/s, 16.1 step/min, respectively) showed significantly greater improvement in comparison to that of the TTFES-TA group (change values, 10.2 cm/s, 7.4 step/min, respectively) and control group (change values, 1.0 cm/s, 1.1 step/min, respectively) after the training. The gait velocity and cadence in the TTFES-TA group showed more significant improvement than that of the control group after training. However, stride lengths in the affected and unaffected sides were not significantly different among the three groups (Table 2, Fig. 1). The percentage of single support time of the affected side was significantly different among the three groups, and that of the TTFES-GM + TA group (change values, 5.3%) showed significantly greater improvement than that of the TTFES-TA group (change values, 1.6%) and the control group (change values, 0.8%) after training (Table 2, Fig. 1). However, the percentage of single support time of the affected side was not significantly different between the TTFES-TA and control groups after training. Temporal asymmetry and spatial asymmetry showed a statistically significant difference among the three groups, with a significantly greater improvement in the TTFES-GM + TA group (change values, 0.1, 0.2, respectively) than in the TTFES-TA group (change values, 0.0, 0.0, respectively) and the control group (change values, 0.0, 0.0, respectively), but no significant difference between the TTFES-TA and control groups. 6MWT showed a significantly greater improvement in the TTFES-GM + TA group (change values, 46.85 m) than in the TTFES-TA group (change values, 12.57 m) and the control group (change values, 11.68 m) (Table 2). After training, GM and TA muscle strength tested using a dynamometer was statistically significantly different among the three groups. Greater improvement was seen in the TTFES-GM + TA group (change values, 1.4 kg, 1.7 kg, respectively) than in the TTFES-TA group (change values, 0.2 kg, 1.6 kg, respectively) and the control group (change values, 0.1 kg, 0.1 kg, respectively) (Table 3, Fig. 2). However, TA muscle strength was not significantly different between the TTFES-GM + TA group and the TTFES-TA group after training (Table 3, Fig. 2). The MRC scale score was significantly different among the three groups after training. The MRC scale score in the TTFES-GM + TA group (change value, 4.3 points) showed statistically significant improvement in comparison to that of the TTFES-TA group (change value, 2.7 points) and the control group (change value, 1.3 points), and that in the TTFES-TA group showed greater improvement than that in the control group (Table 3). The BBS score was significantly different among the three groups after training. The BBS score in the TTFES-GM + TA group (change value, 5.2 points) showed more significant improvement than that of the TTFES-TA group (change value, 2.3 points) and the control group (change value, 1.7 points) after training. However, the BBS score in the TTFES-TA group was not significantly different from that in the control group after training (Table 3, Fig. 2).

4. Discussion The main results of this study were as follows: (1) TTFESGM + TA group showed greater improvement in GM and TA muscle strength than TTFES-TA group and TT only; (2) TTFES-GM + TA

Table 2 Comparison pre-test and post-test among three groups (N = 31). Variables

Gait velocity (cm/s) Cadence (step/min) Stride length in affected side (cm) Stride length in unaffected side (cm) Single support time in affected side (%) Single support time in unaffected side (%) Double support time in affected side (%) Double support time in unaffected side (%) Temporal asymmetry Spatial asymmetry 6MWT (m)

TTFES-GM + TA group (n = 10)

TTFES-TA group (n = 10)

Control group (n = 11)

Pre-test

Post-test

Pre-test

Post-test

Pre-test

Post-test

42.5  15.9* 67.0  19.8 74.3  19.2 74.3  18.9 18.1  12.9 32.5  5.0 44.9  7.8 44.8  7.0 0.3  0.2 0.2  0.2 208.8  92.7

62.3  19.8 83.1  11.7 86.1  18.4 86.5  17.7 26.5  5.3 32.7  5.6 38.9  8.3 39.6  7.3 0.2  0.2 0.1  0.0 255.6  94.4

40.3  14.5 72.7  11.9 65.0  14.9 65.0  14.6 21.5  7.0 33.8  2.4 43.9  7.2 43.9  7.5 0.4  0.2 0.3  0.2 187.8  69.3

50.6  11.4 80.0  10.5 76.5  14.0 77.0  14.2 23.0  4.9 37.1  2.4 37.8  6.7 39.9  6.6 0.4  0.2 0.3  0.2 200.4  62.6

47.4  18.1 76.1  17.0 73.0  15.1 72.9  15.4 24.2  6.9 31.0  4.8 44.3  9.9 44.2  10.2 0.2  0.2 0.2  0.2 204.1  74.9

48.4  20.4 74.2  15.7 77.9  18.2 78.4  18.9 25.0  9.2 31.8  3.6 43.0  10.6 41.7  10.6 0.3  0.2 0.2  0.1 215.7  85.4

p

.001 .001 .398 .210 .033 .262 .053 .401 .004 .050 .030

TTFES-GM + TA group, TT with FES applied on the GM and TA muscles; TTFES-TA group, TT with FES applied on the TA muscle; control group; TT only; 6MWT, 6 min walk test. * Mean  standard deviation.

Please cite this article in press as: Cho M-K, et al. Treadmill gait training combined with functional electrical stimulation on hip abductor and ankle dorsiflexor muscles for chronic hemiparesis. Gait Posture (2015), http://dx.doi.org/10.1016/j.gaitpost.2015.04.009

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Cadence (step/min)

Gait Velocity (cm/s)

40

*† 30 20

*

10 0

*

10 0 -10

Control group

Stride Length in US (cm)

GM+AT group

20

10

0

*†

6

4

2

0 GM+TA group

TA group

Control group

0 -2 -4 -6 -8 GM+TA group

Control group

*†

Control group

GM+TA group

TA group

Control group

GM+TA group

TA group

Control group

TA group

Control group

25 20 15 10 5 0

8 6 4 2 0

0

-2

-4

-6 GM+TA group

0.4

Spatial Asymmetry

0.2

TA group

TA group

Control group

Single Support Time in US (%)

TA group

Double Support Time in US (%)

Stride Length in AS (cm) Single Support Time in AS (%)

TA group

30

GM+TA group

Double Support Time in AS (%)

20

-20

GM+TA Group

Temporary Asymmetry

*†

30

0.1 0.0 -0.1

*†

0.3 0.2 0.1 0.0

-0.2 GM+TA group

TA group

Control group

GM+TA group

TA group

Control group

Fig. 1. Change values of spatiotemporal parameters in participants. AS, affected side; US, unaffected side; GM + TA group, Treadmill training with FES applied to the GM and TA muscles; TA group, treadmill training with FES applied to the TA muscle. *Significant difference compared with control group (p < .05). ySignificant difference compared with TA group (p < .05).

group showed greater improvement in balance function than TTFES-TA group TTFES-TA group and TT only; and (3) TTFESGM + TA group showed greater improvement in gait function, especially gait velocity, cadence, single support time, temporal asymmetry, and spatial asymmetry, than TTFES-TA group and TT only.

This study applied FES to the GM and TA muscles during treadmill gait training and showed the same effects of this treatment as the previous studies by Hesse et al. and Lindquist et al., although this study used different patterns of muscle stimulation during TT. This study also did not include the body weight support of participants during TT. Greater improvements

Please cite this article in press as: Cho M-K, et al. Treadmill gait training combined with functional electrical stimulation on hip abductor and ankle dorsiflexor muscles for chronic hemiparesis. Gait Posture (2015), http://dx.doi.org/10.1016/j.gaitpost.2015.04.009

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GAIPOS-4469; No. of Pages 6 M.-K. Cho et al. / Gait & Posture xxx (2015) xxx–xxx

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Table 3 Comparison pre-test and post-test among three groups (N = 31). Variables

TTFES-GM + TA group (n = 10)

TTFES-TA group (n = 10)

Control group (n = 11)

Pre-test

Post-test

Pre-test

Post-test

Pre-test

Post-test

Berg balance scale (score) TA muscle strength (kg) GM muscle strength (kg) Medical research council scale (score)

46.7  7.5* 4.4  3.7 8.9  3.2 14.0  5.2

51.9  3.8 6.1  3.9 10.3  2.9 18.3  5.2

47.8  4.3 2.7  2.4 7.5  2.4 13.2  3.7

50.1  4.0 4.3  3.3 7.7  2.2 15.9  4.1

49.3  6.0 4.0  3.8 7.3  2.4 14.1  3.7

51.0  5.0 4.1  3.7 7.4  2.5 15.8  4.5

p

.027

Treadmill gait training combined with functional electrical stimulation on hip abductor and ankle dorsiflexor muscles for chronic hemiparesis.

The purpose of this study was to investigate the effects of treadmill training (TT) with functional electrical stimulation (FES) applied to the gluteu...
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