Received 5 April 2016; Revised 23 September 2016; Accepted 23 September 2016

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1 RESEARCH ARTICLE Effects of Weight-shifting Exercise Combined with Transcutaneous Electrical Nerve Stimulation on Muscle Activity and Trunk Control in Patients with Stroke Kyoung-Sim Jung 1, Jin-Hwa Jung 2, Tae-Sung In 3 *, & Hwi-Young Cho 4 *, 1 Institute for Life Sciences, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea 2 Department of Occupational Therapy, Semyung University, Jecheon, Korea 3 Department of Physical Therapy, Gimcheon University, Gimcheon, Korea 4 Department of Physical Therapy, College of Health Science, Gachon University, Incheon, Korea Abstract This study investigated the effects of weight-shifting exercise (WSE) combined with transcutaneous electrical nerve stimulation (TENS), applied to the erector spinae and external oblique (EO) muscles, on muscle activity and trunk control in patients with hemiparetic stroke. Sixty patients with stroke were recruited to this study and randomly distributed into three treatment groups: (1) WSE + TENS, (2) WSE + placebo TENS, and (3) control. All participants underwent 30 sessions of training (30 minutes five times per week for 6 weeks) and received 1 hour of conventional physical therapy five times per week for 6 weeks. Muscle activity, maximum reaching distance and trunk impairment scale scores were assessed in all patients before and after the training. After training, the WSE + TENS group showed significant increase in the EO activity, maximum reaching distance and trunk impairment scale scores compared with the WSE + placebo TENS and control groups. These findings suggest that WSE with TENS applied to the erector spinae and EO muscles increased the trunk muscle activity and improved trunk control. Therefore, WSE with TENS could be a beneficial intervention in clinical settings for individuals with hemiparetic stroke. Copyright 2016 John Wiley & Sons, Ltd. Received 5 April 2016; Revised 23 September 2016; Accepted 23 September 2016 Keywords stroke; transcutaneous electrical nerve stimulation; trunk *Correspondence Tae-Sung In, Department of Physical Therapy, Gimcheon University, 214 Daehak-ro, Gimcheon , Korea. in8386@naver.com Hwi-young Cho, Department of Physical Therapy, College of Health Science, Gachon University, 191 Hambangmoe-ro, Yeonsu-gu, Incheon , Korea. hwiyoung@gachon.ac.kr These two authors contributed equally to this study as co-first author. These authors contributed equally to this work as corresponding authors. Published online 17 October 2016 in Wiley Online Library (wileyonlinelibrary.com) DOI: /oti.1446 Introduction Trunk muscles play important roles in maintaining balance by stabilizing the pelvis and spinal column (Kibler et al., 2006; Behm et al., 2010). Unlike the limb muscles, the trunk muscles can be multidirectional damaged (Dickstein et al., 1999; Fujiwara et al., 2001; Tsuji et al., 2003), and patients with stroke may 436 Occup. Ther. Int. 23 (2016) John Wiley & Sons, Ltd.

2 experience trunk flexor, extensor and bilateral rotator weakness (Bohannon, 1992). Trunk muscle weakness and loss of proprioception not only decrease patient postural control ability, including weight shifting (Badke and Duncan, 1983; Geiger et al., 2001; Tessem et al., 2007), but also increase the risk of falling towards the affected side (Eng et al., 2008). Training has been used to improve trunk control. Previous studies reported that reaching task training and trunk control training effectively improved trunk control (Dean and Shepherd, 1997; Verheyden et al., 2009). Moreover, Karthikbabu et al. (2011) reported exercising on unstable surfaces to be more effective at improving trunk control and balance, as it improved the trunk muscle activity and weight-shift ability by inducing postural sway; however, the study could not confirm whether the improvements were due to increased muscle activity. Supplementing sensory input with transcutaneous electrical nerve stimulation (TENS) causes long-term neuroplastic changes and reinforces motor recovery (Tyson et al., 2013). A study reported that the group receiving TENS combined with task-related training had more statistically significant improvements in the muscle strength and gait speed than the group receiving placebo stimulation (Ng and Hui-Chan, 2007). Chan et al. (2015) assessed the effects of trunk exercise by applying TENS to the latissimus dorsi (LD) and external oblique (EO); this study reported that the group that received TENS showed significantly greater improvement in its mean TIS score than the placebo group. However, the isometric peak trunk flexion torque and extension torque did not differ significantly between the groups, and the authors suggested future studies to investigate the efficacy of targeting other trunk muscles such as the erector spinae (ES) and applying other simulation settings with stroke patients. Most studies on the effect of TENS on patients with stroke have applied TENS to either the lower or upper limb muscles, and studies on the effects of combining Figure 1. Flow diagram of the study participants Occup. Ther. Int. 23 (2016) John Wiley & Sons, Ltd. 437

3 exercise with TENS for the trunk muscles are lacking. This study analysed the effects of weight-shifting exercise (WSE) on an unstable surface combined with TENS, applied to the ES and EO muscles, on trunk control and trunk muscle activity. Materials and methods Subjects The study was approved by the Institutional Review Board of Gachon University. After being informed about the study, all subjects agreed to participate and signed a consent form. Sixty-three patients with hemiparetic stroke were recruited for this study. Two patients were excluded for not satisfying the selection criteria. The remaining 61 patients were divided randomly into WSE + TENS (20 patients), WSE + placebo TENS (20 patients) and control (21 patients) group from S Rehabilitation Center from July to November One participant in the control group withdrew from the study before the posttest because of a change of address (Figure 1). The patient inclusion criteria were diagnosed with first onset of unilateral hemisphere stroke, able to sit independently for 30 seconds on a stable surface, medically stable, no unilateral neglect as indicated by star cancellation test scores over 47, no severe sensory deficits in the pinprick test, no musculoskeletal problems such as low back pain or arthritis affecting motor performance and able to understand and follow simple verbal instructions. Table I lists the general characteristics of subjects in the three groups. Experimental procedure and intervention This study was observer blinded, with a pilot randomized controlled trial design. The patients included in the study were randomly assigned to the three groups by selection from a sealed envelope for allocation. Subjects in the WSE + TENS and WSE + placebo TENS groups participated in weight-shift training in a seated position for 30 minutes, five times a week for 6 weeks, while those in the control group received stretching exercise on supine, prone and side-lying position on limbs and trunk and stationary bicycle exercise for the same amount of time. All subjects in this study received a conventional exercise programme provided by the rehabilitation hospital for 1 hour, five times a week for 6 weeks. For conventional exercise that was performed using the neurodevelopmental treatment and motor relearning based in the Bobath technique, such as tone facilitation and a range of movement exercise. During the WSE, the subjects were instructed to sit with their arms folded and to shift their weight to the right and the left as far as possible. A piece of graph paper was placed behind the participant s back to measure range of weight shifting. The maximum range of weight shifting was measured on a stable surface before training, and the bar was installed at the location that was 2 cm closer to the patient from the Table I. Common and clinical characteristics of the subjects (n = 60) WSE + TENS group (n = 20) WSE + placebo TENS group (n = 20) Control group (n = 20) p Sex (number) Male Female Age (years) 55.3 ± ± ± Height (cm) ± ± ± Weight (kg) 65.9 ± ± ± MMSE 26.2 ± ± ± Duration (months) 5.6 ± ± ± Paretic side Right Left Lesion type Haemorrhage Ischemia Mean ± SD. WSE = weight-shifting exercise; TENS = transcutaneous electrical nerve stimulation; MMSE = mini-mental state examination. 438 Occup. Ther. Int. 23 (2016) John Wiley & Sons, Ltd.

4 maximum range of weight shifting. The markers were attached to the bilateral acromion. The subjects were instructed to shift their weight and hold their position for 10 seconds when their marker reached the target point and then return to the starting position (Figure 2). The range of movement was newly set every week for each patient based on the maximum range of weight shifting. The WSE session consisted of four conditions: (1) to sit on an exercise mat with legs extended and have a balance pad under their buttocks; (2) to sit with legs extended, have a balance pad under the buttocks and a balance cushion under both heels; (3) to sit on the edge of a exercise mat, have a balance pad under the buttocks and a balance cushion under the feet; (4) to sit on the edge of a exercise mat, have a balance pad under the buttocks and a balance cushion under the feet. Each subject performed three sets of 10 trials with a rest period of 1 minute between each set. The WSE were initiated with moderate assistance and progressed to a state of supervision. The subject was provided assistance in the upper trunk portion so that the person could keep balance. Transcutaneous electrical nerve stimulation electrodes were attached over the ES and EO muscles on the affected side. In the WSE + TENS group, electrical stimulation (two to three times the sensory threshold, 100 Hz; 200 μs) was applied to the muscle belly of the ES and EO using a TENS machine (TENS-7000, Koalaty Products Inc., USA). Electrodes were attached at the same location, but electrical stimulation was not applied in the WSE + placebo TENS group. Figure 2. The weight-shifting exercise apparatus. Occup. Ther. Int. 23 (2016) John Wiley & Sons, Ltd. 439

5 Outcome measurements An assessor blinded to the treatment allocation assessed all subjects at baseline and after 6 weeks of treatment. Muscle activity was measured with a surface electromyogram (EMG) (Telemyo 2400 G2, Telemetry EMG System; Noraxon, Scottsdale, AZ, USA, 2007). Before the electrodes were attached, the skin over the two muscles was swabbed with alcohol to minimize skin resistance. Surface electrodes were placed over the ES and EO muscles. The peak EO and ES activities were measured during the weight shifting. The sampling rate was set at 1,500 Hz, and the bandwidth of EMG recordings was set between 20 and 450 Hz. After full-wave rectification, the EMG signals were processed with a root mean square smoothing algorithm (window of 100 ms). The surface EMG amplitude was normalized as a percentage of maximum voluntary isometric contraction (%MVIC). Each MVIC manoeuvre was performed for 5 seconds and was repeated three times. The maximum reaching distance was defined as the distance the acromion moved when the subject seated on a stable surface reached to the affected side. The values of three trials were averaged for analysis. A trunk impairment scale (TIS) was used to evaluate the quality of the upper and lower trunk mobility. The test consists of three subscales: static sitting balance, dynamic sitting balance and coordination. Each subscale consists of 3 to 10 items. TIS scores range from a minimum of 0 to a maximum of 23, with higher scores indicating better trunk performance. TIS is an excellent and reliable tool, with intraclass correlation coefficients for test retest and inter-rater reliability of r = 0.96 and 0.99, respectively (Verheyden et al., 2004). Statistical analysis This study measured activity of the ES and EO muscles, maximum reach distance and trunk control. Data analysis was performed using PASW STATISTICS for Windows, version 18.0 (SPSS Inc., Chicago, IL, USA). The Shapiro Wilk test was used to assess the normality of the data. Differences in variance among the three groups before and after training were analysed by one-way analysis of variance, and the Bonferroni test was used for post hoc analysis. The significance was set at p < 0.05 with 95% confidence limits. Results After training, the EO muscle activity during weight shifting differed significantly among the three groups. Higher improvement was observed in the WSE + TENS group (change values, ± 4.61%MVIC) than in the WSE + placebo TENS (change values, 6.38 ± 2.94%MVIC) and control groups (change values, 2.66 ± 1.76%MVIC) (p <0.05). However, the ES muscle strength during weight shifting was not significantly different between the WSE + TENS and WSE + placebo TENS groups (Table II). Table II. Comparison pre-test and post-test among three groups (n = 60) WSE + TENS group (n = 20) WSE + placebo TENS group (n = 20) Control group (n = 20) p Variables Pre-test Post-test Pre-test Post-test Pre-test Post-test Muscle activity ES ± ± 8.34*** ± ± 6.15* ± ± 4.22* EO ± ± 5.52****** ± ± 5.24*** ± ± 5.38**** Maximum reaching distance 7.14 ± ± 2.28****** 7.01 ± ± 3.01*** 7.74 ± ± 2.77**** Trunk impairment scale Static sitting balance 5.95 ± ± 0.60* 5.85 ± ± 0.59* 6.00 ± ± 0.41* Dynamic sitting balance 4.28 ± ± 1.92*** 4.21 ± ± 1.29*** 4.30 ± ± 1.53**** Coordination 2.00 ± ± 0.97****** 2.12 ± ± 0.89*** 2.22 ± ± 0.79**** Total score ± ± 2.74****** ± ± 1.99*** ± ± 2.17**** Mean ± standard deviation. *Significance (p < 0.05) compared with baseline. **Significance (p < 0.05) compared with the control group. ***Significance (p < 0.05) compared with the placebo TENS + TRE group. WSE = weight-shifting exercise; EMG = electromyography; ES = erector spinae; EO = external oblique; TIS = trunk impairment scale; TENS = transcutaneous electrical nerve stimulation. 440 Occup. Ther. Int. 23 (2016) John Wiley & Sons, Ltd.

6 After training, the maximum reaching distance and TIS scores differed significantly among the three groups. The maximum reaching distance and TIS in the WSE + TENS group (change values, 4.73 ± 1.86 cm, score 5.42 ± 2.63, respectively) showed significantly higher improvement than in the WSE + plaacebo TENS (change values, 3.42 ± 1.89 cm, score 3.85 ± 1.23, respectively) and control groups (change values, 2.13 ± 1.06 cm, score 1.60 ± 1.19, respectively). Compared with the control group, both WSE groups (with TENS or placebo TENS) showed significantly higher improvements in the dynamic sitting balance. However, it did not differ significantly between the WSE + TENS and WSE + placebo TENS groups. The coordination in the WSE + TENS group (change values, 2.10 ± 1.37 score) showed more significant improvement than in the WSE + placebo TENS (change values, 1.30 ± 0.66 score) and control groups (change values, 0.55 ± 0.69 score). However, the static sitting balance was not significantly different among the three groups (Table II). Discussion After training, the experimental group showed significant improvements in the trunk muscle activity compared with the control group and the application of TENS during WSE was more effective than exercise alone in activating the EO muscle. TENS increases the excitability of the sensorimotor cortex through cutaneous stimulation of the muscles (Khaslavskaia et al., 2002), and the cortical representation area is continuously modified through sensory input and motor experiences (Nudo and Milliken, 1996; Liepert et al., 2000). A study that applied TENS to the peroneal nerves reported increased muscle strength through disinhibition of descending voluntary commands to the motor neurons of the paretic muscles (Ng and Hui-Chan, 2007). Similarly, a study by Chan et al. (2015) on trunk exercise that applied TENS to the LD and EO in patients with chronic stroke found significantly improved trunk control in the TENS group. However, no significant differences were observed in the trunk peak torque between TENS and placebo stimulation groups; these results were attributed to the fact that the subject did not need to exert the maximum strength performing the task because the trunk exercise was focused on the trunk control and coordination. Unlike the LD or EO, the ES is the axial trunk muscle that receives the bilateral input from the high brain centre and it is responsible for trunk extension and trunk stabilization bilaterally without a comparable unilateral preponderance (Ferbert et al., 1992; Carr et al., 1994; Dickstein et al., 2004). In this study, TENS was applied to the ES and EO to conduct WSEs effectively in a more normal alignment. These results may indicate that there was a limit to the facilitation of ES and EO activity because the WSE was performed only in the frontal plane and conducted training on unstable surfaces in order to increase the combined effect of TENS and exercise. Moreover, we aimed to more accurately and sensitively measure improvements by measuring the activity of trunk muscles during weight shifts towards the affected side. In the experimental group, activity of EO during the weight shifts improved more significantly than in the placebo stimulation or control groups. Unstable surfaces increase the trunk muscle activity by inducing a postural sway and repeatedly stimulate proprioceptive and somatosensory receptors (Karthikbabu et al., 2011); while Weaver et al. (2012) suggested significant benefit in decreasing rectus abdominis and EO muscle activity onsets and increasing amplitude when seated on an unstable surface. While participants were balancing on unstable surface, TENS might be improved symmetry of the trunk movement, thereby enhancing the trunk muscle activity on the paretic side in the WSE + TENS group (Chan et al., 2015). However, we did not observe any significant effect on ES activity during weight shifting; these results may indicate that there was a limit to the facilitation of ES activity because the WSE was performed only in the frontal plane. We also assessed the effects of TENS on trunk control and observed significant improvements because of TENS in dynamic sitting balance and coordination, which was attributed to improved trunk rotator, EO activity and weight-shift ability (Karthikbabu et al., 2011). Dynamic sitting balance is evaluated by measuring lateral flexion of the upper and lower trunk (Verheyden et al., 2004), and stability is a prerequisite for efficient mobility. Coordination in trunk control requires counter rotation of the upper and lower trunk, and weight shifts towards the affected side are important for counter rotation (Ryerson and Levit, 1997; Davis, 2003). In this study, we conducted weight-shift exercises on both sides of the body on unstable surfaces and gradually increased the Occup. Ther. Int. 23 (2016) John Wiley & Sons, Ltd. 441

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