Abstract
[Purpose] We previously reported that a combination of stepping and functional electrical stimulation on a dynamic tilt table with robotic leg movement improved walking speed in patients with stroke. The purpose of this study was to assess the effect of a single bilateral lower limb exercise session using a dynamic tilt table with robotic leg movement without functional electrical stimulation on walking speed in patients with chronic stroke. [Participants and Methods] Ten patients with chronic stroke who were capable of walking independently (73 ± 44 months post stroke onset) were included. The participants performed passive lower extremity walking for 10 minutes in a standing position on the dynamic tilt table with robotic leg movement. The effects of the intervention on walking speed, cadence, and Modified Ashworth Scale score for the quadriceps muscle on the paralyzed side were assessed using the 10-meter walking test. [Results] The 10-minute intervention significantly increased the walking speed (baseline: 0.49 ± 0.17 m/sec, after: 0.56 ± 0.23 m/sec) and cadence (baseline: 96 ± 22 steps/min, after: 99 ± 24 steps/min); however, it had no effect on the Modified Ashworth Scale score for the paralyzed quadriceps muscle. [Conclusion] This study highlights the potential of the dynamic tilt table with robotic leg movement without functional electrical stimulation in rehabilitation therapy for patients with chronic stroke.
Keywords: Walking speed, Central pattern generator, Spasticity
INTRODUCTION
The activities of daily living and quality of life of stroke patients are related to walking speed1, 2). In order to promote independent living, it is necessary to optimize walking speed. The walking speed of patients with stroke is affected by several factors, which include the severity of paralysis3), muscle strength of the paralyzed and non-paralyzed lower limbs3,4,5), strength of the trunk muscle, muscle mass of the paralyzed lower limbs5), balance5), and spasticity3, 6).
Resistance training7), such as squats and standing up from a seated position; balance training8), such as forward walking and box stepping in tandem; and electrical stimulation of paralyzed lower limb muscles9) have been used to improve speed of walking in patients with stroke. Furthermore, exercise on a bicycle ergometer10) and single-step walking training (on the ground or on a treadmill)11) are reportedly effective for improving walking speed. In addition, previous studies have reported the potential of using virtual reality12) and robotics13) for gait training to improve walking speed.
Dynamic tilt table with robotic leg movements (DTTRLM), a rehabilitation device for early out-of-bed mobilization, was designed to facilitate passive/active stepping. DTTRLM can be used in combination with functional electrical stimulation (FES) of the lower limbs14); this combination improves orthostatic hypotension and consciousness in patients with spinal cord injury15). In patients with acute stroke, studies have reported improvement in cerebral blood flow with the use of DTTRLM with or without FES16) and in neurological symptoms with DTTRLM alone (without FES)17). In addition, DTTRLM alone (without FES) also improves orthostatic hypotension18) and consciousness19) in patients with traumatic brain injury. Therefore, DTTRLM—both in combination with or without FES—may be useful as a pre-conditioning to improve standing tolerance and neurological symptoms after stroke and spinal cord injury.
We previously reported that the use of DTTRLM in combination with FES before walking improves the walking speed of patients with stroke20), and that it is useful as a pre-conditioning before stroke rehabilitation. However, the effect of DTTRLM alone (without FES) on walking speed as a pre-conditioning in patients with chronic stroke has not been investigated.
In this study, we evaluated the effect of a single lower limb exercise session without electrical stimulation using DTTRLM on walking speed in patients with chronic stroke.
PARTICIPANTS AND METHODS
Ten patients with hemiplegia after a stroke were selected for this study. Patients for whom at least 6 months had passed since the stroke onset and who had the ability to walk independently with or without the use of a brace were included in the study. The exclusion criteria for the patients were 1) unstable cardiovascular conditions, 2) severe trunk and lower limb pain, 3) lower limb fracture, and 4) cognitive impairment. The patients’ medical records were carefully examined, and strokes were confirmed by means of diagnostic imaging such as computed tomography or magnetic resonance imaging. The functional status of each patient was assessed using the Modified Rankin Scale21).
The protocol for this study was approved by the ethics committee of Nachikatsuura Balneologic Town Hospital (#R2-3), and the study was conducted in accordance with the principles of the Declaration of Helsinki. After fully explaining the purpose and risks of the study, informed consent was obtained from each participant. In addition, informed consent was obtained from all participants regarding the publication of the study results.
Prior to the intervention, the participants rested for approximately 5 min in a chair (rest period). After the rest period, the base walking speed and cadence in the 10-m walking test (10WT) and the Modified Ashworth Scale for the paralyzed quadriceps muscle were measured. Subsequently, the participants underwent a 10-min training session on the DTTRLM (Erigo Pro, Hocoma AG, Volketswil, Switzerland) (Fig. 1). Immediately after completing the 10-min intervention, another measurement of the walking speed, muscle tone (post-intervention values), and Modified Ashworth Scale of the same muscles was obtained.
Fig. 1.
Photograph of the dynamic tilt table for robotic leg movement (DTTRLM) used in this study. The device facilitates vertical loading of the paralyzed patient and achieves rhythmic and cyclical leg movements.
The DTTRLM can be adjusted to incline from 0 to 80° to assist with walking training, and the periodic leg movement can be set to a pace of 8 to 80 steps/min. After fixing on the DTTRLM, the participants changed their posture from 0 to 80° and walked for 10 min at a pace of 16 steps/min. During the training period, each participant was instructed to walk with effort in accordance with the assistance of the DTTRLM.
Each patient was asked to walk as fast as possible along a 14-m straight course. The start and finish times were set at the 2-m and 12-m points, excluding the acceleration phase of the first 1 m and deceleration phase of the last 2 m of the test. Walking speed was expressed as the time taken to walk 10 m. The number of steps during the 10WT was counted, and the cadence was calculated based on the walking time and number of steps. The average of the results of two consecutive tests was calculated22).
The Modified Ashworth Scale was used to assess the severity of spasticity in the quadriceps muscle on the paralyzed side. The Modified Ashworth Scale is a tool that evaluates muscle tone on a scale of 0 to 4 (0, no increase in muscle tone; 4, stiffness of joint movement due to muscle tone)23).
The measured values are expressed as the mean ± standard deviation. The maximum walking speed, number of steps in the 10WT, and Modified Ashworth Scale score for the paralyzed quadriceps muscle at baseline and after the intervention were analyzed using the Wilcoxon signed-rank test for paired data.
The significance level was set at p<0.05.
RESULTS
Table 1 shows the characteristics of the 10 patients. The mean age of the patients was 69 ± 12 years, and the mean time from stroke onset to study participation was 72.7 ± 44.5 months (range: 7 to 126 months). The Modified Ashworth Scale score for the quadriceps muscle at baseline was 1, 1+, and 2 for six, two, and two patients, respectively. Four participants used articulated metal ankle foot orthosis (AFO), one used an AFO with oil damper, and two used a solid polypropylene AFO. All participants completed the entire 10-min DTTRLM training program. No adverse events were observed during or after the intervention.
Table 1. Demographic characteristics of the 10 study participants.
| Case | Age (years) |
Sex | Weight (kg) |
BMI (kg/m2) |
Lesion type (H/I) |
Lesion site | Paretic side (L/R) |
Time since stroke (months) |
MAS | NIHSS | mRS | Walking with canes |
Wearing ankle-foot orthosis |
| 1 | 70 | F | 50.0 | 25.5 | H | Thalamus | R | 126 | 1 | 7 | 2 | Yes | Yes |
| 2 | 82 | F | 50.0 | 21.4 | I | Corona radiata | R | 55 | 2 | 4 | 2 | Yes | No |
| 3 | 63 | M | 70.5 | 23.6 | H | Putamen | R | 76 | 2 | 10 | 3 | Yes | Yes |
| 4 | 61 | F | 62.0 | 26.1 | H | Thalamus | R | 116 | 1 | 6 | 3 | Yes | Yes |
| 5 | 76 | F | 48.0 | 22.2 | H | Thalamus | L | 124 | 1 | 7 | 3 | Yes | Yes |
| 6 | 65 | M | 59.1 | 21.2 | I | Putamen | R | 7 | 1 | 6 | 3 | Yes | Yes |
| 7 | 71 | M | 46.6 | 16.7 | I | Parieto‐temporal lobe | L | 103 | 1+ | 6 | 3 | Yes | No |
| 8 | 84 | F | 52.4 | 21.8 | H | Thalamus | R | 74 | 1 | 7 | 3 | Yes | No |
| 9 | 75 | F | 51.0 | 24.3 | I | Parietal lobe | R | 25 | 1+ | 6 | 3 | Yes | Yes |
| 10 | 41 | F | 50.0 | 21.9 | I | Pons, Cerebral peduncle | L | 21 | 1 | 6 | 2 | Yes | Yes |
| mean / ratio | 69 ± 12 | F:M | 54.0 ± 7.5 | 22.5 ± 2.7 | H:I | L:R | 72.7 ± 44.5 | 1.3 ± 0.4 | 6.5 ± 1.5 | 2.7 ± 0.5 | Yes:No | Yes:No | |
| 7:3 | 5:5 | 3:7 | 10:0 | 7:3 | |||||||||
F: female; M: male; BMI: body mass index; H: hemorrhage; I: infarction; R: right; L: left; MAS: Modified Ashworth Scale for the paralyzed quadriceps muscle; NIHSS: National Institutes of Health Stroke Scale; mRS: modified Rankin Scale.
The maximum walking speed significantly increased from 0.49 ± 0.17 m/s at baseline to 0.56 ± 0.23 m/s after the intervention (p<0.05). Furthermore, the number of steps significantly increased from 96 ± 22 steps/min at baseline to 99 ± 24 steps/min after the intervention (p<0.05). There was no change in the Modified Ashworth Scale score for the paralyzed quadriceps (Table 2). Furthermore, no differences were observed in walking speed, cadence, or Modified Ashworth Scale scores between the participants using AFO and those not using orthoses after the intervention.
Table 2. Maximum walking speed, Cadence during the 10-m walking test and the Modified Ashworth Scale score before and after DTTRLM training.
| Baseline | After intervention | p-value | |
| Maximum walking speed (m/s) | 0.49 ± 0.17 | 0.56 ± 0.23 | 0.009 |
| Cadence (steps/min) | 96 ± 22 | 99 ± 24 | 0.013 |
| MAS | 1.3 ± 0.4 | 1.3 ± 0.4 | 0.317 |
Data are expressed as the mean ± standard deviation; MAS: Modified Ashworth Scale for the paralyzed quadriceps muscle.
DISCUSSION
Our study revealed that 10-min DTTRLM training for patients with chronic stroke increased walking speed and cadence; however, there was no change in the Modified Ashworth Scale score for the paralyzed quadriceps. The cadence increase after DTTRLM training may have improved the gait speed.
The basic pattern and rhythm of walking can be produced by central pattern generators (CPGs) alone. All forms of bipedal locomotion in humans, from extremely slow walking to fast running, are controlled by a flexible combination of four to five CPGs24). CPGs are a type of spinal interneuron (SINs). SINs have been considered to integrate information from higher central (supraspinal input neurons) and peripheral input neurons, resulting in orchestrated output at motor neurons; thus, facilitating coordinated muscle activity and motor control at all levels from simple reflex responses to complex voluntary movements25). CPGs are present in the brainstem and spinal cord, and spinal CPGs control gait, and affect three factors: 1) rhythm and cycle, 2) intra-limb agonist-antagonist coordination, and 3) inter-limb coordination26).
Stimuli that activate spinal CPGs include 1) hip joint loading27, 28), 2) hip movement28, 29), 3) stretch stimulation of the hip flexor stretch receptors30), 4) stimulation of ankle extensor afferents31), and 5) cutaneous impulses32). Interestingly, when patients with stroke use a walking stick with their unaffected hand, the load on the affected hip joint is reduced33). Therefore, routine cane use may adversely affect CPG output. All the participants in this study used a cane while walking, suggesting that their CPG may have been adversely affected before the study.
The DTTRLM training was performed with an inclination of 80°, almost vertical, increasing hip loading and cutaneous impulses. As flexion and extension exercises of the lower limb were performed with the trunk secured to the tilt table with a belt and the distal thigh attachment secured posteriorly, greater hip flexion and extension exercises than those during daily walking may have been possible. Thus, the increased walking speed after DTTRLM training observed in this study was probably related to stimuli arising from the hip area activating the CPGs, rather than stimulation arising from the ankle region.
In our previous study, we reported that stepping with DTTRLM in combination with FES improved walking speed and the Modified Ashworth Scale score for the paralyzed quadriceps muscle20). However, in the current study, while walking speed improved with DTTRLM alone (without FES), no effect on the Modified Ashworth Scale scores for the same muscles was observed. These results contradict the results of a previous study incorporating 41 chronic stroke patients34). This previous study reported that the Modified Ashworth Scale score for the upper limb on the paralyzed side was significantly improved by 10 min of ergometer exercise on the non-paralyzed side34). Another study reported that the Modified Ashworth Scale scores for the hamstrings of eight patients with spastic cerebral palsy were significantly improved by 10 min of cycle ergometer exercise35). These different results may be because the Modified Ashworth Scale is an ordinal scale, with wide intervals between each level. Therefore, even if spasticity decreased slightly due to DTTRLM training in this study, it may not have been detected using the Modified Ashworth Scale. Apart from the Modified Ashworth Scale, the assessment of muscle tone in paralyzed muscles includes the Modified Tardieu Scale, Quality of Muscle Reaction, and clonus duration. Although these were not assessed in this study, these scales might have detected changes in the paralyzed muscles. In addition, the Modified Ashworth Scale was measured only for the paralyzed quadriceps muscle, and although DTTRLM training did not affect the Modified Ashworth Scale, it is possible that the Modified Ashworth Scale for other paralyzed muscles, which were not measured in this study, changed.
This study has some limitations including 1) the small sample size; 2) lack of comparison with the effect of DTTRLM combined with FES; 3) lack of a control group with normal participants or patients with other neurological diseases; 4) inclusion of participants with mild spasticity; and 5) measurements of only the walking speed, cadence, and Modified Ashworth Scale of the paralyzed quadriceps muscle. To clarify the effects of the same protocol on the Modified Ashworth Scale for other paralyzed muscles and the immediate and long-term effects of DTTRLM in patients with stroke, an intervention study with additional muscles measured for spasticity is needed.
In conclusion, a single 10-min session of bilateral lower limb exercise using DTTRLM without electrical stimulation improved gait speed and cadence in patients with chronic stroke. Therefore, DTTRLM training is considered to be a promising and effective method of pre-conditioning for patients with chronic stroke.
Conflict of interest
The authors declare no conflict of interest.
Acknowledgments
The authors thank the medical staff at the Nachikatsuura Balneologic Town Hospital for their assistance with data collection, especially Messrs. Shogo Okuji, Taiki Yanase, Keigo Shimizu, and Yukio Wada. We also thank Dr. Faiq G. Issa (Word-Medex Pty Ltd., Sydney, Australia; www.word-medex.com.au) for English language editing.
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