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Safety and immediate effects of Hybrid Assistive Limb in children with cerebral palsy: A pilot study
Brain & Development xxx (2019) xxx–xxx www.elsevier.com/locate/braindev
Original article
Safety and immediate effects of Hybrid Assistive Limb in children with cerebral palsy: A pilot study Shogo Nakagawa a,b, Hirotaka Mutsuzaki b,c, Yuki Mataki b, Yusuke Endo d Mayumi Matsuda e, Kenichi Yoskikawa e, Hiroshi Kamada a,⇑, Nobuaki Iwasaki c,f Masashi Yamazaki a b
a Department of Orthopaedic Surgery, Faculty of Medicine, University of Tsukuba, Japan Department of Orthopaedic Surgery, Ibaraki Prefectural University of Health Sciences Hospital, Japan c Center for Medical Sciences, Ibaraki Prefectural University of Health Sciences, Japan d Department of Physical Therapy, Faculty of Health Science, Health Science University, Japan e Department of Physical Therapy, Ibaraki Prefectural University of Health Sciences Hospital, Japan f Department of Pediatrics, Ibaraki Prefectural University of Health Sciences, Japan
Received 9 August 2019; received in revised form 3 October 2019; accepted 4 October 2019
Abstract Purpose: Early intervention is effective for developing motor ability and preventing contractures and deformities in patients with cerebral palsy (CP). Gait training using the newly developed Hybrid Assistive Limb (HAL) shows promise as an intervention to prevent deterioration in walking ability and deformities in pediatric CP patients. The purpose of this pilot study was to examine the safety and immediate effects on walking ability after gait training using the HAL in pediatric CP patients. Methods: Nineteen patients (six females, 13 males; mean age 8.5 years; mean height 120.5 cm; mean weight 23.2 kg) were enrolled. The Gross Motor Functional Classification Scale level was I in two patients, II in two, III in eight, and IV in seven. The HAL was used for a single session of gait training. The primary outcome was safety of the HAL for use in pediatric CP patients. The secondary outcome was the immediate effect after gait training with HAL, evaluated by passive range of motion (ROM) and gait parameters, including gait speed (m/s), step length (cm), and cadence (step/min). Results: All 19 patients were able to carry out the gait training without any severe adverse events. Significant improvements were observed for mean internal/external rotation and abduction angles of the hip joint, and ankle dorsiflexion angles (n = 19). Significant improvements were observed for mean gait speed and step length based on expansion of the hip flexion-extension range (n = 11). Conclusion: Gait training using the HAL is safe and can produce immediate improvements in ROM and walking ability in pediatric patients with CP. Ó 2019 Published by Elsevier B.V. on behalf of The Japanese Society of Child Neurology.
Keywords: Cerebral palsy; Hybrid Assistive Limb; Pediatrics; Safety; Immediate effect
1. Introduction ⇑ Corresponding author at: Department of Orthopaedic Surgery, Faculty of Medicine, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki 305-8575, Japan. E-mail address: [email protected] (H. Kamada).
Cerebral palsy (CP) is defined as a group of permanent progressive disorders of the development of movement and posture which cause activity limitation
https://doi.org/10.1016/j.braindev.2019.10.003 0387-7604/Ó 2019 Published by Elsevier B.V. on behalf of The Japanese Society of Child Neurology.
Please cite this article in press as: Nakagawa S et al. Safety and immediate effects of Hybrid Assistive Limb in children with cerebral palsy: A pilot study. Brain Dev (2019), https://doi.org/10.1016/j.braindev.2019.10.003
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attributed to non-progressive disturbances that occur in the developing fetal or infant brain [1] (1). The brain lesion is a static encephalopathy, but the musculoskeletal pathology is progressive [2]. Although a newborn child with CP usually has no bone deformities or musculoskeletal abnormalities at birth [3], it is generally assumed that around the age of 6 to 12 years, development of gross motor function has reached a plateau and gait parameters show deterioration as joint contractures and bony deformities increase [4]. Earlier intervention is reportedly effective for both motor ability development and prevention of contractures and deformities. In our previous study, we reported that among 19 patients with CP with an average age of 15.0 years, gait training using the Hybrid Assistive Limb (HAL, Cyberdyne, Tsukuba, Japan) was safe and provided immediate positive effects on walking ability [5]. However, we could not include younger children in this study as the HAL was not suitable for younger children with shorter stature at that time. The HAL receives electric signals sent from the brain to the muscles, amplifies them using a computer, and analyzes them in conjunction with a weighting sensor at the sole of the wearer’s foot in order to support optimal joint motion for walking [6]. If gait training can be performed using the HAL before the plateau of motor growth is reached and therefore, prevent deterioration in walking ability, this may also lead to prevention of deformities. Recently, as a case report, we reported that a new smaller and lighter-weight HAL has been developed for pediatric patients and could be safe and feasible for gait training in pediatric patients with CP [7]. We believe that further improvements in walking ability could result from the use of this HAL in younger pediatric patients with a shorter stature. The purpose of this pilot study was to examine the safety and immediate effect on walking ability after gait training using the newly developed HAL in pediatric patients with any type of CP. 2. Methods 2.1. Patients Approval for this study was granted by the Human Ethics Review Committee of Ibaraki Prefectural University of Health Sciences (approval numbers: 682, e83, and e119). We recruited outpatient children with CP aged 14 years or younger from October 2018 to June 2019. The inclusion criteria were (i) diagnosis of CP according to the Gross Motor Function Classification System (GMFCS) [8] levels of I to IV, (ii) usual participation in traditional rehabilitation, including gait training, and (iii) easy recognition of the signals of pain, fear, and discomfort with reliance on the parents. The
patients were excluded if there was (i) difficulty wearing the HAL due to size mismatch, (ii) lack of patient cooperation, or (iii) presence of a severe condition of the heart or lung. Nineteen patients met our inclusion criteria. The intervention method was explained to the patient and their parents using a movie, and written informed consent was obtained from the patient’s parents before intervention was performed. We obtained the following clinical information from parents and our institutional medical records: patient age, sex, cause and type of CP, GMFCS level, presence or absence of speech problems, and the use of walking aids and orthoses. Regarding speech problems, if the patient had never or sometimes exhibited speech problems, we described this as ‘‘no”; however, if speech problems were often exhibited, we described this as ‘‘yes”. There were six female patients and 13 male patients with a mean age of 8.5 years (range, 3 to 14). The mean height was 120.5 cm and the mean weight was 23.2 kg. Of all children with CP, 15 were diagnosed with spastic diplegia, one with spastic hemiplegia, two with ataxia, and one with athetosis. According to the GMFCS, two patients were classified as level I, two as level II, seven as level III, and seven as level IV. Seven patients had speech problems (Table 1). 2.2. HAL training Before the gait training, we measured each patient’s range of motion of the hip, knee, and ankle joint. HAL gait training was performed during standard physical therapy sessions as part of an inpatient stay at our hospital. We used the newly developed HAL (2SHAL; HAL-ML06, lower limb type, 2S size). The weight
Table 1 Clinical characteristics. Mean age (range) (years) Sex (n)
8.5 (3–14) female male
6 13 120.5 (16.6) 23.2 (7.4)
Spastic Diplegia Spastic Hemiplegia Ataxia Athetosis
15 1 2 1
I II III IV
2 2 8 7
No Yes
12 7
Mean height (SD) (cm) Mean weight (SD) (kg) Type of CP (n)
GMFCS level (n)
Speech problems
SD, standard deviation; CP, cerebral palsy; GMFCS, Gross Motor Function Classification System.
Please cite this article in press as: Nakagawa S et al. Safety and immediate effects of Hybrid Assistive Limb in children with cerebral palsy: A pilot study. Brain Dev (2019), https://doi.org/10.1016/j.braindev.2019.10.003
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of the 2S-HAL is about 5 kg, which is less than half that of the previous model (S-HAL; HAL-ML05, lower limb type, S size), and its target user is children with a height of 100–150 cm and a body weight of 15–40 kg. The device was attached to the patient’s thighs and lower legs using bands and cushioning material if needed. Ankle-foot orthoses were used in the sensor shoes of the HAL if the patient had drop feet. After positioning the device, flexion/extension balance and assist torque at the hip and knee joints were optimized. To avoid falling, a walking device was used according to patient preference (either an All-in-One Walking Trainer [Ropox A/S, Naestved, Denmark] or a posture control walker). Of the two therapists who provided assistance, the person in front led the patient in the correct direction, and the person at the back assisted the patient to maintain a good gait pattern by providing feedback. Gait training sessions using the HAL lasted for about 20 min, including a rest time. Patients controlled their own gait speed in this intervention. We adjusted the flexion/extension balance and assist torque during gait training so that the cybernic voluntary control mode (CVC) and walk modes, which help the patient’s spontaneous movements, were used as much as possible [9]. 2.3. Evaluation The primary outcome in this study was safety and feasibility of the HAL for performance of gait training in pediatric patients with CP. Any adverse events were recorded. At the end of the intervention, we asked patients how it felt and checked patients from head to toe to determine whether any skin damage had occurred. The secondary outcome was the immediate effect after gait training with HAL. To evaluate this, we measured the following before and after the intervention: passive range of motion (PROM) in the hip, knee, and ankle joint, and the 10-m walking test (10MWT). The 10MWT was performed by the 11 patients who could walk alone with an assistive device, and one round-trip was performed at each patient’s self-selected walking speed. We measured gait parameters, including gait speed (m/min), step length (cm), and cadence (step/ min). Moreover, gait analysis was performed including joint kinematics and electromyography measurements during the 10MWT. The angles of the hip and knee joint were calculated using a recorded video of the patient taken from the lateral side using 2-dimensional-3dimensional motion analysis software (FlameDIAS version 2.00; DKH Inc., Tokyo, Japan). More than three gait cycles were used to measure accurate joint angles. The peak knee extension angle during stance and knee flexion angle at initial contact were identified. Range of hip and trunk motion were calculated and defined
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as the difference between the maximum and minimum angle of the hip joint and sagittal inclination of the trunk, respectively. Sagittal gait patterns were also classified as drop foot, jump gait, apparent equinus (AE), or crouch, as previously described by Rodda et al. [10]. In two patients with level III on the GMFCS who were able to undergo electromyogram (EMG), muscle activity was also collected bilaterally from the rectus femoris (RF), gluteus maximus (GM), vastus lateralis (VL), and semitendinosus (ST) muscles using a wireless EMG system (Trigno; Delsys, Boston, MA) recording at a sampling rate of 2,000 Hz, and with bandpass filtering of 20–450 Hz. Subsequently, an absolute EMG was integrated by time to calculate an integrated EMG (iEMG). The average values of the obtained parameters were used for analysis. 2.4. Statistical analysis For the comparison of PROM and gait parameters between before and after the intervention, paired t-test was used. A P-value of less than 0.05 was considered significant. Analyses were performed using EZR (Saitama Medical Center, Jichi Medical University, Saitama, Japan), which is a graphical user interface for R (The R Foundation for Statistical Computing, Vienna, Austria, version 2.3–1) [11]. 3. Results All 19 patients were able to carry out the gait training with HAL. The mean walking distance with HAL was 182 m (range, 20 to 480 m) and the walking time was 11.8 min (range, 6.3 to 22.1 min). The mean walking velocity was 27.3 m/min (range, 14.2 to 39.1, n = 11) and 6.6 m/min (range, 1.5 to 23.0, n = 8) in the patients who were able and unable to carry out 10MWT, respectively. Two patients (patients no. 1 and 10) had a minor skin rash on their lower limbs from a band and one patient (patient no. 4) had sore pain after the intervention, but the sores healed naturally. One very young child (patient no. 15) cried and was scared to perform the training, but he carried out the gait training with our encouragement (Table 2). No severe adverse events interrupted the intervention, and no inconvenience occurred, even after the patients returned home. The static parameters are shown in Table 3 (n = 19). The mean abduction angle of the right hip expanded significantly after the intervention, but there was no significant change in the left hip. Significant post-intervention improvements were observed in the mean internal/external rotation angles on both sides. The mean angles of the knee joint did not change significantly. The mean angles of ankle dorsiflexion also significantly improved after intervention, except for those of the right leg with the knee flexed.
Please cite this article in press as: Nakagawa S et al. Safety and immediate effects of Hybrid Assistive Limb in children with cerebral palsy: A pilot study. Brain Dev (2019), https://doi.org/10.1016/j.braindev.2019.10.003
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Patient No. Age Sex Height Weight GMFCS Speech Etiology (cm) (kg) level problems
Type of CP
Walking aids
Gait posture
10MWT
1 2
8 13
M F
123 141
21.5 23.0
2 4
No Yes
Spastic Diplegia Ataxia
AFO Walker, AFO
Jump –
Possible 480 impossible 20
14.3 10.4
33.5 1.9
3 4 5 6 7
11 10 12 10 5
M M F M M
130 138 134 127 100
29.0 29.8 21.0 29.0 16.0
3 4 4 3 4
No No Yes No Yes
Spastic Spastic Spastic Spastic Spastic
Clutch, AFO Walker, AFO Walker, AFO Clutch, AFO Walker, HKAFO
AE – – AE –
Possible impossible impossible Possible impossible
200 150 90 120 30
7.0 6.5 13.4 6.1 19.6
28.4 23.0 6.7 19.8 1.5
8 9 10 11 12 13 14 15 16 17 18 19
7 3 9 10 8 10 4 4 6 7 14 8
F M M M F M M F M F M M
127 92 124 129 120 122 99 93 112 119 154 108
30.0 11.4 26.6 29.0 24.6 26.3 12.7 14.5 18.6 20.9 41.0 16.4
1 3 4 3 3 3 4 1 3 4 2 3
No Yes Yes No No No Yes No No Yes No No
AFO Walker, AFO Walker, AFO Clutch, AFO Clutch, AFO Walker, AFO None AFO Walker HKAFO None Walker
Drop foot – – Crouch AE AE – Jump Crouch – Crouch Jump
Possible impossible impossible Possible Possible Possible impossible Possible Possible impossible Possible Possible
320 40 200 360 160 400 50 120 200 40 280 200
8.2 12.5 19.5 16.4 11.3 11.0 12.5 6.3 8.4 22.1 7.6 10.2
39.1 3.2 10.2 22.0 14.2 36.3 4.0 19.2 23.7 1.8 37.0 19.6
PVL Chromosomal abnormality PVL PVL PVL PVL Chromosomal abnormality HC unknown HC unknown PVL Neonatal meningitis unknown PVL HIE PVL PVL PVL
Diplegia Diplegia Diplegia Diplegia Diplegia
Spastic Hemiplegia Spastic Diplegia Ataxia Spastic Diplegia Spastic Diplegia Spastic Diplegia Athetoid Spastic Diplegia Spastic Diplegia Spastic Diplegia Spastic Diplegia Spastic Diplegia
Walking Walking Walking Comments distance time velocity (m) (min) (m/min) Skin rash
Sole pain occurred
Skin rash
Crying
GMFCS, Gross Motor Function Classification System; CP, cerebral palsy; 10MWT, 10-m walking test; PVL, periventricular leukomalacia; HC, hydrocephalus; HIE, hypoxic ischemic encephalopathy; AFO, ankle-foot orthosis; FO, foot orthosis; HKAFO, hip-knee-ankle-foot-orthosis; AE, apparent equinus.
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Please cite this article in press as: Nakagawa S et al. Safety and immediate effects of Hybrid Assistive Limb in children with cerebral palsy: A pilot study. Brain Dev (2019), https://doi.org/10.1016/j.braindev.2019.10.003
Table 2 Individual demographics and result of gait training.
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Table 3 Change in PROM between pre- and post-intervention (n = 19). 1 Hip (R/L) (°)
Knee (R/L) (°)
Ankle (R/L) (°)
Extension Flexion Adduction Abduction Int. rot Ext. rot Extension Flexion PA DKE DKF
Before
After
P-value
8.2 ± 9.1/10.3 ± 8.8 125.6 ± 13.6/125.0 ± 15.2 20.0 ± 8.5/20.6 ± 6.4 32.9 ± 11.5/34.1 ± 13.0 58.2 ± 22.2/57.4 ± 22.8 57.6 ± 16.1/52.9 ± 15.8 2.1 ± 5.2/ 3.5 ± 7.2 140.3 ± 7.6/140.3 ± 7.6 39.4 ± 17.0/39.4 ± 18.9 3.2 ± 12.5/1.2 ± 12.4 16.5 ± 17.0/17.4 ± 13.2
8.5 ± 10.2/11.2 ± 8.2 127.1 ± 12.3/126.2 ± 14.9 20.6 ± 8.4/20.9 ± 6.8 35.3 ± 11.2/36.5 ± 11.5 63.2 ± 17.5/66.2 ± 16.0 64.1 ± 12.9/61.5 ± 14.8 2.6 ± 3.9/ 4.1 ± 6.7 141.5 ± 5.5/141.8 ± 5.7 37.4 ± 16.2/37.9 ± 19.3 5.0 ± 13.0/2.9 ± 13.8 18.5 ± 17.5/19.4 ± 16.0
0.250/0.104 0.070/0.163 0.430/0.331 0.016*/0.185 0.040*/0.005** 0.003*/<0.001** 1.000/ 0.668 0.331/0.236 0.130/0.236 0.015*/0.028* 0.057/0.046*
PROM, passive range of motion; PA, popliteal angle; DKE, dorsiflexion in knee extension; DKF, dorsiflexion in knee flexion. * P < 0.05, ** P < 0.01.
out severe adverse events, regardless of the type of CP, and even if the patient was very young, had a short stature, or was classified as GMFCS level IV. The newly developed HAL is smaller and lighter than the previous model (target height 100–150 cm [versus 140–165 cm in the S-HAL] with an equipment weight of 5 kg [versus 14 kg in the S-HAL]), so it was possible for preschool children to perform safe gait training. This study also proved that children with communication problems or fear of performing the required tasks can perform gait training using the HAL. For small children, the video was used in advance to explain what to do so they were not scared. Previous reports of robotic rehabilitation in children with CP using Lokomat [12,13] or Gait Trainer GT 1 [14] included children 4 years and over. In the present study, the minimum age of all participants was 3 years. According to a report by Takahashi et al. [5] on gait training with HAL in patients with CP, HAL is very difficult to apply in patients with severe deformities. For pediatric patients, the surgery for contracture and bony torsion is most often required after the age of six [15], so it was thought that younger patients should be able to wear the device without severe difficulty. Furthermore, it is widely known that gross motor function
The gait parameter results are summarized in Table 4 (n = 11). Gait speed and stride length improved significantly after intervention; however, cadence did not. With regard to kinematic data, it was noted that the range of hip movement expanded significantly after intervention. The peak knee extension angle during stance, and the knee flexion angle at initial contact increased, and the range of sagittal motion of the trunk expanded, but the differences were not significant. The iEMG results are shown in Fig. 1a-d (patient no. 6) and Fig. 2a-d (patient no. 16). In patient no. 6, muscle activation of the RF, ST, and GM muscles increased in the terminal stance phase. In patient no. 16, muscle activation of the RF and GM muscles increased during the stance phase, and muscle activation of the VL, ST, and GM muscles increased during the terminal stance phase. In both patients, the VL iEMG decreased during the stance phase. 4. Discussion In this study, we demonstrated that gait training using 2S-HAL was safe and can improve the PROM and gait ability of pediatric patients with CP. Patients were able to perform gait training using the HAL with-
Table 4 Comparison of gait parameters before and after HAL intervention (n = 11). Outcome measure
Before
After
P-value
Gait speed (SD) (m/min) Step length (SD) (cm) Cadence (SD) (step/min) Kinematic data Knee extension maximum during stance (SD) (°) Knee flexion at initial contact (SD) (°) Range of hip flexion–extension (SD) (°) Range of sagittal motion of trunk (SD) (°)
47.1 (18.4) 39.9 (10.1) 115.6 (30.3)
54.7 (22.2) 43.5 (9.8) 122.1 (31.2)
0.019* <0.008** 0.127
22.5 37.0 38.7 19.3
18.8 38.5 43.0 22.2
0.508 0.316 0.028* 0.082
(14.1) (17.7) (8.0) (5.0)
(14.1) (18.0) (10.7) (4.2)
Knee flexion is positive. HAL, hybrid assistive limb; SD, standard deviation. *P < 0.05, **P < 0.01.
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Fig. 1. Pre- and post-intervention integrated electromyographic results of the rectus femoris muscle, vastus lateralis muscle, semitendinosus muscle, and gluteus maximus muscle of patient no. 6.
Fig. 2. Pre- and post-intervention integrated electromyographic results of the rectus femoris muscle, vastus lateralis muscle, semitendinosus muscle and gluteus maximus muscle of the patient no. 16.
growth reaches a plateau at around 7 years of age [4], and it has been previously reported that intensive rehabilitation is more effective for spastic diplegic CP patients if they are younger [16]. Although it would
make it difficult to compare our results with those of the older children, we considered that it was necessary to create a pediatric rehabilitation program using the HAL.
Please cite this article in press as: Nakagawa S et al. Safety and immediate effects of Hybrid Assistive Limb in children with cerebral palsy: A pilot study. Brain Dev (2019), https://doi.org/10.1016/j.braindev.2019.10.003
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The improvements in walking ability and the changes in gait pattern appear to be due to changes in muscle activity [17]. As previously reported, we measured changes in muscle activity in an 11 year old male with CP level III on the GMFCS after training with the 2SHAL [7]. In the report, we stated that the normalization of muscle balance allowed the patient to move his legs forward more easily. In this study, improvement of clearance during opposite leg swing and expansion of the hip extension range due to increased activity of the ST and GM muscles during the terminal stance phase may have been predominantly related to the increase in step length, although there were great differences in muscle activity between patients. The two patients in the present study who were able to undergo EMG showed different gait patterns, one showed AE and the other showed a crouched gait posture, and the walking aids used were also different. The form of muscle activity differs greatly between patients. The muscle activity during walking differs in children depending on age [18], and it is believed that the form of muscle activity necessary for improvement in gait differs greatly from one patient to another. This study also showed improvement in the PROM. According to past reports analyzing the kinematics after walking training using the HAL, co-contraction of the hip and knee extension/flexion muscles during walking improves [7,19]. As improvements in PROM of the knee joint were not found in this study, it is possible that this was because the muscle contractures were relatively light. The treatment options for spastic co-contraction have so far included botulinum toxin [20], selective dorsal rhizotomy [21], and orthopedic surgery [22], but robot-assisted voluntary joint exercise training may become one of the options in the future. Considering the gait parameter results and joint kinematics data obtained during the 10MWT, expansion of the range of hip flexion-extension can lead to an increase in step length, which leads to improvements in gait speed, and our results are similar to those reported by Takahashi et al. [5]. Since we performed gait training using the HAL only once, it is unlikely that muscle strengthening occurred. Some reports have revealed that robot rehabilitation including the HAL can improve the body balance and symmetry of walking in patients with several gait disorders [23–25], but pre- and post- gait analysis is rarely performed. In future studies, it will be necessary to increase the number of patients and perform a kinematic analysis using electromyography and three-dimension gait analysis to clarify how muscle activity improves following training using a robot. There were some limitations to this study. The sample size was small and follow-up period was short, therefore we should follow many patients over time to increase the level of evidence and to confirm that the effect continues. Furthermore, it was very challenging to discuss the
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effects of this intervention because they are classified by the type of cerebral palsy and because there were few cases of ataxia and athetosis. Moreover, the intervention was performed only once. It is necessary to investigate the outcomes after a number of training sessions to determine the period in which the effectiveness of walking training using HAL can be maximized. In conclusion, gait training using the newly developed HAL was safe and feasible in pediatric patients with CP. This device may normalize the motor function of the joint and improve gait ability. Funding source This work was supported by a Grant-in-Aid for Project Research (1655) from the Ibaraki Prefectural University of Health Sciences. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.braindev.2019.10.003. References [1] Rosenbaum P, Paneth N, Leviton A, Goldstein M, Bax M, Damiano D, et al. A report: the definition and classification of cerebral palsy April 2006. Dev Med Child Neurol Suppl 2007;109:8–14. [2] Blair E, Watson L. Epidemiology of cerebral palsy. Semin Fetal Neonatal Med 2006;11:117–25. [3] Kerr Graham H, Selber P. Musculoskeletal aspects of cerebral palsy. J Bone Joint Surg Br 2003;85:157–66. [4] Hanna SE, Rosenbaum PL, Bartlett DJ, Palisano RJ, Walter SD, Avery L, et al. Stability and decline in gross motor function among children and youth with cerebral palsy aged 2 to 21 years. Dev Med Child Neurol 2009;51:295–302. [5] Takahashi K, Mutsuzaki H, Mataki Y, Yoshikawa K, Matsuda M, Enomoto K, et al. Safety and immediate effect of gait training using a Hybrid Assistive Limb in patients with cerebral palsy. J Phys Ther Sci 2018;30:1009–13. [6] Kawamoto H, Sankai Y. Power assist method based on phase sequence and muscle force condition for HAL. Adv Robotics 2005;19:717–34. [7] Nakagawa S, Mutsuzaki H, Mataki Y, Endo Y, Matsuda M, Yoshikawa K, et al. Newly developed hybrid assistive limb for pediatric patients with cerebral palsy: a case report. J Phys Ther Sci 2019;31:702–7. [8] Palisano R, Rosenbaum P, Walter S, Russell D, Wood E, Galuppi B. Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol 1997;39:214–23. [9] Matsuda M, Mataki Y, Mutsuzaki H, Yoshikawa K, Takahashi K, Enomoto K, et al. Immediate effects of a single session of robot-assisted gait training using Hybrid Assistive Limb (HAL) for cerebral palsy. J Phys Ther Sci 2018;30:207–12. [10] Rodda J, Graham HK. Classification of gait patterns in spastic hemiplegia and spastic diplegia: a basis for a management algorithm. Eur J Neurol 2001;8:98–108. [11] Kanda Y. Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant 2013;48:452–8.
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[19] Endo Y, Mutsuzaki H, Mizukami M, Yoshikawa K, Kobayashi Y, Yozu A, et al. Long-term sustained effect of gait training using a hybrid assistive limb on gait stability via prevention of knee collapse in a patient with cerebral palsy: a case report. J Phys Ther Sci 2018;30:1206–10. [20] Borton D, Walker K, Pirpiris M, Nattrass G, Graham H. Isolated calf lengthening in cerebral palsy: outcome analysis of risk factors. J Bone Joint Surg Br 2001;83:364–70. [21] Wright FV, Sheil EM, Drake JM, Wedge JH, Naumann S. Evaluation of selective dorsal rhizotomy for the reduction of spasticity in cerebral palsy: a randomized controlled trial. Dev Med Child Neurol 1998;40:239–47. [22] McGinley JL, Dobson F, Ganeshalingam R, Shore BJ, Rutz E, Graham HK. Single-event multilevel surgery for children with cerebral palsy: a systematic review. Dev Med Child Neurol 2012;54:117–28. [23] Kawamoto H, Kamibayashi K, Nakata Y, Yamawaki K, Ariyasu R, Sankai Y, et al. Pilot study of locomotion improvement using hybrid assistive limb in chronic stroke patients. BMC Neurol 2013;13:141. [24] Bertolucci F, Di Martino S, Orsucci D, Ienco EC, Siciliano G, Rossi B, et al. Robotic gait training improves motor skills and quality of life in hereditary spastic paraplegia. NeuroRehabilitation 2015;36:93–9. [25] Matsuda M, Iwasaki N, Mataki Y, Mutsuzaki H, Yoshikawa K, Takahashi K, et al. Robot-assisted training using Hybrid Assistive LimbÒ for cerebral palsy. Brain Dev 2018;40:642–8.
Please cite this article in press as: Nakagawa S et al. Safety and immediate effects of Hybrid Assistive Limb in children with cerebral palsy: A pilot study. Brain Dev (2019), https://doi.org/10.1016/j.braindev.2019.10.003
Original article
Safety and immediate effects of Hybrid Assistive Limb in children with cerebral palsy: A pilot study Shogo Nakagawa a,b, Hirotaka Mutsuzaki b,c, Yuki Mataki b, Yusuke Endo d Mayumi Matsuda e, Kenichi Yoskikawa e, Hiroshi Kamada a,⇑, Nobuaki Iwasaki c,f Masashi Yamazaki a b
a Department of Orthopaedic Surgery, Faculty of Medicine, University of Tsukuba, Japan Department of Orthopaedic Surgery, Ibaraki Prefectural University of Health Sciences Hospital, Japan c Center for Medical Sciences, Ibaraki Prefectural University of Health Sciences, Japan d Department of Physical Therapy, Faculty of Health Science, Health Science University, Japan e Department of Physical Therapy, Ibaraki Prefectural University of Health Sciences Hospital, Japan f Department of Pediatrics, Ibaraki Prefectural University of Health Sciences, Japan
Received 9 August 2019; received in revised form 3 October 2019; accepted 4 October 2019
Abstract Purpose: Early intervention is effective for developing motor ability and preventing contractures and deformities in patients with cerebral palsy (CP). Gait training using the newly developed Hybrid Assistive Limb (HAL) shows promise as an intervention to prevent deterioration in walking ability and deformities in pediatric CP patients. The purpose of this pilot study was to examine the safety and immediate effects on walking ability after gait training using the HAL in pediatric CP patients. Methods: Nineteen patients (six females, 13 males; mean age 8.5 years; mean height 120.5 cm; mean weight 23.2 kg) were enrolled. The Gross Motor Functional Classification Scale level was I in two patients, II in two, III in eight, and IV in seven. The HAL was used for a single session of gait training. The primary outcome was safety of the HAL for use in pediatric CP patients. The secondary outcome was the immediate effect after gait training with HAL, evaluated by passive range of motion (ROM) and gait parameters, including gait speed (m/s), step length (cm), and cadence (step/min). Results: All 19 patients were able to carry out the gait training without any severe adverse events. Significant improvements were observed for mean internal/external rotation and abduction angles of the hip joint, and ankle dorsiflexion angles (n = 19). Significant improvements were observed for mean gait speed and step length based on expansion of the hip flexion-extension range (n = 11). Conclusion: Gait training using the HAL is safe and can produce immediate improvements in ROM and walking ability in pediatric patients with CP. Ó 2019 Published by Elsevier B.V. on behalf of The Japanese Society of Child Neurology.
Keywords: Cerebral palsy; Hybrid Assistive Limb; Pediatrics; Safety; Immediate effect
1. Introduction ⇑ Corresponding author at: Department of Orthopaedic Surgery, Faculty of Medicine, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki 305-8575, Japan. E-mail address: [email protected] (H. Kamada).
Cerebral palsy (CP) is defined as a group of permanent progressive disorders of the development of movement and posture which cause activity limitation
https://doi.org/10.1016/j.braindev.2019.10.003 0387-7604/Ó 2019 Published by Elsevier B.V. on behalf of The Japanese Society of Child Neurology.
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attributed to non-progressive disturbances that occur in the developing fetal or infant brain [1] (1). The brain lesion is a static encephalopathy, but the musculoskeletal pathology is progressive [2]. Although a newborn child with CP usually has no bone deformities or musculoskeletal abnormalities at birth [3], it is generally assumed that around the age of 6 to 12 years, development of gross motor function has reached a plateau and gait parameters show deterioration as joint contractures and bony deformities increase [4]. Earlier intervention is reportedly effective for both motor ability development and prevention of contractures and deformities. In our previous study, we reported that among 19 patients with CP with an average age of 15.0 years, gait training using the Hybrid Assistive Limb (HAL, Cyberdyne, Tsukuba, Japan) was safe and provided immediate positive effects on walking ability [5]. However, we could not include younger children in this study as the HAL was not suitable for younger children with shorter stature at that time. The HAL receives electric signals sent from the brain to the muscles, amplifies them using a computer, and analyzes them in conjunction with a weighting sensor at the sole of the wearer’s foot in order to support optimal joint motion for walking [6]. If gait training can be performed using the HAL before the plateau of motor growth is reached and therefore, prevent deterioration in walking ability, this may also lead to prevention of deformities. Recently, as a case report, we reported that a new smaller and lighter-weight HAL has been developed for pediatric patients and could be safe and feasible for gait training in pediatric patients with CP [7]. We believe that further improvements in walking ability could result from the use of this HAL in younger pediatric patients with a shorter stature. The purpose of this pilot study was to examine the safety and immediate effect on walking ability after gait training using the newly developed HAL in pediatric patients with any type of CP. 2. Methods 2.1. Patients Approval for this study was granted by the Human Ethics Review Committee of Ibaraki Prefectural University of Health Sciences (approval numbers: 682, e83, and e119). We recruited outpatient children with CP aged 14 years or younger from October 2018 to June 2019. The inclusion criteria were (i) diagnosis of CP according to the Gross Motor Function Classification System (GMFCS) [8] levels of I to IV, (ii) usual participation in traditional rehabilitation, including gait training, and (iii) easy recognition of the signals of pain, fear, and discomfort with reliance on the parents. The
patients were excluded if there was (i) difficulty wearing the HAL due to size mismatch, (ii) lack of patient cooperation, or (iii) presence of a severe condition of the heart or lung. Nineteen patients met our inclusion criteria. The intervention method was explained to the patient and their parents using a movie, and written informed consent was obtained from the patient’s parents before intervention was performed. We obtained the following clinical information from parents and our institutional medical records: patient age, sex, cause and type of CP, GMFCS level, presence or absence of speech problems, and the use of walking aids and orthoses. Regarding speech problems, if the patient had never or sometimes exhibited speech problems, we described this as ‘‘no”; however, if speech problems were often exhibited, we described this as ‘‘yes”. There were six female patients and 13 male patients with a mean age of 8.5 years (range, 3 to 14). The mean height was 120.5 cm and the mean weight was 23.2 kg. Of all children with CP, 15 were diagnosed with spastic diplegia, one with spastic hemiplegia, two with ataxia, and one with athetosis. According to the GMFCS, two patients were classified as level I, two as level II, seven as level III, and seven as level IV. Seven patients had speech problems (Table 1). 2.2. HAL training Before the gait training, we measured each patient’s range of motion of the hip, knee, and ankle joint. HAL gait training was performed during standard physical therapy sessions as part of an inpatient stay at our hospital. We used the newly developed HAL (2SHAL; HAL-ML06, lower limb type, 2S size). The weight
Table 1 Clinical characteristics. Mean age (range) (years) Sex (n)
8.5 (3–14) female male
6 13 120.5 (16.6) 23.2 (7.4)
Spastic Diplegia Spastic Hemiplegia Ataxia Athetosis
15 1 2 1
I II III IV
2 2 8 7
No Yes
12 7
Mean height (SD) (cm) Mean weight (SD) (kg) Type of CP (n)
GMFCS level (n)
Speech problems
SD, standard deviation; CP, cerebral palsy; GMFCS, Gross Motor Function Classification System.
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of the 2S-HAL is about 5 kg, which is less than half that of the previous model (S-HAL; HAL-ML05, lower limb type, S size), and its target user is children with a height of 100–150 cm and a body weight of 15–40 kg. The device was attached to the patient’s thighs and lower legs using bands and cushioning material if needed. Ankle-foot orthoses were used in the sensor shoes of the HAL if the patient had drop feet. After positioning the device, flexion/extension balance and assist torque at the hip and knee joints were optimized. To avoid falling, a walking device was used according to patient preference (either an All-in-One Walking Trainer [Ropox A/S, Naestved, Denmark] or a posture control walker). Of the two therapists who provided assistance, the person in front led the patient in the correct direction, and the person at the back assisted the patient to maintain a good gait pattern by providing feedback. Gait training sessions using the HAL lasted for about 20 min, including a rest time. Patients controlled their own gait speed in this intervention. We adjusted the flexion/extension balance and assist torque during gait training so that the cybernic voluntary control mode (CVC) and walk modes, which help the patient’s spontaneous movements, were used as much as possible [9]. 2.3. Evaluation The primary outcome in this study was safety and feasibility of the HAL for performance of gait training in pediatric patients with CP. Any adverse events were recorded. At the end of the intervention, we asked patients how it felt and checked patients from head to toe to determine whether any skin damage had occurred. The secondary outcome was the immediate effect after gait training with HAL. To evaluate this, we measured the following before and after the intervention: passive range of motion (PROM) in the hip, knee, and ankle joint, and the 10-m walking test (10MWT). The 10MWT was performed by the 11 patients who could walk alone with an assistive device, and one round-trip was performed at each patient’s self-selected walking speed. We measured gait parameters, including gait speed (m/min), step length (cm), and cadence (step/ min). Moreover, gait analysis was performed including joint kinematics and electromyography measurements during the 10MWT. The angles of the hip and knee joint were calculated using a recorded video of the patient taken from the lateral side using 2-dimensional-3dimensional motion analysis software (FlameDIAS version 2.00; DKH Inc., Tokyo, Japan). More than three gait cycles were used to measure accurate joint angles. The peak knee extension angle during stance and knee flexion angle at initial contact were identified. Range of hip and trunk motion were calculated and defined
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as the difference between the maximum and minimum angle of the hip joint and sagittal inclination of the trunk, respectively. Sagittal gait patterns were also classified as drop foot, jump gait, apparent equinus (AE), or crouch, as previously described by Rodda et al. [10]. In two patients with level III on the GMFCS who were able to undergo electromyogram (EMG), muscle activity was also collected bilaterally from the rectus femoris (RF), gluteus maximus (GM), vastus lateralis (VL), and semitendinosus (ST) muscles using a wireless EMG system (Trigno; Delsys, Boston, MA) recording at a sampling rate of 2,000 Hz, and with bandpass filtering of 20–450 Hz. Subsequently, an absolute EMG was integrated by time to calculate an integrated EMG (iEMG). The average values of the obtained parameters were used for analysis. 2.4. Statistical analysis For the comparison of PROM and gait parameters between before and after the intervention, paired t-test was used. A P-value of less than 0.05 was considered significant. Analyses were performed using EZR (Saitama Medical Center, Jichi Medical University, Saitama, Japan), which is a graphical user interface for R (The R Foundation for Statistical Computing, Vienna, Austria, version 2.3–1) [11]. 3. Results All 19 patients were able to carry out the gait training with HAL. The mean walking distance with HAL was 182 m (range, 20 to 480 m) and the walking time was 11.8 min (range, 6.3 to 22.1 min). The mean walking velocity was 27.3 m/min (range, 14.2 to 39.1, n = 11) and 6.6 m/min (range, 1.5 to 23.0, n = 8) in the patients who were able and unable to carry out 10MWT, respectively. Two patients (patients no. 1 and 10) had a minor skin rash on their lower limbs from a band and one patient (patient no. 4) had sore pain after the intervention, but the sores healed naturally. One very young child (patient no. 15) cried and was scared to perform the training, but he carried out the gait training with our encouragement (Table 2). No severe adverse events interrupted the intervention, and no inconvenience occurred, even after the patients returned home. The static parameters are shown in Table 3 (n = 19). The mean abduction angle of the right hip expanded significantly after the intervention, but there was no significant change in the left hip. Significant post-intervention improvements were observed in the mean internal/external rotation angles on both sides. The mean angles of the knee joint did not change significantly. The mean angles of ankle dorsiflexion also significantly improved after intervention, except for those of the right leg with the knee flexed.
Please cite this article in press as: Nakagawa S et al. Safety and immediate effects of Hybrid Assistive Limb in children with cerebral palsy: A pilot study. Brain Dev (2019), https://doi.org/10.1016/j.braindev.2019.10.003
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Patient No. Age Sex Height Weight GMFCS Speech Etiology (cm) (kg) level problems
Type of CP
Walking aids
Gait posture
10MWT
1 2
8 13
M F
123 141
21.5 23.0
2 4
No Yes
Spastic Diplegia Ataxia
AFO Walker, AFO
Jump –
Possible 480 impossible 20
14.3 10.4
33.5 1.9
3 4 5 6 7
11 10 12 10 5
M M F M M
130 138 134 127 100
29.0 29.8 21.0 29.0 16.0
3 4 4 3 4
No No Yes No Yes
Spastic Spastic Spastic Spastic Spastic
Clutch, AFO Walker, AFO Walker, AFO Clutch, AFO Walker, HKAFO
AE – – AE –
Possible impossible impossible Possible impossible
200 150 90 120 30
7.0 6.5 13.4 6.1 19.6
28.4 23.0 6.7 19.8 1.5
8 9 10 11 12 13 14 15 16 17 18 19
7 3 9 10 8 10 4 4 6 7 14 8
F M M M F M M F M F M M
127 92 124 129 120 122 99 93 112 119 154 108
30.0 11.4 26.6 29.0 24.6 26.3 12.7 14.5 18.6 20.9 41.0 16.4
1 3 4 3 3 3 4 1 3 4 2 3
No Yes Yes No No No Yes No No Yes No No
AFO Walker, AFO Walker, AFO Clutch, AFO Clutch, AFO Walker, AFO None AFO Walker HKAFO None Walker
Drop foot – – Crouch AE AE – Jump Crouch – Crouch Jump
Possible impossible impossible Possible Possible Possible impossible Possible Possible impossible Possible Possible
320 40 200 360 160 400 50 120 200 40 280 200
8.2 12.5 19.5 16.4 11.3 11.0 12.5 6.3 8.4 22.1 7.6 10.2
39.1 3.2 10.2 22.0 14.2 36.3 4.0 19.2 23.7 1.8 37.0 19.6
PVL Chromosomal abnormality PVL PVL PVL PVL Chromosomal abnormality HC unknown HC unknown PVL Neonatal meningitis unknown PVL HIE PVL PVL PVL
Diplegia Diplegia Diplegia Diplegia Diplegia
Spastic Hemiplegia Spastic Diplegia Ataxia Spastic Diplegia Spastic Diplegia Spastic Diplegia Athetoid Spastic Diplegia Spastic Diplegia Spastic Diplegia Spastic Diplegia Spastic Diplegia
Walking Walking Walking Comments distance time velocity (m) (min) (m/min) Skin rash
Sole pain occurred
Skin rash
Crying
GMFCS, Gross Motor Function Classification System; CP, cerebral palsy; 10MWT, 10-m walking test; PVL, periventricular leukomalacia; HC, hydrocephalus; HIE, hypoxic ischemic encephalopathy; AFO, ankle-foot orthosis; FO, foot orthosis; HKAFO, hip-knee-ankle-foot-orthosis; AE, apparent equinus.
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Table 2 Individual demographics and result of gait training.
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Table 3 Change in PROM between pre- and post-intervention (n = 19). 1 Hip (R/L) (°)
Knee (R/L) (°)
Ankle (R/L) (°)
Extension Flexion Adduction Abduction Int. rot Ext. rot Extension Flexion PA DKE DKF
Before
After
P-value
8.2 ± 9.1/10.3 ± 8.8 125.6 ± 13.6/125.0 ± 15.2 20.0 ± 8.5/20.6 ± 6.4 32.9 ± 11.5/34.1 ± 13.0 58.2 ± 22.2/57.4 ± 22.8 57.6 ± 16.1/52.9 ± 15.8 2.1 ± 5.2/ 3.5 ± 7.2 140.3 ± 7.6/140.3 ± 7.6 39.4 ± 17.0/39.4 ± 18.9 3.2 ± 12.5/1.2 ± 12.4 16.5 ± 17.0/17.4 ± 13.2
8.5 ± 10.2/11.2 ± 8.2 127.1 ± 12.3/126.2 ± 14.9 20.6 ± 8.4/20.9 ± 6.8 35.3 ± 11.2/36.5 ± 11.5 63.2 ± 17.5/66.2 ± 16.0 64.1 ± 12.9/61.5 ± 14.8 2.6 ± 3.9/ 4.1 ± 6.7 141.5 ± 5.5/141.8 ± 5.7 37.4 ± 16.2/37.9 ± 19.3 5.0 ± 13.0/2.9 ± 13.8 18.5 ± 17.5/19.4 ± 16.0
0.250/0.104 0.070/0.163 0.430/0.331 0.016*/0.185 0.040*/0.005** 0.003*/<0.001** 1.000/ 0.668 0.331/0.236 0.130/0.236 0.015*/0.028* 0.057/0.046*
PROM, passive range of motion; PA, popliteal angle; DKE, dorsiflexion in knee extension; DKF, dorsiflexion in knee flexion. * P < 0.05, ** P < 0.01.
out severe adverse events, regardless of the type of CP, and even if the patient was very young, had a short stature, or was classified as GMFCS level IV. The newly developed HAL is smaller and lighter than the previous model (target height 100–150 cm [versus 140–165 cm in the S-HAL] with an equipment weight of 5 kg [versus 14 kg in the S-HAL]), so it was possible for preschool children to perform safe gait training. This study also proved that children with communication problems or fear of performing the required tasks can perform gait training using the HAL. For small children, the video was used in advance to explain what to do so they were not scared. Previous reports of robotic rehabilitation in children with CP using Lokomat [12,13] or Gait Trainer GT 1 [14] included children 4 years and over. In the present study, the minimum age of all participants was 3 years. According to a report by Takahashi et al. [5] on gait training with HAL in patients with CP, HAL is very difficult to apply in patients with severe deformities. For pediatric patients, the surgery for contracture and bony torsion is most often required after the age of six [15], so it was thought that younger patients should be able to wear the device without severe difficulty. Furthermore, it is widely known that gross motor function
The gait parameter results are summarized in Table 4 (n = 11). Gait speed and stride length improved significantly after intervention; however, cadence did not. With regard to kinematic data, it was noted that the range of hip movement expanded significantly after intervention. The peak knee extension angle during stance, and the knee flexion angle at initial contact increased, and the range of sagittal motion of the trunk expanded, but the differences were not significant. The iEMG results are shown in Fig. 1a-d (patient no. 6) and Fig. 2a-d (patient no. 16). In patient no. 6, muscle activation of the RF, ST, and GM muscles increased in the terminal stance phase. In patient no. 16, muscle activation of the RF and GM muscles increased during the stance phase, and muscle activation of the VL, ST, and GM muscles increased during the terminal stance phase. In both patients, the VL iEMG decreased during the stance phase. 4. Discussion In this study, we demonstrated that gait training using 2S-HAL was safe and can improve the PROM and gait ability of pediatric patients with CP. Patients were able to perform gait training using the HAL with-
Table 4 Comparison of gait parameters before and after HAL intervention (n = 11). Outcome measure
Before
After
P-value
Gait speed (SD) (m/min) Step length (SD) (cm) Cadence (SD) (step/min) Kinematic data Knee extension maximum during stance (SD) (°) Knee flexion at initial contact (SD) (°) Range of hip flexion–extension (SD) (°) Range of sagittal motion of trunk (SD) (°)
47.1 (18.4) 39.9 (10.1) 115.6 (30.3)
54.7 (22.2) 43.5 (9.8) 122.1 (31.2)
0.019* <0.008** 0.127
22.5 37.0 38.7 19.3
18.8 38.5 43.0 22.2
0.508 0.316 0.028* 0.082
(14.1) (17.7) (8.0) (5.0)
(14.1) (18.0) (10.7) (4.2)
Knee flexion is positive. HAL, hybrid assistive limb; SD, standard deviation. *P < 0.05, **P < 0.01.
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Fig. 1. Pre- and post-intervention integrated electromyographic results of the rectus femoris muscle, vastus lateralis muscle, semitendinosus muscle, and gluteus maximus muscle of patient no. 6.
Fig. 2. Pre- and post-intervention integrated electromyographic results of the rectus femoris muscle, vastus lateralis muscle, semitendinosus muscle and gluteus maximus muscle of the patient no. 16.
growth reaches a plateau at around 7 years of age [4], and it has been previously reported that intensive rehabilitation is more effective for spastic diplegic CP patients if they are younger [16]. Although it would
make it difficult to compare our results with those of the older children, we considered that it was necessary to create a pediatric rehabilitation program using the HAL.
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The improvements in walking ability and the changes in gait pattern appear to be due to changes in muscle activity [17]. As previously reported, we measured changes in muscle activity in an 11 year old male with CP level III on the GMFCS after training with the 2SHAL [7]. In the report, we stated that the normalization of muscle balance allowed the patient to move his legs forward more easily. In this study, improvement of clearance during opposite leg swing and expansion of the hip extension range due to increased activity of the ST and GM muscles during the terminal stance phase may have been predominantly related to the increase in step length, although there were great differences in muscle activity between patients. The two patients in the present study who were able to undergo EMG showed different gait patterns, one showed AE and the other showed a crouched gait posture, and the walking aids used were also different. The form of muscle activity differs greatly between patients. The muscle activity during walking differs in children depending on age [18], and it is believed that the form of muscle activity necessary for improvement in gait differs greatly from one patient to another. This study also showed improvement in the PROM. According to past reports analyzing the kinematics after walking training using the HAL, co-contraction of the hip and knee extension/flexion muscles during walking improves [7,19]. As improvements in PROM of the knee joint were not found in this study, it is possible that this was because the muscle contractures were relatively light. The treatment options for spastic co-contraction have so far included botulinum toxin [20], selective dorsal rhizotomy [21], and orthopedic surgery [22], but robot-assisted voluntary joint exercise training may become one of the options in the future. Considering the gait parameter results and joint kinematics data obtained during the 10MWT, expansion of the range of hip flexion-extension can lead to an increase in step length, which leads to improvements in gait speed, and our results are similar to those reported by Takahashi et al. [5]. Since we performed gait training using the HAL only once, it is unlikely that muscle strengthening occurred. Some reports have revealed that robot rehabilitation including the HAL can improve the body balance and symmetry of walking in patients with several gait disorders [23–25], but pre- and post- gait analysis is rarely performed. In future studies, it will be necessary to increase the number of patients and perform a kinematic analysis using electromyography and three-dimension gait analysis to clarify how muscle activity improves following training using a robot. There were some limitations to this study. The sample size was small and follow-up period was short, therefore we should follow many patients over time to increase the level of evidence and to confirm that the effect continues. Furthermore, it was very challenging to discuss the
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effects of this intervention because they are classified by the type of cerebral palsy and because there were few cases of ataxia and athetosis. Moreover, the intervention was performed only once. It is necessary to investigate the outcomes after a number of training sessions to determine the period in which the effectiveness of walking training using HAL can be maximized. In conclusion, gait training using the newly developed HAL was safe and feasible in pediatric patients with CP. This device may normalize the motor function of the joint and improve gait ability. Funding source This work was supported by a Grant-in-Aid for Project Research (1655) from the Ibaraki Prefectural University of Health Sciences. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.braindev.2019.10.003. References [1] Rosenbaum P, Paneth N, Leviton A, Goldstein M, Bax M, Damiano D, et al. A report: the definition and classification of cerebral palsy April 2006. Dev Med Child Neurol Suppl 2007;109:8–14. [2] Blair E, Watson L. Epidemiology of cerebral palsy. Semin Fetal Neonatal Med 2006;11:117–25. [3] Kerr Graham H, Selber P. Musculoskeletal aspects of cerebral palsy. J Bone Joint Surg Br 2003;85:157–66. [4] Hanna SE, Rosenbaum PL, Bartlett DJ, Palisano RJ, Walter SD, Avery L, et al. Stability and decline in gross motor function among children and youth with cerebral palsy aged 2 to 21 years. Dev Med Child Neurol 2009;51:295–302. [5] Takahashi K, Mutsuzaki H, Mataki Y, Yoshikawa K, Matsuda M, Enomoto K, et al. Safety and immediate effect of gait training using a Hybrid Assistive Limb in patients with cerebral palsy. J Phys Ther Sci 2018;30:1009–13. [6] Kawamoto H, Sankai Y. Power assist method based on phase sequence and muscle force condition for HAL. Adv Robotics 2005;19:717–34. [7] Nakagawa S, Mutsuzaki H, Mataki Y, Endo Y, Matsuda M, Yoshikawa K, et al. Newly developed hybrid assistive limb for pediatric patients with cerebral palsy: a case report. J Phys Ther Sci 2019;31:702–7. [8] Palisano R, Rosenbaum P, Walter S, Russell D, Wood E, Galuppi B. Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol 1997;39:214–23. [9] Matsuda M, Mataki Y, Mutsuzaki H, Yoshikawa K, Takahashi K, Enomoto K, et al. Immediate effects of a single session of robot-assisted gait training using Hybrid Assistive Limb (HAL) for cerebral palsy. J Phys Ther Sci 2018;30:207–12. [10] Rodda J, Graham HK. Classification of gait patterns in spastic hemiplegia and spastic diplegia: a basis for a management algorithm. Eur J Neurol 2001;8:98–108. [11] Kanda Y. Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant 2013;48:452–8.
Please cite this article in press as: Nakagawa S et al. Safety and immediate effects of Hybrid Assistive Limb in children with cerebral palsy: A pilot study. Brain Dev (2019), https://doi.org/10.1016/j.braindev.2019.10.003
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Please cite this article in press as: Nakagawa S et al. Safety and immediate effects of Hybrid Assistive Limb in children with cerebral palsy: A pilot study. Brain Dev (2019), https://doi.org/10.1016/j.braindev.2019.10.003