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Feasibility of Neurorehabilitation Using a Hybrid Assistive Limb for Patients Who Underwent Spine Surgery

Feasibility of Neurorehabilitation Using a Hybrid Assistive Limb for Patients Who Underwent Spine... Hindawi Applied Bionics and Biomechanics Volume 2018, Article ID 7435746, 11 pages https://doi.org/10.1155/2018/7435746 Research Article Feasibility of Neurorehabilitation Using a Hybrid Assistive Limb for Patients Who Underwent Spine Surgery 1,2 1 1,2 2 1 Aya Yatsugi, Takashi Morishita , Hiroyuki Fukuda, Naoya Kotani, Kenji Yagi, 1 2 1 Hiroshi Abe, Etsuji Shiota, and Tooru Inoue Department of Neurological Surgery, Fukuoka University Faculty of Medicine, Fukuoka, Japan Department of Rehabilitation Medicine, Fukuoka University Hospital, Fukuoka, Japan Correspondence should be addressed to Takashi Morishita; tmorishita@fukuoka-u.ac.jp Received 17 February 2018; Revised 21 May 2018; Accepted 19 June 2018; Published 10 July 2018 Academic Editor: Liwei Shi Copyright © 2018 Aya Yatsugi et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Recent studies of robotic rehabilitation have demonstrated its efficacy for neurological disorders. However, few studies have used the Hybrid Assistive Limb (HAL) during the early postoperative stage of spine disorders. We aimed to evaluate the safety and efficacy of HAL treatment during the early postoperative period for spine disorder patients. We retrospectively identified patients who underwent spine surgery and who could complete HAL treatment. We evaluated the 10-m walking test (10MWT), the modified Gait Abnormality Rating Scale (GARS-M), Barthel Index (BI), and the walking index for spinal cord injury II (WISCI II) score results before and after robotic rehabilitation. Clinical outcomes were compared after treatment. We included nine patients with various spine problems. After HAL treatment, the speed during the 10MWT significantly improved from 64.1 ± 16.0 to 74.8 ± 10.8 m/min, and the walking cadence decreased from 102.7 ± 17.6 to 92.7 ± 10.9 steps/min. The BI score also improved from 83.3 ± 16.0 to 95.6 ± 5.8, and the WISCI II score improved from 19.7 ± 0.5 to 20.0 ± 0.0. Furthermore, the total GARS-M score improved from 6.0 ± 5.7 to 2.3 ± 3.3. The maximum angles of the trunk swing were improved from 2.2 ± 1.9 to 1.2 ± 0.9 degrees. Neurorehabilitation therapy using HAL for spinal surgery patients was considered feasible following spine surgery. 1. Introduction generate sensory feedback to the brain (i.e., iBF) and acceler- ate motor learning in the process of functional recovery. Recent studies have shown the safety and efficacy of reha- Robotic technologies have been increasingly gaining atten- bilitation using HAL robotics for various disorders, including tion in the field of neurorehabilitation. The Hybrid Assistive stroke [3–7], spinal cord injury (SCI) [8–14], and quadriceps Limb (HAL) (Cyberdyne Inc., Ibaraki, Japan) is a unique arthrogenic muscle inhibition [15]. Another recent study exoskeleton robot for neurorehabilitation that was developed by Sankai and colleagues based on the interactive biofeed- demonstrated neuroplasticity induced by HAL treatment [16, 17]. However, five case reports have focused on the effi- back (iBF) theory [1, 2]. HAL has a hybrid system that allows cacy of HAL therapy for postoperative thoracic ossification of both voluntary and autonomous modes of action to support the posterior longitudinal ligament (OPLL) [18–22]. These training, and it supports voluntary muscle movement by reports indicated that HAL was used as a last resort for gait detecting bioelectrical signals (BES). For walking training, movements of the joints are accurately adjusted by the pres- recovery during the almost chronic phase of the postopera- tive state [21, 22], and the authors recommended starting sure sensor in the foot bottom and joint angle sensors of the HAL-assisted training during the early stage following sur- frame. Based on the input information, four actuators of the gery. Neurorehabilitation during the postoperative state is hip and knee joint are controlled independently [3]. Move- essential for returning to social activities and preventing ments of the affected limbs supported by the HAL system 2 Applied Bionics and Biomechanics disuse syndrome. Based on the findings indicated by these All spine disorders five case reports [18–22], in addition to the reports demon- treated with HAL N = 31 strating the efficacy of HAL training for SCI cases [8–14], we hypothesized that using HAL may facilitate early recovery Nonoperative cases after spine surgery. Therefore, we aimed to evaluate the safety (N = 13) and efficacy of HAL-assisted rehabilitation for spine disorder Surgical cases patients during the early postoperative period. N = 18 Severely impaired patients who were 2. Materials and Methods unable to use HAL (N = 5) <3 sessions of HAL treatment (N = 4) 2.1. Patient Selection and Study Design. We performed a ret- rospective chart review of patients with spine disorders treated at our neurosurgical department from October 2011 Total participants to February 2016. To evaluate the effects of HAL treatment N = 9 for improvements in gait, we included patients who could Figure 1: Patient selection flowchart. complete HAL treatment at least three times. Additionally, because voluntary muscle contractions are required to gain assistance from the HAL system, we excluded patients with performed by one or two physiotherapists and a medical doc- tor who were trained to use the HAL system. During gait complete or nearly complete paralysis. The protocol of the present study was approved by our institutional review board training, the physiotherapist checked the BES and adjusted the HAL assist level. (IRB), and HAL treatment was performed after receiving written informed consent from each patient. During HAL treatment, several sets of a knee extension HAL treatment was performed for 31 patients with spine movement were performed (10 times with the left leg and 10 times with the right leg). The standing movement was per- disorders; however, 22 patients did not meet the inclusion criteria of the current study (Figure 1). Among those 22 formed 10 times. Balance training was performed for several seconds with open eyes or closed eyes so that the center of patients, 13 did not undergo surgery. We investigated the remaining nine patients (six male gravity would be in the middle. Finally, walking training patients and three female patients) with the following charac- was performed on a flat ground or a treadmill. During bal- ance training and gait training, we used a monitor displayed teristics: severe impairment resulting in the inability to use HAL (n =5) and less than three sessions of HAL treat- in front of the patient to provide visual feedback regarding the center of gravity, posture, and balance (Figure 2). ment (n =4). The mean age of the cohort was 53.6 years (SD, ±16.1). Diagnoses were dural arteriovenous fistula We focused on walking training. We used a walk aid (AVF) (n =2), cervical ossification of the posterior longitudi- called All-In-One Walking Trainer (Ropox A/S, Naestved, Denmark) to secure the safety of patients when walking on nal ligament (OPLL) (n =1), spinal lipoma (n =1), arachnoid cyst (n =1), spinal ependymoma (n =3), and cervical spon- a flat floor. It is able to support body weight and enables safe HAL treatment with the use of a harness. We did not use dylosis (n =1). Spine lesion levels are summarized in Table 1. body weight support. After the patient became accustomed 2.2. Rehabilitation Program. We performed conventional to walking on the ground, we began treadmill walking. Patients performed several sets of 5 minutes of walking at a physical therapy in addition to HAL treatment. Conventional physical therapy started within 2 days after surgery. Depend- speed that was comfortable with HAL. If patients wanted to ing on the patient’s condition, the programs included manual continue and were not fatigued, then we increased the speed leg stretching, muscular workouts, and basic movement or increased the walking time. When there was deflection of training such as standing, walking, and going up and down the center of gravity (it does not take weight to walk on tip- toes), we instructed the patient to move the weight from stairs. When patients felt fatigue during the HAL treatment, they were allowed to rest. Each session lasted approximately the heel to the tiptoes. 50 minutes, including time necessary for robotic attachment, and was performed two or three times per week. 2.3. Outcome Measures. All patients were video-recorded HAL treatment started when the patients were able to sit during rehabilitation. The speed and steps during the 10-m stably. On average, intervention with therapists and HAL walking test (10MWT) as an evaluation of motor function treatment began 14.2 ± 8.1 days (range 7–29 days) after at the time of treatment immediately before wearing HAL surgery. The mean number of HAL treatment sessions was and during the last training session after excluding HAL were 5.0 ± 2.6 (range 3–12). Rehabilitation periods comprised used to evaluate HAL treatment times. We used the modified 13.6 ± 9.1 days (range 4–35 days) during hospitalization at Gait Abnormality Rating Scale (GARS-M) [23], the Barthel our institution (Table 1). Index (BI), and the walking index for spinal cord injury II A bilateral leg version of HAL was used for patients (WISCI II) to evaluate walking appearance, activities of daily involved in this study (HAL for Living Support–Lower Limb; living (ADL), and the patients’ ambulatory walking capacity Cyberdyne Inc.). Training started with the Cybernic Volun- on the basis of the need for physical assistance and assistive tary Control mode, which measures BES from the extensor devices, respectively [24]. The GARS-M includes variables and flexor muscles of the hip and knee. HAL treatment was that provide a description of gait associated with an increased Applied Bionics and Biomechanics 3 Table 1: Patient characteristics. Surgery-HAL Number of HAL Rehabilitation Patient Age (years) Sex Diagnosis Lesion level interval (days) sessions period (days) 1 48 Male Arachnoid cyst C5–Th1 7 3 7 2 65 Male Dural AVF Th6-7 13 12 35 3 56 Male Dural AVF Th6-7 10 3 4 4 70 Male Cervical OPLL C2–Th1 14 5 9 5 67 Male Spinal lipoma L2–521 5 7 6 72 Male Cervical spondylosis C4–511 5 10 7 29 Female Spinal ependymoma C6 29 4 18 8 36 Female Spinal ependymoma C2-3 14 3 21 9 39 Female Spinal ependymoma Medulla oblongata to Th1 19 5 11 Mean ± SD 53.6 ± 16.1 14.2 ± 8.1 5.0 ± 2.6 13.6 ± 9.1 AVF = arteriovenous fistula; OPLL = ossification of the posterior longitudinal ligament; SD = standard deviation. (a) (b) Figure 2: (a, b) Hybrid Assistive Limb (HAL) treatment. Gait training on a treadmill in front of a large monitor. risk of falling. The GARS-M considered the following seven The WISCI II score also improved from 19.7 ± 0.5 to items: (1) variability, (2) guardedness, (3) staggering, (4) foot 20.0 ± 0.0 (P =0 081). These scores are summarized in contact, (5) hip range of motion (ROM), (6) shoulder exten- Figure 3. There were no adverse events due to HAL treatment sion, and (7) arm–heel strike synchrony. Each item of the such as pain and/or falling. GARS-M is rated from 0 to 3, with a maximum of 21 points; It is noteworthy that almost all subjects had improved a score of 21 points indicates the worst state. We measured gait posture. After reviewing each item before and after the maximum angle of the trunk swing during the 10MWT HAL treatment, it became clear that the subscores of before and after treatment using the Total Motion Coordi- guardedness (item 2), staggering (item 3), and shoulder nate System version 3.28 (Toso System Inc., Tokyo, Japan) extension (item 6) showed the most dramatic improve- motion analysis device. ments. Momentum and the ability to move the legs for- ward were improved. Collapse of balance toward the side 2.4. Statistical Analysis. We performed a paired t-test to was decreased. The movement range of the shoulder toward compare the clinical outcomes and baseline. We used SPSS the backside was expanded. version 21.0 (IBM Corp., Armonk, NY, USA) for the analy- ses. The mean ± SD values are described. 3.1. Representative Case (Case 2). A 65-year-old man was diagnosed with dural AVF at the level of Th6-7 3. Results and underwent laminectomy for ligation of the draining After HAL treatment, the speed during the 10MWT sig- vein. Preoperatively, he had urinary continence and was nificantly improved from 64.1 ± 16.0 to 74.8 ± 10.8 m/min wheelchair-bound. A few days after surgery, conventional (P =0 031), and the cadence decreased from 102.7 ± 17.6 to physical therapy was started and his walking ability gradually 92.7 ± 10.9 steps/min (P =0 046). The BI score also improved improved so that he could walk with an aid on postoperative day 9. However, his gait posture had involved sweeping out from 83.3 ± 16.0 to 95.6 ± 5.8 (P =0 043). Furthermore, the total GARS-M score improved from 6.0 ± 5.7 to 2.3 ± 3.3 his lower limbs at the cost of laterally bending the trunk to (P =0 005). The maximum angles of the trunk swing were the opposite side (Figure 4). He also had difficulty in kicking improved from 2.2 ± 1.9 to 1.2 ± 0.9 degrees (P =0 033). the ground with the toes. 4 Applied Bionics and Biomechanics p = 0.043 p = 0.081 p = 0.005 p = 0.046 140 20 100 100 16 p = 0.033 p = 0.031 120 95 12 70 100 90 8 19 80 85 4 40 60 80 0 0 18 Pre Post Pre Post Pre Post Pre Post Pre Post Pre Post 10 MWT 10 MWT Barthel index GARS-M Trunk swing WISCI II (m/min) (steps/min) (ADL) (gait form) angle (º) Figure 3: Graph showing functional outcomes evaluated by the 10-m walking test (10MWT): speed (m/min), cadence (steps/min), the Barthel Index, modified Gait Abnormality Rating Scale (GARS-M), trunk swing angle before and after Hybrid Assistive Limb (HAL) treatment, and the walking index for spinal cord injury II (WISCI II) score. Whiskers represent the standard deviation. Pre: before treatment; Post: after treatment. Pre Post We started using HAL on postoperative day 13. At this point, his WISCI II score was 19. At first, he performed knee 1.4º extension movements and standing training. Next, he 4.6º started balance training and gait training with a walking device (All-In-One Walking Trainer; Ropox A/S). Later, walking training on a treadmill was initiated. Before HAL treatment, his trunk was bending forward and he required walking support. After 12 sessions of HAL treatment, the trunk lifted while walking and posture improved. He could constantly set the position of his foot and the step width. He became able to kick the ground on tip- toes and swing out his lower limbs without side bending of the trunk. The angle of his trunk swing during 10MWT decreased from 4.6 to 1.4 degrees (Figure 4). His 10MWT speed improved from 43.4 to 65.7 m/min, and the walking cadence decreased from 132 to 96 steps/min. The total Figure 4: Representative case showing improvements in walking appearance. Prior to Hybrid Assistive Limb (HAL) treatment, the GARS-M score improved from 16 to 10. Similarly, the BI trunk leaned toward the left when standing with the left leg. and WISCI II score improved from 55 to 100 and from 19 Furthermore, the trunk was leaned 4.6 to the left. After 12 to 20, respectively. sessions of HAL treatment, the upper body was stabilized. Pre: before training; Post: after training. 4. Discussion The HAL was invented based on the iBF theory [1, 2] that level of the central pattern generator (CPG) results in a movements of the affected limbs supported by the HAL loss of supraspinal drive and spasticity. The consequences are hyperexcitability of short-latency reflexes, loss of long- system generate sensory feedback to the brain (i.e., iBF) and accelerate motor learning in the process of functional latency reflexes, and changes in muscle properties [25]. recovery. HAL therapy may address spasticity due to central According to the iBF theory, sensory input is sent back nervous system (CNS) lesions. A CNS lesion above the to the CNS to activate the impaired neuronal networks Applied Bionics and Biomechanics 5 Table 2: Review of reports of several postoperative spinal diseases. Sample size, Age (years) Follow-up Rehabilitation Long-term results after Diagnosis Author, year Outcome measures Presenting symptoms n (sex) (mean) (mean) program surgical treatment Pain: 13 cases 21 patients had complete Lower extremity weakness: remission of symptoms Categorized as 12 cases 13 days to 6 patients had symptom Arachnoid Bond et al., 31 complete remission, Gait instability: 10 cases 1–17 (8.1) 12.6 years N/A improvement cyst 2012 [31] (M 14; F 17) improvement, stable, Spasticity: 6 cases (4.4 years) 3 patients were stable or worse Sensory loss: 3 cases 1 patient had worsened Bladder dysfunction: 2 symptoms cases Flaccid: 9 patients Improved: 67%; unchanged: Muscle strength N/A Spastic: 12 patients 19%; deteriorated: 14% Improved: 57%; unchanged: Walking distance Wheelchair: 7 patients N/A 29%; deteriorated: 14% Behrens and 5 months to 21 33–75 Thron, 1999 11 years Sensory disturbance: Improved: 38%; unchanged: (M 18; F 3) (57.0) Sensory loss N/A [30] (50 months) 18 patients 62% Dural AVF Improved: 5%; unchanged: Pain No patient N/A 71%; deteriorated: 24% BI (score) 70.5 ± 20.43 (range 20–95) N/A 85.75 ± 13.81 (range 50–100) Van Dijk 12 days to The median gait score was 3 49 Aminoff score of The median gait score was 2 et al., 2002 28–78 (63) 9.9 years The median bladder score N/A disability (M 39; F 10) The median gait score was 2 [32] (32.9 months) was 3 Improvement: 2 grades in Grade a: no patient 16 patients Okamoto’s classification Onari et al., 30 34–61 10–23 years Grade b: 9 patients Improvement: 1 grade in for the degree of walking N/A 2001 [33] (M 22; F 8) (51.3) (14.7 years) Grade c: 18 patients 8 patients ∗∗ disability Grade d: 3 patients Ambulatory deterioration in 6 patients Cervical OPLL The mean preoperative The mean last follow-up total total JOA score was 8.9 JOA score was 13.8 Iwasaki JOA scoring system for 64 10–16 years UE motor score: 2.5 ± 1.0 UE motor score: 3.5 ± 0.8 et al., 2002 42–78 (56) N/A ∗∗∗ cervical myelopathy (M 43; F 21) (12.2 years) LE motor score: 2.2 ± 0.9 LE motor score: 2.9 ± 1.1 [34] Sensory score: 2.2 ± 1.7 Sensory score: 4.6 ± 1.4 Bladder score: 2.2 ± 0.8 Bladder score: 2.7 ± 0.5 Grade I: no patient Grade І: 1 patient 12–96 Clinical and functional Spinal Lee et al., 6 Grade II: 3 patients Grade II: 2 patients 8–45 (27) months N/A ∗∗∗∗ classification scheme lipoma 1995 [35] (M 3; F 3) Grade III: 3 patients Grade III: 2 patients (53.8 months) Grade IV: no patient Grade IV: 1 patient 6 Applied Bionics and Biomechanics Table 2: Continued. Sample size, Age (years) Follow-up Rehabilitation Long-term results after Diagnosis Author, year Outcome measures Presenting symptoms n (sex) (mean) (mean) program surgical treatment Score 0: 6 patients Score 0: 64 patients Score 1: 72 patients Score 1: 56 patients Nurick score for Wang et al., 204 Score 2: 71 patients Score 2: 31 patients 36–92 (63) 16 months N/A ∗∗∗∗∗ 2004 [36] (M 145; F 59) myelopathy Score 3: 28 patients Score 3: 10 patients Score 4: 24 patients Score 4: 19 patients Score 5: 8 patients Score 5: 19 patients Singh et al., 50 56.7 ± 13.7 3 years 30-m walking test (sec) 53.6 ± 10.3 N/A 38.6 ± 6.9 2009 [37] (M 36; F 14) Cervical 64 12 years 10-m walking test (sec) N/A (M, 46; F, 18) spondylosis Without Without surgery: ∗∗∗∗∗∗ surgery: 7.0 (5.3; 10.7) Kadaňka 12 years 10-m walking test (sec) N/A 7.1 (5.1; 12.5) 47–65 n =32 et al., 2011 (54.5) [38] With With surgery: surgery: 12 years 10-m walking test (sec) 8.0 (5.0; 29.8) N/A 7.3 (5.1; 25.7) 41–65 n =32 (51.0) Grade I: 18 patients Grade I: 15 patients Modified McCormick Li et al., 38 11–60 Grade II: 11 patients Grade II: 14 patients 1 year N/A ∗∗∗∗∗∗∗ 2013 [39] (M 19; F 19) (35.3) classification Grade III: 9 patients Grade III: 7 patients Grade IV: 0 patient Grade IV: 2 patients Spinal They performed ependymoma Grade I: 11 patients rehabilitation from Grade I: 20 patients 12–168 Kaner et al., 21 Modified McCormick Grade II: 5 patients an early postoperative Grade II: 1 patient 17–57 (34) months 2010 [40] (M, 13; F, 8) classification Grade III: 3 patients day, but the content Grade III: 0 patient (54 months) Grade IV: 2 patients and method were Grade IV: 0 patient not described at all M = male; F = female; N/A = not available; AVF = arteriovenous fistula; BI = Barthel Index; OPLL = ossification of the posterior longitudinal ligament; JOA = Japanese Orthopaedic Association; UE = upper extremity; LE = lower extremity; the mean ± the standard deviation. Aminoff score of disability (classification of gait disturbance: grade 1: leg weakness or abnormal gait and no restricted activity; grade 2: grade 1 with restricted activity; grade 3: requiring 1 stick or similar support for walking; grade 4: requiring 2 sticks or crutches for walking; and grade 5: unable to stand and confined to bed or wheelchair. ∗∗ Classification of micturition: grade 1: hesitance, urgency, or frequency; grade 2: occasional urinary incontinence or retention; and grade 3: total urinary incontinence or retention). Okamoto’s classification for the degree of walking disability (a: impossible to walk; b: walk with aids; c: independent walk with spasm; d: walk with difficulty, with or without spasm; e: walk easily but difficult to walk continuously; and ∗∗∗ f: normal or almost normal walking). JOA scoring system for cervical myelopathy (motor function of fingers, shoulder and elbow, and lower extremity; sensory function of upper extremity, trunk, and lower ∗∗∗∗ extremity; and bladder function. Total score for a healthy patient = 17. Normal score of UE motor: 4, LE motor: 4, sensory: 6, and bladder: 3). Clinical and functional classification scheme (grade I: ∗∗∗∗∗ neurologically normal, grade II: sensorimotor deficit affecting the function of the involved limb, grade III: more severe neurological deficit, and grade IV: severe deficit). Nurick score for myelopathy (0: root involvement but no evidence of spinal cord disease; 1: spinal cord disease but no difficulty in walking; 2: slight difficulty in walking, but still employable; 3: difficulty in walking preventing full-time work ∗∗∗∗∗∗ ∗∗∗∗∗∗∗ or housework but independent ambulation; 4: able to walk with assistance or a walker; and 5: chair-bound or bedridden). Median (5th–95th percentile range). Modified McCormick classification (grade I: neurologically normal, normal ambulation and professional activity, and minimal dysesthesia; grade II: mild motor and sensory deficit, independent function, and ambulation maintained; grade III: moderate sensorimotor deficit, restriction of function, and independent with an external aid; grade IV: severe sensorimotor deficit, restricted function, and dependent; and grade V: paraplegia and quadriplegia and even/flickering movement). Applied Bionics and Biomechanics 7 Table 3: Review of HAL treatment for spinal disease. Age Number 10MWT 10MWT Author, Time when BI WISCI II (years), Diagnosis of HAL Speed (m/min) Cadence (steps/min) year starting HAL sex sessions Pre Post Pre Post Pre Post Pre Post 2-3 53.6 POD 14.2 times/ 19.7 20.0 Our result ± 16.1, M Table 1 64.1 ± 16.0 74.8 ± 10.8 102.7 ± 17.6 92.7 ± 10.9 83.3 ± 16.0 95.6 ± 5.8 (7–29 days) week, ± 0.5 ± 0.0 6; F 3 5.0 ± 2.6 T2–8 Sakakima POD 49 OPLL, 6 times/ et al., 2013 60, F (after bed rest) N/A N/A N/A N/A N/A N/A 0 8 T9–10 week, 48 [18] to 15 weeks OLF Kubota T8–11, 2-3 Approximately Approximately Approximately Approximately et al., 2016 43, M L1–3 POD 14–44 times/ 60 85 13 16 ∗ ∗ ∗ ∗ 20 50 42 85 [19] OPLL week, 10 POD 44 2-3 Fujii et al., T3–7 63, F (after bed rest) times/ 15.9 31.8 43.8 77.9 N/A N/A 8 16 2017 [20] OPLL to POD 73 week, 10 Kubota Once/2 C5-6 14 years after et al., 2017 66, F weeks, 22.5 46.7 61.9 81.6 N/A N/A 16 16 OPLL surgery [21] 10 Shimizu T12–L1 6 months after 2 times/ Approximately Approximately Approximately Approximately et al., 2017 48, M N/A N/A 7 12 ∗ ∗ ∗ ∗ 13 29 39 62 SDAVF surgery week, 10 [41] T9–12, Taketomi L2/3, L5 1 year after his 2 times/ et al., 2018 70, M 49.8 58.2 109.8 120 N/A N/A N/A N/A OLF, C3– third surgery week, 10 [22] 7 OPLL 59.6 ± 13.9, M POD 24.4 Approximately Approximately Approximately Approximately 2; F 3 N/A N/A N/A N/A ∗ ∗ ∗ ∗ 28 54 63 83 (15–32 days) (acute Puentes 2 times/ group) et al., 2018 OPLL week, 10 [26] 70.1 ± 6.9, Approximately Approximately Approximately Approximately M7 POD 1151.4 N/A N/A N/A N/A ∗ ∗ ∗ ∗ 48 56 100 100 (chronic (287–3655 days) group) 5 times/ 8.1 (1–19) years Aach et al., 48 ± 9.4, T8–L2 week, 0.28 ± 0.28 10 11.1 posttrauma—90 0.5 ± 0.34 N/A N/A N/A N/A 2014 [9] M6; F2 SCI 51.75 (m/sec) ± 4.3 ± 3.7 days ± 5.6 8 Applied Bionics and Biomechanics Table 3: Continued. Age Number 10MWT 10MWT Author, Time when BI WISCI II (years), Diagnosis of HAL Speed (m/min) Cadence (steps/min) year starting HAL sex sessions Pre Post Pre Post Pre Post Pre Post 10 years 52, M L3 SCI posttrauma—12 5 times/ Cruciger weeks week, 85.6 ± 56.9 et al., 2016 44.3 ± 34.6 N/A N/A N/A N/A N/A N/A mean (sec) 19 years [10] 54.5 40, F L1 SCI posttrauma—12 weeks 8.8 (0.7–17) Sczesny- 46.9 ± 2.7, T8–L2 years 5 times/ 0.25 ± 0.05 Kaiser et al, 0.5 ± 0.07 N/A N/A N/A N/A N/A N/A M7; F4 SCI postinjury—12 week, 60 (m/sec) 2015 [11] weeks 3-4 T12–L1 times/ 62, M 7 days post onset 21.6 39.6 62 99.5 35 60 5 18 SCI week, 7- Watanabe et al., 2017 3-4 [12] T8–10 14 days post times/ 61, F 21.6 60.7 52 97.3 60 80 4 13 SCI onset week, 7-8 Grasmücke 44.3 6.9 (1–22) years C2–L4 5 times/ 70.45 ± 61.5 9.35 11.04 et al., 2017 ± 13.9, M posttrauma—12 35.22 ± 30.8 N/A N/A N/A N/A SCI week, 60 (sec) ± 5.12 ± 4.52 [8] 43; F 12 weeks 5 times/ 8.1 (1–19) years 48 ± 9.4, T8–L2 week, 0.28 ± 0.10 10 11.13 posttrauma—12 0.5 ± 0.12 41.85 ± 9.45 56.7 ± 9.9 N/A N/A M6; F2 SCI 51.75 (m/sec) ± 1.5 ± 1.3 weeks ± 5.6 3–5 Jansen times/ No patient Subgroup T8–L2 Plus 40 weeks 28.61 ± 6.9 et al., 2017 week, 21.22 ± 6.6 49.71 ± 8.8 72.16 ± 6.9 N/A N/A improved or 1: n =4 SCI (at 52 weeks) (sec) [13] 126.8 worsened ± 7.9 Once/ No patient Subgroup T8–L2 Plus 40 weeks week, 34.28 ± 18.2 34.61 ± 17.3 63.65 ± 18.7 62 ± 18.8 N/A N/A improved or 2: n =4 SCI (at 52 weeks) 32.3 (sec) worsened ± 3.3 Jansen 44.8 6.5 (1–19) years 30.9 ± 8.71 C4–L3 5 times/ 61.17 ± 44.27 10.7 11.7 et al., 2018 ± 13.8, M posttrauma—12 32.18 ± 25.53 (number 20.7 ± 5.51 N/A N/A SCI week, 60 (sec) ± 4.95 ± 4.5 [14] 15; F 6 weeks of steps) M = male; F = female; 10MWT = 10-m walking test; BI = Barthel Index; WISCI II = the walking index for spinal cord injury; POD = postoperative day; Pre = before training; Post = after training; N/A = not available; OPLL = ossification of the posterior longitudinal ligament; OLF = ossification of ligamentum flavum; SDAVF = spinal dural arteriovenous fistula; SCI = spinal cord injury. Estimated from the presented figure in the paper. Applied Bionics and Biomechanics 9 indicated that long steps decreased the cadence. Although (biofeedback); in turn, the activated CNS enhances its descending signals [2]. Therefore, the spasticity could be natural recovery in the acute state following injury or surgical ameliorated by HAL therapy. Furthermore, a previous intervention has to be taken into account, it was thought that the functional recovery rate could be facilitated by study showed that HAL was effective for treating spastic hemiplegia due to stroke [16], and two studies have shown HAL treatment from an early stage [18–20, 26]. that HAL treatment for stroke patients facilitated cortical Even though our study showed a significant improve- activities in the damaged brain [16, 17]. ment with HAL treatment, it had several limitations. We In this study, significant improvements were seen in investigated a relatively small number of patients with het- erogeneous characteristics. Our patients underwent HAL gait ability following robotic rehabilitation. The results showed improvements in a series of clinical scales such as treatment during the early postoperative state, but our 10MWT, BI, GARS-M, and WISCI II. All participants cohort did not have a control group. Therefore, it is possi- showed improvements in gait ability that were similar to ble that spontaneous recovery following surgery may have those of previous reports concerning the use of HAL for contributed to the postoperative course. However, it should also be noted that our patients experienced earlier recov- spine disorders such as SCI [8–14], SDAVF [41], and OPLL [18–22, 26]. It is noteworthy that participants in our study ery than those described in previous reports [18–20, 26] underwent surgery for various reasons such as spinal cord because our patients started HAL therapy during relatively tumor, vascular disease, and bone degenerative disease. Addi- early postoperative periods. tionally, clinical manifestations of vascular disease and tumors in the spine are similar [27, 28], and rehabilitation 5. Conclusions outcomes following vascular-related and traumatic SCI were reportedly not significantly different [29]. These facts may We showed the feasibility and safety of HAL treatment and determined that it could potentially facilitate functional indicate that HAL therapy may be applied for a variety of disorders with spinal cord origins. recovery, even for postoperative patients. Further studies involving more patients and a control group are warranted This study also showed the usefulness of HAL for postop- to verify our findings. erative rehabilitation. There have been only five case reports of HAL-assisted rehabilitation for a patient who underwent surgery for thoracic OPLL [18–22]. It is advantageous that Data Availability HAL does not interfere with the skin incision and can be used The data used to support the findings of this study are avail- for patients with a corset. In our experience, HAL was con- able from the corresponding author upon request. sidered to facilitate early recovery after spine surgery. In this study, HAL treatment was performed for patients with rare spinal diseases. In previous studies, the diagnosis Conflicts of Interest and surgical management were emphasized rather than the The authors declare that they have no conflicts of interest. rehabilitation programs, even though it has been consid- ered that improvement after surgery depends on the length of time and initiation of neurological rehabilitation Acknowledgments [30]. However, outcome measures have not been standard- This study was partly supported by the Japan Society for ized. Previous reports showing the clinical outcomes of the Promotion of Science grant-in-aid for young scientists treatment for the same spine disorders are summarized ((B) 15 K19984); Takeda Science Foundation, Uehara in Table 2 [30–40]. Memorial Foundation; and Central Research Institute, We also reviewed clinical studies of gait training using Fukuoka University (Grant no. 161042). The authors appre- HAL for spine disorders. A systematic search of the liter- ciate the help of Ms. Asuka Ikezaki, who assisted with the ature was conducted using the PubMed database. Search statistical analysis. terms were “HAL” OR “Hybrid Assistive Limb” AND “Spinal Cord Injury” OR “OPLL.” We searched Google Scholar, and only one work [19] was included from that References search. Studies only reporting HAL for gait training were [1] K. Suzuki, G. Mito, H. Kawamoto, Y. Hasegawa, and Y. Sankai, included. Of 20 literatures, six were excluded due to the “Intention-based walking support for paraplegia patients with difference in the type of HAL robot. Overall, 14 studies robot suit HAL,” Advanced Robotics, vol. 21, no. 12, pp. 1441– met the inclusion criteria and were subject to critical review 1469, 2007. (Table 3) [8–14, 18–22, 26, 41]. [2] T. Morishita and T. Inoue, “Interactive bio-feedback therapy Results of the systematic review revealed that HAL treat- using hybrid assistive limbs for motor recovery after stroke: ment was performed mainly for spinal cord injury and current practice and future perspectives,” Neurologia Medico- degenerative disease at various stages of disorders. Overall, Chirurgica, vol. 56, no. 10, pp. 605–612, 2016. these previous reports [12, 13, 19–22, 41] showed that both [3] H. Kawamoto, S. Taal, H. Niniss et al., “Voluntary motion sup- the speed and cadence were increased compared with our port control of robot suit HAL triggered by bioelectrical signal results. We considered the difference in the change in for hemiplegia,” in 2010 Annual International Conference of the gait speed. Previous reports [12, 13, 19–22, 41] indicated the IEEE Engineering in Medicine and Biology, pp. 462–466, that more steps increased the cadence, whereas our results Buenos Aires, Argentina, 2010. 10 Applied Bionics and Biomechanics concept study using functional near infrared spectroscopy,” [4] T. Ueba, O. Hamada, T. Ogata, T. Inoue, E. Shiota, and Y. Sankai, “Feasibility and safety of acute phase rehabilitation PLoS One, vol. 13, no. 1, article e0191361, 2018. after stroke using the Hybrid Assistive Limb robot suit,” Neu- [18] H. Sakakima, K. Ijiri, F. 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Kawamoto et al., “Intensive coordination by robotic intervention in myelopathy patients after surgery,” Frontiers in Neuroscience, vol. 12, p. 99, 2018. gait treatment using a robot suit Hybrid Assistive Limb in acute spinal cord infarction: report of two cases,” The Journal [27] K. Jellema, C. C. Tijssen, and J. van Gijn, “Spinal dural arterio- of Spinal Cord Medicine, pp. 1–7, 2017. venous fistulas: a congestive myelopathy that initially mimics a peripheral nerve disorder,” Brain, vol. 129, no. 12, pp. 3150– [13] O. Jansen, T. A. Schildhauer, R. C. Meindl et al., “Functional 3164, 2006. outcome of neurologic-controlled HAL-exoskeletal neuroreh- abilitation in chronic spinal cord injury: a pilot with one year [28] F. J. Rodriguez, B. A. Crum, W. E. Krauss, B. W. Scheithauer, treatment and variable treatment frequency,” Global Spine and C. 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Feasibility of Neurorehabilitation Using a Hybrid Assistive Limb for Patients Who Underwent Spine Surgery

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Copyright © 2018 Aya Yatsugi et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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Hindawi Applied Bionics and Biomechanics Volume 2018, Article ID 7435746, 11 pages https://doi.org/10.1155/2018/7435746 Research Article Feasibility of Neurorehabilitation Using a Hybrid Assistive Limb for Patients Who Underwent Spine Surgery 1,2 1 1,2 2 1 Aya Yatsugi, Takashi Morishita , Hiroyuki Fukuda, Naoya Kotani, Kenji Yagi, 1 2 1 Hiroshi Abe, Etsuji Shiota, and Tooru Inoue Department of Neurological Surgery, Fukuoka University Faculty of Medicine, Fukuoka, Japan Department of Rehabilitation Medicine, Fukuoka University Hospital, Fukuoka, Japan Correspondence should be addressed to Takashi Morishita; tmorishita@fukuoka-u.ac.jp Received 17 February 2018; Revised 21 May 2018; Accepted 19 June 2018; Published 10 July 2018 Academic Editor: Liwei Shi Copyright © 2018 Aya Yatsugi et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Recent studies of robotic rehabilitation have demonstrated its efficacy for neurological disorders. However, few studies have used the Hybrid Assistive Limb (HAL) during the early postoperative stage of spine disorders. We aimed to evaluate the safety and efficacy of HAL treatment during the early postoperative period for spine disorder patients. We retrospectively identified patients who underwent spine surgery and who could complete HAL treatment. We evaluated the 10-m walking test (10MWT), the modified Gait Abnormality Rating Scale (GARS-M), Barthel Index (BI), and the walking index for spinal cord injury II (WISCI II) score results before and after robotic rehabilitation. Clinical outcomes were compared after treatment. We included nine patients with various spine problems. After HAL treatment, the speed during the 10MWT significantly improved from 64.1 ± 16.0 to 74.8 ± 10.8 m/min, and the walking cadence decreased from 102.7 ± 17.6 to 92.7 ± 10.9 steps/min. The BI score also improved from 83.3 ± 16.0 to 95.6 ± 5.8, and the WISCI II score improved from 19.7 ± 0.5 to 20.0 ± 0.0. Furthermore, the total GARS-M score improved from 6.0 ± 5.7 to 2.3 ± 3.3. The maximum angles of the trunk swing were improved from 2.2 ± 1.9 to 1.2 ± 0.9 degrees. Neurorehabilitation therapy using HAL for spinal surgery patients was considered feasible following spine surgery. 1. Introduction generate sensory feedback to the brain (i.e., iBF) and acceler- ate motor learning in the process of functional recovery. Recent studies have shown the safety and efficacy of reha- Robotic technologies have been increasingly gaining atten- bilitation using HAL robotics for various disorders, including tion in the field of neurorehabilitation. The Hybrid Assistive stroke [3–7], spinal cord injury (SCI) [8–14], and quadriceps Limb (HAL) (Cyberdyne Inc., Ibaraki, Japan) is a unique arthrogenic muscle inhibition [15]. Another recent study exoskeleton robot for neurorehabilitation that was developed by Sankai and colleagues based on the interactive biofeed- demonstrated neuroplasticity induced by HAL treatment [16, 17]. However, five case reports have focused on the effi- back (iBF) theory [1, 2]. HAL has a hybrid system that allows cacy of HAL therapy for postoperative thoracic ossification of both voluntary and autonomous modes of action to support the posterior longitudinal ligament (OPLL) [18–22]. These training, and it supports voluntary muscle movement by reports indicated that HAL was used as a last resort for gait detecting bioelectrical signals (BES). For walking training, movements of the joints are accurately adjusted by the pres- recovery during the almost chronic phase of the postopera- tive state [21, 22], and the authors recommended starting sure sensor in the foot bottom and joint angle sensors of the HAL-assisted training during the early stage following sur- frame. Based on the input information, four actuators of the gery. Neurorehabilitation during the postoperative state is hip and knee joint are controlled independently [3]. Move- essential for returning to social activities and preventing ments of the affected limbs supported by the HAL system 2 Applied Bionics and Biomechanics disuse syndrome. Based on the findings indicated by these All spine disorders five case reports [18–22], in addition to the reports demon- treated with HAL N = 31 strating the efficacy of HAL training for SCI cases [8–14], we hypothesized that using HAL may facilitate early recovery Nonoperative cases after spine surgery. Therefore, we aimed to evaluate the safety (N = 13) and efficacy of HAL-assisted rehabilitation for spine disorder Surgical cases patients during the early postoperative period. N = 18 Severely impaired patients who were 2. Materials and Methods unable to use HAL (N = 5) <3 sessions of HAL treatment (N = 4) 2.1. Patient Selection and Study Design. We performed a ret- rospective chart review of patients with spine disorders treated at our neurosurgical department from October 2011 Total participants to February 2016. To evaluate the effects of HAL treatment N = 9 for improvements in gait, we included patients who could Figure 1: Patient selection flowchart. complete HAL treatment at least three times. Additionally, because voluntary muscle contractions are required to gain assistance from the HAL system, we excluded patients with performed by one or two physiotherapists and a medical doc- tor who were trained to use the HAL system. During gait complete or nearly complete paralysis. The protocol of the present study was approved by our institutional review board training, the physiotherapist checked the BES and adjusted the HAL assist level. (IRB), and HAL treatment was performed after receiving written informed consent from each patient. During HAL treatment, several sets of a knee extension HAL treatment was performed for 31 patients with spine movement were performed (10 times with the left leg and 10 times with the right leg). The standing movement was per- disorders; however, 22 patients did not meet the inclusion criteria of the current study (Figure 1). Among those 22 formed 10 times. Balance training was performed for several seconds with open eyes or closed eyes so that the center of patients, 13 did not undergo surgery. We investigated the remaining nine patients (six male gravity would be in the middle. Finally, walking training patients and three female patients) with the following charac- was performed on a flat ground or a treadmill. During bal- ance training and gait training, we used a monitor displayed teristics: severe impairment resulting in the inability to use HAL (n =5) and less than three sessions of HAL treat- in front of the patient to provide visual feedback regarding the center of gravity, posture, and balance (Figure 2). ment (n =4). The mean age of the cohort was 53.6 years (SD, ±16.1). Diagnoses were dural arteriovenous fistula We focused on walking training. We used a walk aid (AVF) (n =2), cervical ossification of the posterior longitudi- called All-In-One Walking Trainer (Ropox A/S, Naestved, Denmark) to secure the safety of patients when walking on nal ligament (OPLL) (n =1), spinal lipoma (n =1), arachnoid cyst (n =1), spinal ependymoma (n =3), and cervical spon- a flat floor. It is able to support body weight and enables safe HAL treatment with the use of a harness. We did not use dylosis (n =1). Spine lesion levels are summarized in Table 1. body weight support. After the patient became accustomed 2.2. Rehabilitation Program. We performed conventional to walking on the ground, we began treadmill walking. Patients performed several sets of 5 minutes of walking at a physical therapy in addition to HAL treatment. Conventional physical therapy started within 2 days after surgery. Depend- speed that was comfortable with HAL. If patients wanted to ing on the patient’s condition, the programs included manual continue and were not fatigued, then we increased the speed leg stretching, muscular workouts, and basic movement or increased the walking time. When there was deflection of training such as standing, walking, and going up and down the center of gravity (it does not take weight to walk on tip- toes), we instructed the patient to move the weight from stairs. When patients felt fatigue during the HAL treatment, they were allowed to rest. Each session lasted approximately the heel to the tiptoes. 50 minutes, including time necessary for robotic attachment, and was performed two or three times per week. 2.3. Outcome Measures. All patients were video-recorded HAL treatment started when the patients were able to sit during rehabilitation. The speed and steps during the 10-m stably. On average, intervention with therapists and HAL walking test (10MWT) as an evaluation of motor function treatment began 14.2 ± 8.1 days (range 7–29 days) after at the time of treatment immediately before wearing HAL surgery. The mean number of HAL treatment sessions was and during the last training session after excluding HAL were 5.0 ± 2.6 (range 3–12). Rehabilitation periods comprised used to evaluate HAL treatment times. We used the modified 13.6 ± 9.1 days (range 4–35 days) during hospitalization at Gait Abnormality Rating Scale (GARS-M) [23], the Barthel our institution (Table 1). Index (BI), and the walking index for spinal cord injury II A bilateral leg version of HAL was used for patients (WISCI II) to evaluate walking appearance, activities of daily involved in this study (HAL for Living Support–Lower Limb; living (ADL), and the patients’ ambulatory walking capacity Cyberdyne Inc.). Training started with the Cybernic Volun- on the basis of the need for physical assistance and assistive tary Control mode, which measures BES from the extensor devices, respectively [24]. The GARS-M includes variables and flexor muscles of the hip and knee. HAL treatment was that provide a description of gait associated with an increased Applied Bionics and Biomechanics 3 Table 1: Patient characteristics. Surgery-HAL Number of HAL Rehabilitation Patient Age (years) Sex Diagnosis Lesion level interval (days) sessions period (days) 1 48 Male Arachnoid cyst C5–Th1 7 3 7 2 65 Male Dural AVF Th6-7 13 12 35 3 56 Male Dural AVF Th6-7 10 3 4 4 70 Male Cervical OPLL C2–Th1 14 5 9 5 67 Male Spinal lipoma L2–521 5 7 6 72 Male Cervical spondylosis C4–511 5 10 7 29 Female Spinal ependymoma C6 29 4 18 8 36 Female Spinal ependymoma C2-3 14 3 21 9 39 Female Spinal ependymoma Medulla oblongata to Th1 19 5 11 Mean ± SD 53.6 ± 16.1 14.2 ± 8.1 5.0 ± 2.6 13.6 ± 9.1 AVF = arteriovenous fistula; OPLL = ossification of the posterior longitudinal ligament; SD = standard deviation. (a) (b) Figure 2: (a, b) Hybrid Assistive Limb (HAL) treatment. Gait training on a treadmill in front of a large monitor. risk of falling. The GARS-M considered the following seven The WISCI II score also improved from 19.7 ± 0.5 to items: (1) variability, (2) guardedness, (3) staggering, (4) foot 20.0 ± 0.0 (P =0 081). These scores are summarized in contact, (5) hip range of motion (ROM), (6) shoulder exten- Figure 3. There were no adverse events due to HAL treatment sion, and (7) arm–heel strike synchrony. Each item of the such as pain and/or falling. GARS-M is rated from 0 to 3, with a maximum of 21 points; It is noteworthy that almost all subjects had improved a score of 21 points indicates the worst state. We measured gait posture. After reviewing each item before and after the maximum angle of the trunk swing during the 10MWT HAL treatment, it became clear that the subscores of before and after treatment using the Total Motion Coordi- guardedness (item 2), staggering (item 3), and shoulder nate System version 3.28 (Toso System Inc., Tokyo, Japan) extension (item 6) showed the most dramatic improve- motion analysis device. ments. Momentum and the ability to move the legs for- ward were improved. Collapse of balance toward the side 2.4. Statistical Analysis. We performed a paired t-test to was decreased. The movement range of the shoulder toward compare the clinical outcomes and baseline. We used SPSS the backside was expanded. version 21.0 (IBM Corp., Armonk, NY, USA) for the analy- ses. The mean ± SD values are described. 3.1. Representative Case (Case 2). A 65-year-old man was diagnosed with dural AVF at the level of Th6-7 3. Results and underwent laminectomy for ligation of the draining After HAL treatment, the speed during the 10MWT sig- vein. Preoperatively, he had urinary continence and was nificantly improved from 64.1 ± 16.0 to 74.8 ± 10.8 m/min wheelchair-bound. A few days after surgery, conventional (P =0 031), and the cadence decreased from 102.7 ± 17.6 to physical therapy was started and his walking ability gradually 92.7 ± 10.9 steps/min (P =0 046). The BI score also improved improved so that he could walk with an aid on postoperative day 9. However, his gait posture had involved sweeping out from 83.3 ± 16.0 to 95.6 ± 5.8 (P =0 043). Furthermore, the total GARS-M score improved from 6.0 ± 5.7 to 2.3 ± 3.3 his lower limbs at the cost of laterally bending the trunk to (P =0 005). The maximum angles of the trunk swing were the opposite side (Figure 4). He also had difficulty in kicking improved from 2.2 ± 1.9 to 1.2 ± 0.9 degrees (P =0 033). the ground with the toes. 4 Applied Bionics and Biomechanics p = 0.043 p = 0.081 p = 0.005 p = 0.046 140 20 100 100 16 p = 0.033 p = 0.031 120 95 12 70 100 90 8 19 80 85 4 40 60 80 0 0 18 Pre Post Pre Post Pre Post Pre Post Pre Post Pre Post 10 MWT 10 MWT Barthel index GARS-M Trunk swing WISCI II (m/min) (steps/min) (ADL) (gait form) angle (º) Figure 3: Graph showing functional outcomes evaluated by the 10-m walking test (10MWT): speed (m/min), cadence (steps/min), the Barthel Index, modified Gait Abnormality Rating Scale (GARS-M), trunk swing angle before and after Hybrid Assistive Limb (HAL) treatment, and the walking index for spinal cord injury II (WISCI II) score. Whiskers represent the standard deviation. Pre: before treatment; Post: after treatment. Pre Post We started using HAL on postoperative day 13. At this point, his WISCI II score was 19. At first, he performed knee 1.4º extension movements and standing training. Next, he 4.6º started balance training and gait training with a walking device (All-In-One Walking Trainer; Ropox A/S). Later, walking training on a treadmill was initiated. Before HAL treatment, his trunk was bending forward and he required walking support. After 12 sessions of HAL treatment, the trunk lifted while walking and posture improved. He could constantly set the position of his foot and the step width. He became able to kick the ground on tip- toes and swing out his lower limbs without side bending of the trunk. The angle of his trunk swing during 10MWT decreased from 4.6 to 1.4 degrees (Figure 4). His 10MWT speed improved from 43.4 to 65.7 m/min, and the walking cadence decreased from 132 to 96 steps/min. The total Figure 4: Representative case showing improvements in walking appearance. Prior to Hybrid Assistive Limb (HAL) treatment, the GARS-M score improved from 16 to 10. Similarly, the BI trunk leaned toward the left when standing with the left leg. and WISCI II score improved from 55 to 100 and from 19 Furthermore, the trunk was leaned 4.6 to the left. After 12 to 20, respectively. sessions of HAL treatment, the upper body was stabilized. Pre: before training; Post: after training. 4. Discussion The HAL was invented based on the iBF theory [1, 2] that level of the central pattern generator (CPG) results in a movements of the affected limbs supported by the HAL loss of supraspinal drive and spasticity. The consequences are hyperexcitability of short-latency reflexes, loss of long- system generate sensory feedback to the brain (i.e., iBF) and accelerate motor learning in the process of functional latency reflexes, and changes in muscle properties [25]. recovery. HAL therapy may address spasticity due to central According to the iBF theory, sensory input is sent back nervous system (CNS) lesions. A CNS lesion above the to the CNS to activate the impaired neuronal networks Applied Bionics and Biomechanics 5 Table 2: Review of reports of several postoperative spinal diseases. Sample size, Age (years) Follow-up Rehabilitation Long-term results after Diagnosis Author, year Outcome measures Presenting symptoms n (sex) (mean) (mean) program surgical treatment Pain: 13 cases 21 patients had complete Lower extremity weakness: remission of symptoms Categorized as 12 cases 13 days to 6 patients had symptom Arachnoid Bond et al., 31 complete remission, Gait instability: 10 cases 1–17 (8.1) 12.6 years N/A improvement cyst 2012 [31] (M 14; F 17) improvement, stable, Spasticity: 6 cases (4.4 years) 3 patients were stable or worse Sensory loss: 3 cases 1 patient had worsened Bladder dysfunction: 2 symptoms cases Flaccid: 9 patients Improved: 67%; unchanged: Muscle strength N/A Spastic: 12 patients 19%; deteriorated: 14% Improved: 57%; unchanged: Walking distance Wheelchair: 7 patients N/A 29%; deteriorated: 14% Behrens and 5 months to 21 33–75 Thron, 1999 11 years Sensory disturbance: Improved: 38%; unchanged: (M 18; F 3) (57.0) Sensory loss N/A [30] (50 months) 18 patients 62% Dural AVF Improved: 5%; unchanged: Pain No patient N/A 71%; deteriorated: 24% BI (score) 70.5 ± 20.43 (range 20–95) N/A 85.75 ± 13.81 (range 50–100) Van Dijk 12 days to The median gait score was 3 49 Aminoff score of The median gait score was 2 et al., 2002 28–78 (63) 9.9 years The median bladder score N/A disability (M 39; F 10) The median gait score was 2 [32] (32.9 months) was 3 Improvement: 2 grades in Grade a: no patient 16 patients Okamoto’s classification Onari et al., 30 34–61 10–23 years Grade b: 9 patients Improvement: 1 grade in for the degree of walking N/A 2001 [33] (M 22; F 8) (51.3) (14.7 years) Grade c: 18 patients 8 patients ∗∗ disability Grade d: 3 patients Ambulatory deterioration in 6 patients Cervical OPLL The mean preoperative The mean last follow-up total total JOA score was 8.9 JOA score was 13.8 Iwasaki JOA scoring system for 64 10–16 years UE motor score: 2.5 ± 1.0 UE motor score: 3.5 ± 0.8 et al., 2002 42–78 (56) N/A ∗∗∗ cervical myelopathy (M 43; F 21) (12.2 years) LE motor score: 2.2 ± 0.9 LE motor score: 2.9 ± 1.1 [34] Sensory score: 2.2 ± 1.7 Sensory score: 4.6 ± 1.4 Bladder score: 2.2 ± 0.8 Bladder score: 2.7 ± 0.5 Grade I: no patient Grade І: 1 patient 12–96 Clinical and functional Spinal Lee et al., 6 Grade II: 3 patients Grade II: 2 patients 8–45 (27) months N/A ∗∗∗∗ classification scheme lipoma 1995 [35] (M 3; F 3) Grade III: 3 patients Grade III: 2 patients (53.8 months) Grade IV: no patient Grade IV: 1 patient 6 Applied Bionics and Biomechanics Table 2: Continued. Sample size, Age (years) Follow-up Rehabilitation Long-term results after Diagnosis Author, year Outcome measures Presenting symptoms n (sex) (mean) (mean) program surgical treatment Score 0: 6 patients Score 0: 64 patients Score 1: 72 patients Score 1: 56 patients Nurick score for Wang et al., 204 Score 2: 71 patients Score 2: 31 patients 36–92 (63) 16 months N/A ∗∗∗∗∗ 2004 [36] (M 145; F 59) myelopathy Score 3: 28 patients Score 3: 10 patients Score 4: 24 patients Score 4: 19 patients Score 5: 8 patients Score 5: 19 patients Singh et al., 50 56.7 ± 13.7 3 years 30-m walking test (sec) 53.6 ± 10.3 N/A 38.6 ± 6.9 2009 [37] (M 36; F 14) Cervical 64 12 years 10-m walking test (sec) N/A (M, 46; F, 18) spondylosis Without Without surgery: ∗∗∗∗∗∗ surgery: 7.0 (5.3; 10.7) Kadaňka 12 years 10-m walking test (sec) N/A 7.1 (5.1; 12.5) 47–65 n =32 et al., 2011 (54.5) [38] With With surgery: surgery: 12 years 10-m walking test (sec) 8.0 (5.0; 29.8) N/A 7.3 (5.1; 25.7) 41–65 n =32 (51.0) Grade I: 18 patients Grade I: 15 patients Modified McCormick Li et al., 38 11–60 Grade II: 11 patients Grade II: 14 patients 1 year N/A ∗∗∗∗∗∗∗ 2013 [39] (M 19; F 19) (35.3) classification Grade III: 9 patients Grade III: 7 patients Grade IV: 0 patient Grade IV: 2 patients Spinal They performed ependymoma Grade I: 11 patients rehabilitation from Grade I: 20 patients 12–168 Kaner et al., 21 Modified McCormick Grade II: 5 patients an early postoperative Grade II: 1 patient 17–57 (34) months 2010 [40] (M, 13; F, 8) classification Grade III: 3 patients day, but the content Grade III: 0 patient (54 months) Grade IV: 2 patients and method were Grade IV: 0 patient not described at all M = male; F = female; N/A = not available; AVF = arteriovenous fistula; BI = Barthel Index; OPLL = ossification of the posterior longitudinal ligament; JOA = Japanese Orthopaedic Association; UE = upper extremity; LE = lower extremity; the mean ± the standard deviation. Aminoff score of disability (classification of gait disturbance: grade 1: leg weakness or abnormal gait and no restricted activity; grade 2: grade 1 with restricted activity; grade 3: requiring 1 stick or similar support for walking; grade 4: requiring 2 sticks or crutches for walking; and grade 5: unable to stand and confined to bed or wheelchair. ∗∗ Classification of micturition: grade 1: hesitance, urgency, or frequency; grade 2: occasional urinary incontinence or retention; and grade 3: total urinary incontinence or retention). Okamoto’s classification for the degree of walking disability (a: impossible to walk; b: walk with aids; c: independent walk with spasm; d: walk with difficulty, with or without spasm; e: walk easily but difficult to walk continuously; and ∗∗∗ f: normal or almost normal walking). JOA scoring system for cervical myelopathy (motor function of fingers, shoulder and elbow, and lower extremity; sensory function of upper extremity, trunk, and lower ∗∗∗∗ extremity; and bladder function. Total score for a healthy patient = 17. Normal score of UE motor: 4, LE motor: 4, sensory: 6, and bladder: 3). Clinical and functional classification scheme (grade I: ∗∗∗∗∗ neurologically normal, grade II: sensorimotor deficit affecting the function of the involved limb, grade III: more severe neurological deficit, and grade IV: severe deficit). Nurick score for myelopathy (0: root involvement but no evidence of spinal cord disease; 1: spinal cord disease but no difficulty in walking; 2: slight difficulty in walking, but still employable; 3: difficulty in walking preventing full-time work ∗∗∗∗∗∗ ∗∗∗∗∗∗∗ or housework but independent ambulation; 4: able to walk with assistance or a walker; and 5: chair-bound or bedridden). Median (5th–95th percentile range). Modified McCormick classification (grade I: neurologically normal, normal ambulation and professional activity, and minimal dysesthesia; grade II: mild motor and sensory deficit, independent function, and ambulation maintained; grade III: moderate sensorimotor deficit, restriction of function, and independent with an external aid; grade IV: severe sensorimotor deficit, restricted function, and dependent; and grade V: paraplegia and quadriplegia and even/flickering movement). Applied Bionics and Biomechanics 7 Table 3: Review of HAL treatment for spinal disease. Age Number 10MWT 10MWT Author, Time when BI WISCI II (years), Diagnosis of HAL Speed (m/min) Cadence (steps/min) year starting HAL sex sessions Pre Post Pre Post Pre Post Pre Post 2-3 53.6 POD 14.2 times/ 19.7 20.0 Our result ± 16.1, M Table 1 64.1 ± 16.0 74.8 ± 10.8 102.7 ± 17.6 92.7 ± 10.9 83.3 ± 16.0 95.6 ± 5.8 (7–29 days) week, ± 0.5 ± 0.0 6; F 3 5.0 ± 2.6 T2–8 Sakakima POD 49 OPLL, 6 times/ et al., 2013 60, F (after bed rest) N/A N/A N/A N/A N/A N/A 0 8 T9–10 week, 48 [18] to 15 weeks OLF Kubota T8–11, 2-3 Approximately Approximately Approximately Approximately et al., 2016 43, M L1–3 POD 14–44 times/ 60 85 13 16 ∗ ∗ ∗ ∗ 20 50 42 85 [19] OPLL week, 10 POD 44 2-3 Fujii et al., T3–7 63, F (after bed rest) times/ 15.9 31.8 43.8 77.9 N/A N/A 8 16 2017 [20] OPLL to POD 73 week, 10 Kubota Once/2 C5-6 14 years after et al., 2017 66, F weeks, 22.5 46.7 61.9 81.6 N/A N/A 16 16 OPLL surgery [21] 10 Shimizu T12–L1 6 months after 2 times/ Approximately Approximately Approximately Approximately et al., 2017 48, M N/A N/A 7 12 ∗ ∗ ∗ ∗ 13 29 39 62 SDAVF surgery week, 10 [41] T9–12, Taketomi L2/3, L5 1 year after his 2 times/ et al., 2018 70, M 49.8 58.2 109.8 120 N/A N/A N/A N/A OLF, C3– third surgery week, 10 [22] 7 OPLL 59.6 ± 13.9, M POD 24.4 Approximately Approximately Approximately Approximately 2; F 3 N/A N/A N/A N/A ∗ ∗ ∗ ∗ 28 54 63 83 (15–32 days) (acute Puentes 2 times/ group) et al., 2018 OPLL week, 10 [26] 70.1 ± 6.9, Approximately Approximately Approximately Approximately M7 POD 1151.4 N/A N/A N/A N/A ∗ ∗ ∗ ∗ 48 56 100 100 (chronic (287–3655 days) group) 5 times/ 8.1 (1–19) years Aach et al., 48 ± 9.4, T8–L2 week, 0.28 ± 0.28 10 11.1 posttrauma—90 0.5 ± 0.34 N/A N/A N/A N/A 2014 [9] M6; F2 SCI 51.75 (m/sec) ± 4.3 ± 3.7 days ± 5.6 8 Applied Bionics and Biomechanics Table 3: Continued. Age Number 10MWT 10MWT Author, Time when BI WISCI II (years), Diagnosis of HAL Speed (m/min) Cadence (steps/min) year starting HAL sex sessions Pre Post Pre Post Pre Post Pre Post 10 years 52, M L3 SCI posttrauma—12 5 times/ Cruciger weeks week, 85.6 ± 56.9 et al., 2016 44.3 ± 34.6 N/A N/A N/A N/A N/A N/A mean (sec) 19 years [10] 54.5 40, F L1 SCI posttrauma—12 weeks 8.8 (0.7–17) Sczesny- 46.9 ± 2.7, T8–L2 years 5 times/ 0.25 ± 0.05 Kaiser et al, 0.5 ± 0.07 N/A N/A N/A N/A N/A N/A M7; F4 SCI postinjury—12 week, 60 (m/sec) 2015 [11] weeks 3-4 T12–L1 times/ 62, M 7 days post onset 21.6 39.6 62 99.5 35 60 5 18 SCI week, 7- Watanabe et al., 2017 3-4 [12] T8–10 14 days post times/ 61, F 21.6 60.7 52 97.3 60 80 4 13 SCI onset week, 7-8 Grasmücke 44.3 6.9 (1–22) years C2–L4 5 times/ 70.45 ± 61.5 9.35 11.04 et al., 2017 ± 13.9, M posttrauma—12 35.22 ± 30.8 N/A N/A N/A N/A SCI week, 60 (sec) ± 5.12 ± 4.52 [8] 43; F 12 weeks 5 times/ 8.1 (1–19) years 48 ± 9.4, T8–L2 week, 0.28 ± 0.10 10 11.13 posttrauma—12 0.5 ± 0.12 41.85 ± 9.45 56.7 ± 9.9 N/A N/A M6; F2 SCI 51.75 (m/sec) ± 1.5 ± 1.3 weeks ± 5.6 3–5 Jansen times/ No patient Subgroup T8–L2 Plus 40 weeks 28.61 ± 6.9 et al., 2017 week, 21.22 ± 6.6 49.71 ± 8.8 72.16 ± 6.9 N/A N/A improved or 1: n =4 SCI (at 52 weeks) (sec) [13] 126.8 worsened ± 7.9 Once/ No patient Subgroup T8–L2 Plus 40 weeks week, 34.28 ± 18.2 34.61 ± 17.3 63.65 ± 18.7 62 ± 18.8 N/A N/A improved or 2: n =4 SCI (at 52 weeks) 32.3 (sec) worsened ± 3.3 Jansen 44.8 6.5 (1–19) years 30.9 ± 8.71 C4–L3 5 times/ 61.17 ± 44.27 10.7 11.7 et al., 2018 ± 13.8, M posttrauma—12 32.18 ± 25.53 (number 20.7 ± 5.51 N/A N/A SCI week, 60 (sec) ± 4.95 ± 4.5 [14] 15; F 6 weeks of steps) M = male; F = female; 10MWT = 10-m walking test; BI = Barthel Index; WISCI II = the walking index for spinal cord injury; POD = postoperative day; Pre = before training; Post = after training; N/A = not available; OPLL = ossification of the posterior longitudinal ligament; OLF = ossification of ligamentum flavum; SDAVF = spinal dural arteriovenous fistula; SCI = spinal cord injury. Estimated from the presented figure in the paper. Applied Bionics and Biomechanics 9 indicated that long steps decreased the cadence. Although (biofeedback); in turn, the activated CNS enhances its descending signals [2]. Therefore, the spasticity could be natural recovery in the acute state following injury or surgical ameliorated by HAL therapy. Furthermore, a previous intervention has to be taken into account, it was thought that the functional recovery rate could be facilitated by study showed that HAL was effective for treating spastic hemiplegia due to stroke [16], and two studies have shown HAL treatment from an early stage [18–20, 26]. that HAL treatment for stroke patients facilitated cortical Even though our study showed a significant improve- activities in the damaged brain [16, 17]. ment with HAL treatment, it had several limitations. We In this study, significant improvements were seen in investigated a relatively small number of patients with het- erogeneous characteristics. Our patients underwent HAL gait ability following robotic rehabilitation. The results showed improvements in a series of clinical scales such as treatment during the early postoperative state, but our 10MWT, BI, GARS-M, and WISCI II. All participants cohort did not have a control group. Therefore, it is possi- showed improvements in gait ability that were similar to ble that spontaneous recovery following surgery may have those of previous reports concerning the use of HAL for contributed to the postoperative course. However, it should also be noted that our patients experienced earlier recov- spine disorders such as SCI [8–14], SDAVF [41], and OPLL [18–22, 26]. It is noteworthy that participants in our study ery than those described in previous reports [18–20, 26] underwent surgery for various reasons such as spinal cord because our patients started HAL therapy during relatively tumor, vascular disease, and bone degenerative disease. Addi- early postoperative periods. tionally, clinical manifestations of vascular disease and tumors in the spine are similar [27, 28], and rehabilitation 5. Conclusions outcomes following vascular-related and traumatic SCI were reportedly not significantly different [29]. These facts may We showed the feasibility and safety of HAL treatment and determined that it could potentially facilitate functional indicate that HAL therapy may be applied for a variety of disorders with spinal cord origins. recovery, even for postoperative patients. Further studies involving more patients and a control group are warranted This study also showed the usefulness of HAL for postop- to verify our findings. erative rehabilitation. There have been only five case reports of HAL-assisted rehabilitation for a patient who underwent surgery for thoracic OPLL [18–22]. It is advantageous that Data Availability HAL does not interfere with the skin incision and can be used The data used to support the findings of this study are avail- for patients with a corset. In our experience, HAL was con- able from the corresponding author upon request. sidered to facilitate early recovery after spine surgery. In this study, HAL treatment was performed for patients with rare spinal diseases. In previous studies, the diagnosis Conflicts of Interest and surgical management were emphasized rather than the The authors declare that they have no conflicts of interest. rehabilitation programs, even though it has been consid- ered that improvement after surgery depends on the length of time and initiation of neurological rehabilitation Acknowledgments [30]. However, outcome measures have not been standard- This study was partly supported by the Japan Society for ized. Previous reports showing the clinical outcomes of the Promotion of Science grant-in-aid for young scientists treatment for the same spine disorders are summarized ((B) 15 K19984); Takeda Science Foundation, Uehara in Table 2 [30–40]. Memorial Foundation; and Central Research Institute, We also reviewed clinical studies of gait training using Fukuoka University (Grant no. 161042). The authors appre- HAL for spine disorders. A systematic search of the liter- ciate the help of Ms. Asuka Ikezaki, who assisted with the ature was conducted using the PubMed database. Search statistical analysis. terms were “HAL” OR “Hybrid Assistive Limb” AND “Spinal Cord Injury” OR “OPLL.” We searched Google Scholar, and only one work [19] was included from that References search. Studies only reporting HAL for gait training were [1] K. Suzuki, G. Mito, H. Kawamoto, Y. Hasegawa, and Y. 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