Combined robotic-aided gait training and physical therapy improve functional abilities and hip kinematics during gait in children and adolescents with acquired brain injury.

Brain Injury

ISSN: 0269-9052 (Print) 1362-301X (Online) Journal homepage: http://www.tandfonline.com/loi/ibij20

Combined robotic-aided gait training and physical therapy improve functional abilities and hip kinematics during gait in children and adolescents with acquired brain injury Elena Beretta, Marianna Romei, Erika Molteni, Paolo Avantaggiato & Sandra Strazzer To cite this article: Elena Beretta, Marianna Romei, Erika Molteni, Paolo Avantaggiato & Sandra Strazzer (2015) Combined robotic-aided gait training and physical therapy improve functional abilities and hip kinematics during gait in children and adolescents with acquired brain injury, Brain Injury, 29:7-8, 955-962, DOI: 10.3109/02699052.2015.1005130 To link to this article: http://dx.doi.org/10.3109/02699052.2015.1005130

Published online: 27 Apr 2015.

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Date: 15 September 2015, At: 01:50

http://informahealthcare.com/bij ISSN: 0269-9052 (print), 1362-301X (electronic) Brain Inj, 2015; 29(7–8): 955–962 ! 2015 Informa UK Ltd. DOI: 10.3109/02699052.2015.1005130

ORIGINAL ARTICLE

Combined robotic-aided gait training and physical therapy improve functional abilities and hip kinematics during gait in children and adolescents with acquired brain injury Elena Beretta1, Marianna Romei2, Erika Molteni1, Paolo Avantaggiato1, & Sandra Strazzer1 Acquired Brain Injury Unit and 2Bioengineering Lab, Scientific Institute IRCCS Eugenio Medea, Bosisio Parini, Lecco, Italy

Downloaded by [Central Michigan University] at 01:50 15 September 2015

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Abstract

Keywords

Purpose: To evaluate the combined effect of robotic-aided gait training (RAGT) and physical therapy (PT) on functional abilities and gait pattern in children and adolescents exiting acquired brain injury (ABI), through functional clinical scales and 3D-Gait Analysis (GA). Methods: A group of 23 patients with ABI underwent 20 sessions of RAGT in addition to traditional manual PT. All the patients were evaluated before and after the training by using the Gross Motor Function Measures (GMFM) and the Functional Assessment Questionnaire. Ambulant children were also evaluated through the 6 Minutes Walk Test (6MinWT) and GA. Finally, results were compared with those obtained from a control group of ABI children who underwent PT only. Results: After the training, the GMFM showed significant improvement in both dimensions ‘D’ (standing) and ‘E’ (walking). In ambulant patients the 6MinWT showed significant improvement after training and GA highlighted a significant increase in cadence, velocity and stride length. Moreover, hip kinematics on the sagittal plane revealed a statistically significant increase in range of motion (ROM) during the whole gait cycle, increased hip extension during terminal stance and increased ROM during the swing phase. Conclusions: The data suggest that the combined programme RAGT + PT induces improvements in functional activities and gait pattern in children and adolescents with ABI and demonstrated it to be an elective tool for the maintenance of the patients’ full compliance throughout the rehabilitative programme.

3D-Gait Analysis (GA), acquired brain injury (ABI), body-weight support, lower limb kinematics, range of motion of the hip joint, robotic-aided gait training (RAGT), spatio-temporal parameters of gait

Introduction Acquired brain injury (ABI) may result in lifelong impairment of physical, cognitive and psychosocial functions. The movement disorders of patients with ABI (i.e. abnormal strength, co-ordination, balance, gait) often come along with partial or total impairment of the lower limbs movements and central gait disorders, up to the complete loss of ambulation. The recovery of walking ability is often a primary rehabilitation goal for patients with traumatic brain injury (TBI), as well as one of the major challenges for rehabilitation specialists [1]. Among the most common causes that may preclude gait recovery after ABI, the loss of sufficient strength or balance to maintain an erect posture has been identified [2]. Task-specific gait training rehabilitation groups a large spectrum of approaches, ranging from manually assisted conventional over-ground gait training to the more recently developed robotic-aided gait training (RAGT). Using robotic orthoses with a system to partially or totally support the

Correspondence: Elena Beretta, MD, Acquired Brain Injury Unit, Scientific Institute IRCCS Eugenio Medea, Bosisio Parini, Lecco, Italy. Tel: +39.031.877851. E-mail: [email protected]

History Received 1 April 2014 Revised 14 October 2014 Accepted 5 January 2015 Published online 23 April 2015

body-weight and a treadmill, RAGT drives the patient’s lower legs to experience the repetitive practice of gait, with attention to the ideal kinematic and physiological temporal features of gait [3]. RAGT allows to repeat a very large number of steps during a single training session and promotes the movement of limbs and trunk to generate sensory information consistent with locomotion, so as to enhance neuroplasticity and, thus, to improve the potential for the recovery of walking after neurologic injury [4]. Recently, the effects of RAGT and, more generically, of body-weight supported treadmill training (BWSTT) have been investigated in patients with neurological disorders. In many pathologies BWSTT has been proven to contribute functional benefits such as earlier gait rehabilitation [5] and greater weight-bearing ability, while RAGT pointed out improved gait symmetry [6], increased walking speed and endurance [7] and improved gait pattern over ground [8]. Wilson and Swaboda [9] first reported that two patients with ABI, classified as acute (56 months) and chronic (42 years), improved their gait ability after partial weight-bearing gait training, including muscle strength, level of spasticity, balance and walking ability. In 2006, Wilson et al. [10] provided evidence that, in a cohort of 38 adult patients with TBI, RAGT was as effective as conventional over-ground gait


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training in restoring ambulation, as measured by some commonly used clinical scales. Similarly, a later work by Esquenazi et al. [6] found similar improvements in gait velocity, endurance and a specific mobility scale after both manual traditional gait training and RAGT; additionally, they demonstrated grater improvement in gait symmetry for patients who had had RAGT. However, similar results supporting RAGT in gait rehabilitation of patients with neurological impairment were limited in other studies [11–13]. Recently, Lapitskaya et al. [14] investigated the effects of RAGT on electroencephalographic activity in patients with severe ABI and in healthy people. The study showed that RAGT induced measurable changes in the EEG power spectrum of healthy controls after one session of treatment, while no changes were observed in patients with severe TBI, probably due to the severity of brain dysfunction. As neuroplasticity is thought to be higher in children, robotic-aided gait training in this population may be even more beneficial than in older patients. Considering the paediatric patients’ population, although a number of works has already been carried on to investigate the changes induced by RAGT in children with Cerebral Palsy (CP) [7, 11, 15–20], to the authors’ knowledge no work has ever been focused on the effect of RAGT on functional abilities and gait pattern in groups of children and adolescents suffering from ABI. In particular, previous studies exist in which the walking ability was addressed by using clinical scales and/or spatio-temporal gait parameters only, while the analysis of joint kinematics during gait after RAGT has been uniquely performed on a group of children with CP [11]. The aim of this work is, thus, the investigation of the functional changes induced by the combined administration of RAGT and PT in a group of 23 children and adolescents with ABI, by using clinical functional scales and 3D Gait Analysis and by considering both spatio-temporal parameters and lower limb joint kinematics.

Methods Participants Twenty-three participants (12 boys and 11 girls) were recruited in the experimental group (‘Ex’) from the in-patient setting of the Neurorehabilitation Unit 3, I.R.C.C.S. E. Medea- Ass. La Nostra Famiglia, Bosisio Parini, Italy. All patients who entered the clinic within a 2-year timeframe were screened for inclusion and exclusion criteria and the ones who met the inclusion criteria were asked to participate in the study. Inclusion criteria comprised (1) diagnosis of ABI in paediatric age and adolescence (2–20 years), (2) age at injury 520 years; (3) femur length 421 cm, (4) the ability to follow the instructions and (5) the ability to signal fear, pain and discomfort. Exclusion criteria were (1) severe lower extremity contractures, fractures, osseous instabilities and osteoporosis, (2) open skin lesions of the lower extremity, (3) thromboembolic disease or cardio-vascular instability, (4) aggressive or self-harming behaviour, (5) lower limb orthopaedic surgery and/or botulinum toxin injection during the 6 months prior to the enrolment and (6) neurological or cognitive-behavioural deficit/impairment manifested before

Brain Inj, 2015; 29(7–8): 955–962

the ABI event. Presence of scoliosis was not an exclusion criterion. Following the same inclusion/exclusion criteria, 11 children (seven boys and four girls) were recruited, who made up the control group (‘Ct’). Written consent was obtained from the parents/guardians of each patient younger than 18 years; while patients aged 18 years and older were asked to provide their personal consent, if sufficient cognitive abilities had been previously assessed; parents/guardians provided consent in all the other cases. The study protocol was approved by the Ethics Committee of I.R.C.C.S. E. Medea- Ass. La Nostra Famiglia, Bosisio Parini, Italy and it was conducted in accordance with the Declaration of Helsinki. Patients’ characteristics (age at assessment time, gender, weight and height) and clinical information were collected during the study recruitment. Clinical information comprised aetiology, age at injury, classification in acute (0–6 months), sub-acute (6–12 months) and chronic (412 months) condition at assessment time, previous neurosurgery, type of motor impairment, severity of motor impairment classified according to Gross Motor Function Classification System (GMFCS) and ambulant/not ambulant condition. Rehabilitation protocol The aim of RAGT was to gain or improve walking capacity, depending on the individual GMFCS level. The rehabilitation protocol of this study included one session of RAGT per day, in addition to traditional physiotherapy. Traditional PT consisted of exercises for improving gait, balance and functional abilities, for strengthening the extensor muscles and for stretching the flexor muscles. Each RAGT session lasted 45 minutes; the treatment was administered five times per week, during the working days and had a total duration of 4 weeks. Group ‘Ex’ received RAGT + PT sessions, while group ‘Ct’ received PT only in two sessions per day. RAGT RAGT was performed using the commercially available Driven Gait Orthosis (DGO) LokomatÕ (Hocoma AG, Volketswil, Switzerland). The DGO consists of two exoskeletons, which are adjustable to the patient’s morphology (a paediatric and an adult module are available in the Institute). Several braces are used to fasten the patient to the DGO. The legs of the DGO are connected to the frame of a body-weight support system by a four-bar linkage, which allows vertical movements and provides vertical stability. On each leg, two linear drives move the hip and knee joints of the orthosis. These drives are position-controlled so that a kinematics—mimicking the normal walking pattern—can be performed and synchronized with the treadmill. Walking speed can be set between 1.0–3.2 km h1. For body-weight support, a counter system with a harness is used. Several security measures provide safe training conditions. These include stop buttons for both therapist and patient and a controller that limits both excessive force at the drives and deviations from the desired position of the joint angles, so that the DGO stops immediately if severe spasticity or dystonia

Robotic training of hip kinematics in child ABI


DOI: 10.3109/02699052.2015.1005130

occurs [21]. During the training, LokomatÕ can also provide an augmented performance feedback that emphasizes the patient’s active participation and motivation through several virtual environments and different-level exercises/games. The amount of RAGT unloading was initially set at 50% of body weight, to be decreased successively according to gains in muscle strength (allowing no excessive knee flexion during stance). Initial gait velocity during the RAGT was chosen according to the capabilities of the child (1.5 km h1 on average). The leading force was continuously reduced from 100% to 5% higher than the value leading to the activation of the control system of LokomatÕ to stop the device. During RAGT, patients continuously received encouragement by therapists and augmented performance feedback was used in all the sessions in order to engage them as much as possible and to increase their active participation and motivation. Active participation was additionally achieved by varying the speed, the body-weight support or the leading force of LokomatÕ during any single session. Evaluation measures Before (T0) and at the end of the treatment (T1), all the patients underwent a clinical examination that included the Gross Motor Function Measure and the Functional Assessment Questionnaire for the assessment of motor functional abilities. For ambulant patients the assessment also included the 6-Minute Walk Test and the 3D-Gait Analysis for the evaluation of the gait endurance and the gait pattern, respectively. The Gross Motor Function Measure (GMFM) was developed and validated specifically for children and provides a measure of the child’s overall functional motor abilities [22–24]; it consists of 88 items, divided into the following sections: (A) lying and rolling, (B) sitting, (C) crawling and kneeling, (D) standing and (E) walking, running and jumping. Each section contributes to the total GMFM score (range ¼ 0– 100). The GMFM is widely employed in clinical rehabilitation for rating the severity of motor disability and it is the elective measurement tool for the assessment of motor function in children with CP. In a multi-centre trial, however, Linder-Lucht [25] also demonstrated the reliability of GMFM in the evaluation of functional abilities in children with ABI. The Functional Assessment Questionnaire (FAQ) consists of a 10-level classification of ambulatory function in everyday-life [26]; the relatives or caregivers are asked to score the walking ability of their children. For the ambulant patients the 6-Minute Walk Test (6MinWT) was applied in the present study to assess gait endurance [27]; it is a self-paced, submaximal test that assesses the functional capability of walking a long distance, thus providing a reliable estimation of the ability to walk in the community. Patients are instructed, by means of standardized verbal instructions, to walk at a comfortable speed, covering as much distance as possible in 6 minutes along a standardized route through the hospital corridors [28]. 3D-Gait Analysis (GA) was performed with an eight cameras optoelectronic system working at 100 Hz (Elite, BTS Bioengineering, Milan, Italy) and two force plates (Kistler, Winterthur, Switzerland). During 3D-GA the children were

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asked to walk at their preferred speed and to wear their usual orthoses and footwear only if they were unable to walk in a barefoot condition. For each assessment, at least five trials for the left and the right limbs were collected and processed using dedicated software (EliClinic, BTS Bioengineering). A GA experienced physiatrist selected the most representative trial of each child for further analysis. Walking velocity, cadence, bilateral stance duration (as a percentage of gait cycle), bilateral step length, bilateral stride length and bilateral step width were measured as spatio-temporal gait parameters. In addition, symmetry indexes for stance, step length and stride length were calculated, as previously proposed by Robinson et al. [29]. GA kinematic parameters of the pelvis, hip and knee included: mean pelvic tilt, Range of Motion (ROM) of pelvic tilt, mean pelvic rotation, ROM of pelvic rotation, ROM of hip flex-extension, maximum hip extension, ROM of hip extension during swing phase, peak of hip adduction during swing phase, mean hip rotation during stance, ROM of knee flex-extension and knee flexion at Initial Contact. From the kinematic parameters, the Gillette Gait Index (GGI) was calculated as a summary of the gait deviation from the normal walking pattern [30]. Statistics First, the distribution of all the clinical, spatio-temporal and kinematic data was tested by applying the KolmogorovSmirnov test; for each variable, the normality of data distribution was checked. For group analyses, mean ± standard deviations (SD) were calculated in the case of continuous data, while median and range values (minimum value– maximum value) were calculated for ordinal data. GMFM and FAQ data were analysed by considering the whole group first and then the sub-group of ambulant patients only; median and range values were provided for the groups in both the analyses. According to the Kolmogorov-Smirnov test results, a parametric t-test for paired samples was applied to normal data to perform T0–T1 comparisons, while a non-parametric Wilcoxon test was employed for comparing the remaining data ( ¼ 0.05). The level of significance was set at p50.05 for all the statistical comparisons. Statistical analyses were carried out using NCSS software (Kaysville, UT).

Results Table I reports the patients’ data. The group ‘Ex’ comprised 11 girls and 12 boys; all the patients completed the whole rehabilitation programme consisting of 20 RAGT and 20 PT sessions. The subjects’ mean age at injury was 11 years and 8 months (SD ¼ 4 years and 10 months) and the subjects’ mean age at T0 was 13 years and 11 months (SD ¼ 5 years and 5 months). The aetiology was traumatic injury in 47.8% of patients, brain tumour in 30.4 %, ictus in 17.4% and anoxia in 4.3%. At the beginning of the RAGT + PT, eight (34.8%) patients were in the acute stage, two (8.7%) in the sub-acute stage and 13 (56.5%) in the chronic condition. In the group, 52.1% of the cases (12 out of 23 patients) had previously received a neurosurgical treatment. According to GMFCS, six patients were assigned to level II, nine to level III and eight to

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Table I. Patients’ clinical description.

N

Group

Sex

Height (cm)

Weight (kg)

Age at injury

Age at study

Neuro-surgery

GMFCS

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34

Ex Ex Ex Ex Ex Ex Ex Ex Ex Ex Ex Ex Ex Ex Ex Ex Ex Ex Ex Ex Ex Ex Ex Ct Ct Ct Ct Ct Ct Ct Ct Ct Ct Ct

F F M F M M M F M F F M F M F F F M M M M M F M F M M M M M F M F F

144 105 108 156 146 140 181 137 189 170 150 143 163 155 130 167 115 170 170 175 115 177 151 107 127 177 98 163 162 138 144 125 110 120

32 20 24 54 44 36 68 38 62 64 49 50 75 51 25 45 17 74 70 83 20 81 67 18 23 76 15 47 72 35 40 24 20 23

10.0 4.9 4.3 19.3 10.7 2.5 17.1 14.0 15.0 11.3 12.5 11.8 16.2 12.0 5.7 15.4 4.4 14.9 12.2 15.7 7.2 18.9 11.6 4.0 7.9 17.2 3.3 11.3 11.9 11.8 11.6 6.0 1.3 6.0

10.4 5.4 4.8 20.3 10.9 10.0 18.2 14.1 17.8 17.0 21.1 12.4 19.7 13.7 6.1 16.8 5.1 19.0 14.0 20.0 7.7 19.9 15.4 4.2 8.4 20.8 3.6 17.3 14.7 12.1 12.9 7.5 5.7 7.0

no no yes yes no yes no yes no no no yes no yes no no yes no yes yes yes yes yes no yes no yes no yes yes yes no yes yes

2 2 2 2 2 2 3 3 3 3 3 3 3 3 3 4 4 4 4 4 4 4 4 2 2 3 3 3 3 3 4 4 4 4

Functional impairment left hemiplegia right hemiplegia tetraplegia ataxia right hemiplegia right hemiplegia tetraplegia left hemiplegia paraplegia tetraplegia paraplegia paraplegia right hemiplegia ataxia left hemiplegia tetraplegia tetraplegia tetraplegia right hemiplegia tetraplegia tetraplegia left hemiplegia tetraplegia tetraplegia left hemiplegia tetraplegia ataxia tetraplegia right hemiplegia tetraplegia tetraplegia ataxia left hemiplegia tetraplegia

Autonomous gait yes* yes* yes* yes* yes* yes* yes* yes* yes* yes* yes no yes yes yes no no no yes no no yes yes yes* yes* yes* yes* yes* no no no no no no

*Ambulant patients who underwent GA at T0 and T1.

level IV. All the patients were affected by motor impairment, with a prevalence of quadriplegia (nine patients), hemiparesis (nine patients: five right and four left), ataxia (two patients) or paraplegia (three patients). At the beginning of the study, 17 out of 23 patients presented autonomous gait without walking aids, at least for short distances; among this group of independent walkers, 10 children, five boys and five girls, underwent GA assessment at T0 and T1, as their parents/guardians provided additional consent for that evaluation (asterisk in the last column of Table I). The group ‘Ct’ comprised seven boys and four girls (Table I); all the patients completed the whole rehabilitation programme, consisting of 40 sessions of traditional manual PT. All the ambulant children in the group underwent GA assessment at T0 and T1, as their parents/guardians provided additional consent for that evaluation. Table II shows the GMFM and FAQ values for the two groups at T0 and T1. The GMFM total score showed statistically significant improvement after the combined rehabilitation programme RAGT + PT (Z ¼ 3.60, p50.001) and the GMFM percentage confirmed the statistically significant improvement in functional abilities after the training. Considering the dimensions ‘D’ and ‘E’, that are strongly related to the subject’s ability to stand and walk, run and

jump, respectively, a statistically significant increase was found for group ‘Ex’ after training and for both dimensions (Z ¼ 3.50, p50.001 for dimension ‘D’; Z ¼ 3.42, p50.001 for dimension ‘E’). Moreover, improvement was observed for dimension ‘C’, related to crawling and kneeling (Z ¼ 2.49 and p ¼ 0.006) and for dimension ‘A’, pertaining to laying and rolling (Z ¼ 2.62, p ¼ 0.004). On the other hand, no significant changes were found for dimension ‘B’, related to sitting. Additionally, the FAQ values also showed significant differences after the RAGT + PT (Z ¼ 2.64, p ¼ 0.004). The separate analysis of the sub-group of ambulant patients receiving RAGT + PT (17 out of 23) confirmed GMFM results obtained from the entire sample. Also, statistically significant improvements were observed for dimension ‘D’ (standing), which moved from 66.5 (range ¼ 13–90) at T0 to 73.0 (range ¼ 18–97) at T1 (Z ¼ 4.02, p ¼ 0.001), for dimension ‘E’ (walking), which moved from 44.0 (range ¼ 4–90) at T0 to 53.0 (range ¼ 4–92) at T1 (Z ¼ 3.03, p ¼ 0.001) and for dimension ‘C’ (crawling and kneeling), which moved from 80.0 (range ¼ 0–100) at T0 to 96.5 (range ¼ 0–100) at T1 (Z ¼ 2.94, p50.006). The ‘Ct’ group provided significant improvement in dimension ‘C’ only. Ambulant patients in group ‘Ex’ provided FAQ with a median score of 4 (range ¼ 2–9) before the training and a


DOI: 10.3109/02699052.2015.1005130

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Table II. Median and range (minimum value–maximum value) of GMFM (total score, percentage and dimensions) and FAQ for groups ‘Ex’ (RAGT + PT) and ‘Ct’ (PT only) before (T0) and after (T1). Group ‘Ex’ (RAGT + PT) T0 GMFM GMFM GMFM GMFM GMFM GMFM GMFM FAQ

total % dim A dim B dim C dim D dim E

171 67 96 97 69 54 32 3

Group ‘Ct’ (PT only)

T1

(27–253) (11–96) (27–100) (0–100) (0–100) (0–90) (0–90) (1–9)

185 73 96 97 76 62 37 4

T0

(32–257)*** (12–98)*** (47–100)** (3–100) (0–100)** (0–97)*** (0–92)*** (1–9)**

190 76 94 97 81 67 25 4

T1

(89–247) (33–94) (45–100) (62–100) (7–95) (3–95) (4–82) (1–8)

195 78 100 100 83 74 25 4

(95–254) (37–97) (69–100) (65–100) (12–100)** (10–95) (8–89) (1–8)

**p value50.01 when compared with T0; ***p value50.001 when compared with T0.


Table III. Mean (SD) values of GA spatio-temporal parameters for the ambulant patients of groups ‘Ex’ (RAGT + PT) and ‘Ct’ (PT only) before (T0) and after (T1). Group ‘Ex’ (RAGT + PT) T0 Left Stance, % stride Right Stance, % stride Stance Symmetry Cadence, step/min Step length left, mm Step length right, mm Mean Step length, mm Step Symmetry Velocity, m s1 Stride length left, mm Stride length right, mm Mean Stride length, mm Stride Symmetry Step Width, mm

67.50 68.40 14.34 76.20 344.70 392.80 368.75 19.48 0.49 753.00 731.50 742.25 5.50 146.50

(11.9) (11.9) (10.1) (41.6) (115.7) (154.1) (132.2) (6.7) (0.3) (265.0) (249.1) (250.6) (4.1) (38.6)

T1 66.00 65.90 15.04 82.30 449.00 425.90 437.45 16.52 0.65 883.60 895.00 889.30 5.58 150.20

(12.2) (9.6) (8.6) (39.6)* (156.9)* (157.3) (152.3)* (13.9) (0.4)* (319.5)* (289.3)** (302.5)* (8.9) (38.1)

Group ‘Ct’ (PT only) T0 67.8 63.0 8.7 82.8 333.2 361.2 347.2 23.6 0.5 672.4 685.0 678.7 8.2 135.6

(11.5) (6.8) (9.2) (45.5) (102.9) (100.1) (93.0) (12.5) (0.3) (195.1) (179.4) (184.9) (8.0) (56.3)

T1 66.0 65.2 8.7 78.2 372.2 385.2 378.7 22.3 0.5 762.2 777.4 769.8 4.6 133.4

(10.1) (4.5) (5.6) (31.4) (97.1) (97.9) (80.6) (17.5) (0.3) (164.7) (131.8) (147.7) (6.0) (67.2)

*p value50.05 when compared with T0; **p value50.005 when compared with T0.

median score of 5 (range ¼ 2–9) at the end of the training (Z ¼ 2.75, p ¼ 0.007). Moreover, 6MinWT moved from 198.1 (SD ¼ 155.7), as measured before RAGT + PT, to 233.6 (SD ¼ 152.4) (p50.005); after the training only one patient decreased the distance she walked and two patients walked the same distance at T0 and T1. Group ‘Ct’ lacked in significant differences between T0 and T1 at FAQ and 6MinWT. As reported in Table I, 10 patients of the group ‘Ex’ and five patients of the group ‘Ct’ underwent GA before and after the rehabilitation programme. Among the spatio-temporal parameters (Table III), statistically significant changes after the training were found in group ‘Ex’ for cadence, step length left, mean step length, velocity, stride length left, stride length right and mean stride length. Table IV reports mean values (SD) of the kinematic parameters of the pelvis, hip and knee for the groups of patients who underwent GA. Regarding group ‘Ex’, the kinematic parameters that changed with statistical significance after RAGT + PT were all the hip joint parameters: the ROM of hip flex-extension of the whole gait cycle, the maximal hip extension and the ROM of hip flex-extension during the swing phase. Gillette Gait index slightly decreased after the training, but the difference between T0 and T1 data was not statistically

significant. Group ‘Ct’ showed concordant trends for several measures: pelvic rotation, maximum hip extension, ROM of hip flex-extension during swing phase and Gillette Gait index. Nevertheless, measures in group ‘Ct’ could not reach significance.

Discussion The present study was carried out in order to evaluate the effect of combined administration of Robotic-Aided Gait Training and traditional physical therapy on functional abilities and on lower limb joint kinematics during gait in a group of children and adolescents suffering from ABI. Clinical functional scales for the whole group of patients and 3D Gait Analysis for the ambulant patients were used as assessment tools. The main finding of this study is that RAGT + PT was effective in improving functional abilities of all the enrolled patients and improvements in gait spatiotemporal parameters and in hip joint kinematics were found for the group of ambulant patients receiving RAGT + PT. Considering the whole group ‘Ex’, the clinical results showed an increase in GMFM score, suggesting a global improvement in motor and functional abilities after RAGT + PT. In particular, the results related to GMFM dimensions ‘D’ and ‘E’ indicated global enhancement in

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Table IV. Mean (SD) values of GA kinematic parameters for the ambulant patients of groups ‘Ex’ (RAGT + PT) and ‘Ct’ (PT only) before (T0) and after (T1). Group ‘Ex’ (RAGT + PT) T0

Mean Pelvic Tilt ( ) ROM Pelvic Tilt ( ) Mean Pelvic Rotation ( ) ROM pelvic rotation ( ) ROM Hip Flex-Extension during gait cycle ( ) Maximum hip extension ( ) ROM Hip flex-extension during swing phase ( ) Mean hip rotation during gait cycle ( ) Peak hip adduction in swing ( ) Knee Flexion at IC ( ) ROM Knee Flex-Extension ( ) Gillette Gait Index

16.81 10.27 0.17 14.74 41.62 0.47 41.49 13.77 10.97 8.60 53.37 155.5

(5.20) (3.90) (7.21) (4.27) (10.50) (8.99) (10.45) (7.96) (4.82) (118.00) (10.90) (86.8)

Group ‘Ct’ (PT only)

T1 17.90 10.27 0.06 18.52 46.54 3.03 46.00 13.37 10.19 9.79 54.94 142.8

(5.10) (4.10) (9.59) (6.84) (12.20)* (10.56)* (12.66)* (8.32) (4.77) (7.40) (9.70) (67.3)

T0 12.91 8.67 0.17 15.18 40.31 3.21 30.79 0.00 7.59 10.10 54.33 117.2

(5.77) (4.16) (5.09) (7.05) (12.20) (14.35) (13.98) (13.05) (3.40) (11.10) (11.97) (114.9)

T1 13.15 8.34 0.00 18.93 42.16 5.45 35.22 4.86 6.87 5.79 54.39 113.9

(6.15) (5.26) (8.40) (43.00) (10.23) (11.82) (9.49) (10.49) (5.12) (9.75) (12.10) (116.3)


*p value50.05 when compared with T0.

patients’ standing and walking abilities. These data confirmed what was previously reported by other authors regarding the RAGT effects on children with CP [7, 17], on children with central gait impairment [8] and on adults with TBI [10]. The increase in FAQ scores also confirmed that parents and caregivers succeeded in perceiving the children’s improvement in several motor skills. After RAGT + PT, ambulant patients of this study were able to walk for longer distance, as demonstrated by the 6 Minute Walk Test. This result confirmed the significant increase of the same parameter observed in children with central gait impairment [8, 17] and in adults with TBI [6]. Patients of group ‘Ex’ who underwent Gait Analysis showed relevant improvements in gait pattern after RAGT + PT. The analysis of spatio-temporal parameters highlighted statistically significant changes for cadence and velocity, which are known to be reduced in patients with TBI [31]; after RAGT + PT, these parameters increased in the subgroup of ambulant patients. Further evidence of a global gait improvement was found in the significant increase in step and stride length after training. After ABI, patients indeed show a decreased step length, which is directly linked to the patient’s instability during the single support phase [31]. Thus, enhancement in step length could be ascribed to re-gained stability (i.e. postural and balance skills recovery) [32]. The results related to step and stride symmetry could not demonstrate RAGT + PT efficacy in the improvement/recovery of global gait symmetry. In this regard, previous works reported controversial results. Indeed, in a comparison between RAGT and manually assisted conventional overground gait training for the treatment of adult people suffering from chronic TBI, Brown et al. [33] observed a decrease in gait symmetry after BWSTT. Conversely, Esquenazi et al. [6] reported an increase in gait symmetry after treatment with both conventional over-ground gait training and RAGT, but they concluded that the reduction of asymmetry was greater and significant for the robotic-assisted treadmill training group. The kinematics analysis showed a main RAGT + PT effect on the hip joint motion on the sagittal plane. After RAGT + PT, the ambulant patients significantly increased

their hip extension during terminal stance and increased their hip range of motion during the swing phase. This is directly related to the increased stride length and gait velocity of these patients. No significant effects on pelvic and knee joints were found. The RAGT effect on hip joint movement can be explained by considering the LokomatÕ driven gait orthoses mechanics, that directly act on the hip and knee joints and have a maximal fulcrum at hip level. During RAGT, the pelvis is fixed in the horizontal plane. The pelvis vertical motion is left free, although supported by a body-weight support system. As a consequence, only slight rotations of the pelvis are still possible. In group ‘Ex’, this limitation in pelvic movement could have contributed to enhance hip movements on the sagittal plane, in particular during the terminal stance and swing phases. This interpretation would also match the EMG findings of Hidler and Wall [34], who demonstrated changes in the muscle activation pattern when the pelvis is fixed and the leg movement is limited by the use of LokomatÕ . Another possible explanation for the improvement in hip kinematics could be due to an increment of muscle strength after the training. Unfortunately, muscle strength was not directly evaluated during this study; however, during RAGT patients were continuously encouraged and stimulated to actively move their legs by using the virtual environments and the exercises/games that LokomatÕ provided. During the games, the patients in group ‘Ex’ had to increase their stride length and to extend the hip more in order to have better performance. This result adds up to previous findings of augmented maximum hip flexion during the swing phase in adult patients [32] affected by TBI and to evidences of improvement in the maximal range of flexion in the hip joint subsequent to RAGT in children with CP [11]. Overall, results from group ‘Ct’ provided a sole significant increase in dimension ‘C’ of GMFM, while no modifications were observed in any of the gait spatiotemporal and kinematic parameters; on the other hand, several improvements in group ‘Ex’ emerged from clinical measures as well as from the spatiotemporal and kinematic domains of GA, thus intimating more extensive effects of the combined RAGT + PT on walking abilities. In most cases, paediatric patients suffering from severe ABI undergo long periods of rehabilitative therapies and their


DOI: 10.3109/02699052.2015.1005130

hospitalization lasts for months. Despite the emotional burden due to absence from home, school and their familiar social environments, motivation remains a key component of the rehabilitative process. For this reason, striking importance is attributed to a number of additional evidences: (i) no dropout was registered during the study (i.e. all the patients enrolled remained in the study until the end), (ii) none of the patients missed any RAGT session, (iii) all the patients actively participated in the sessions, throughout the 45 minute intervals, independently from their age, (iv) no specific adaptations were required (e.g. changes to the RAGT instrumentation, need of additional orthoses or softening protections, etc.) and (v) virtual reality and the therapist’ verbal encouragement made possible the fulfillment of the entire rehabilitation programme. One can, thus, conclude that RAGT constituted the elective tool for the maintenance of the patients’ full compliance throughout the rehabilitative route and that intensive RAGT programmes are feasible, even in young patients with ABI. The authors are aware of several limitations of the present study. First, this study did not consider measures of brain plasticity; however, it is possible that RAGT + PT induced modifications at the brain level and that, concurrently, such possible modifications were (at least in part) responsible for the changes in kinematic and gait parameters observed in the patients. Literature has indeed demonstrated that large brain plasticity can occur, even in the presence of small modifications of the kinematic movement parameters [35]; yet, whether younger age at injury and higher residual myelination capabilities vouch for wider cerebral re-organization remains debated [36, 37]. Second, the patients recruited had heterogeneous aetiology, age and severity of the lower limbs functional impairment; however, they represent a quite reliable depiction of the neurorehabilitation clinic population. Third, the two groups discussed in this study are heavily unbalanced in size, as the control group (‘Ct’, PT only) was smaller than the experimental (‘Ex’, RAGT + PT) one. Fourth, outcome assessors were not blinded to the pre- and post-training condition. Last, the study attempted to perform assessments with identical examiners; however, due to organizational reasons, this was not achieved in all cases. However, the extent of GMFM improvements in this patients’ group was greater than those normally anticipated, without intervention, at this stage of the children’s development and within the time frame involved [25]. It is, therefore, reasonable to conclude that the experimental intervention may have been responsible, at least in part, for the observed changes. This study excluded patients who had been recently injected with botulinum toxin, in order to assess the pure effect of RAGT + PT on patients’ functional improvement. Nevertheless, clinicians and therapists should consider the potential benefits deriving from combining botulinum toxin therapy with RAGT + PT.

Conclusion A group of children and adolescents affected by ABI, who underwent a treatment with RAGT + PT, were studied. The GMFM scale showed global improvement in motor and functional abilities and GMFM D and E dimensions


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specifically demonstrated improvement in standing, walking, jumping and running. Moreover, for the ambulant patients the 6MinWT and Gait Analysis provided evidence of improved gait pattern, also confirmed by an increased walked distance, improved spatiotemporal parameters and significant changes in hip joint kinematics on the sagittal plane. Further studies focused on the investigation of long-term effect of RAGT are needed in order to assess whether the induced changes on functional abilities and gait pattern are likely to be maintained over time.

Declaration of interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. This work was supported by a grant of Fondazione Cariplo: SPIDER@Lecco.

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