Improvement of motor performance in children with cerebral palsy treated with exoskeleton robotic training: A retrospective explorative analysis 1

Abstract

Background:

Robot-assisted gait training (RAGT) is widely used in children with cerebral palsy (CP), but information about optimal intervention frequency and duration is still lacking and the current evidence about effect of RAGT on motor endurance and fitness is very preliminary.

Objective:

To investigate the effect of RAGT on motor performance and endurance in children affected by CP.

Methods:

Data from 14 consecutive children (6 females, age range: 4.6–15.8 years) affected by CP, who underwent a multidisciplinary rehabilitation program during a 18–24 month period, were retrospectively collected. Rehabilitation program included conventional physical therapy and RAGT (60/60 minutes, 20 daily sessions, 5 days/week). CP severity was stratified according to the Gross Motor Function Classification System. Clinical evaluation was performed by means of the six-minute walking test, the modified Ashworth scale, and RAGT measures (total distance, mean distance for session and speed).

Results:

Clinical outcomes and speed did not improve after treatment, while total distance (p = 0.006) and mean distance for session (p = 0.007) significantly improved.

Conclusions:

Our preliminary study suggests that RAGT combined with conventional treatment may improve motor performance and endurance in children with CP. Future randomized controlled trials comparing RAGT to conventional treatment are needed.

Keywords

Robotic gait training cerebral palsy endurance neurorehabilitation outcome

1. Introduction

Cerebral palsy (CP) includes a number of neurological conditions secondary to non-progressive brain injury that occurred in the developing fetal or infant brain, and result in abnormal development of movement and postural control often accompanied by seizures and disturbances in sensation, cognition, communication, perception, and/or behavior (Rosenbaum et al., 2007).

Typically, motor impairment of children with CP is heterogeneous and characterized by muscle weakness, spasticity, and reduced ability to achieve selective motor control that together cause abnormal biomechanical alignment and reduction in the performance of activities of daily living and participation (van den Berg-Emons et al., 1995; Sanger et al., 2003; Deon & Gaebler-Spira, 2010). Some studies showed that, compared to their healthy peers, children affected by CP have a decreased level of daily physical activity and do not use their physical reserves sufficiently during the day to achieve optimal levels of performance (van den Berg-Emons et al., 1995).

Specifically, improvement or maintenance of the ability to walk and/or higher level of physical fitness represent key components for well-being and a priority for many children with CP and their parents (Dickinson, 2007; Vargus-Adams, 2011; Beveridge, 2015), as well as one of the main rehabilitative goals (Rimmer, 2001).

During the last 15 years, different approaches have been proposed with the aim to improve motor performances in children with CP, such as the cyclo-ergometers (Calmels et al., 2011; Jin et al., 2012) or the treadmill training with or without body weight support (Provost et al., 2007). In the same period, new robotic technologies (e.g. driven gait orthoses for robot-assisted gait training, RAGT and over ground exoskeleton) have been originally developed for adults and subsequently adapted for children (Colombo et al., 2000; Hesse et al., 2003; Meyer-Heim et al., 2007; Bayón et al., 2016; Lefman et al., 2017).

A number of studies explored RAGT associated with conventional therapies in the pediatric neurorehabilitation setting (Papathanasiou et al., 2016; Wallard et al., 2017), and showed this approach to be a feasible and safe therapeutic option to improve motor performances (Meyer-Heim, 2007; Borggraefe, 2010; Peri, 2017). However, information about optimal intervention frequency and duration is still lacking and the current evidence about the clinical effectiveness of RAGT in pediatric population is still vague and inconclusive (Aurich-Sculer, 2015; Lefmann, 2017), in particular in children with poor chances of recovery or improvement. The aim of this retrospective exploratory study was to investigate the effects of RAGT on motor performance and endurance in a group of children affected by CP.

2. Materials and methods

2.1. Subjects

Data from 14 children affected by CP and consecutively referred to a rehabilitation outpatients service between December 2012 and August 2016 were retrospectively collected.

Inclusion criteria were: children aged 4–18 years, diagnosis of CP, indication to perform robotic rehabilitation by means of an exoskeleton, ability to follow instructions and to communicate discomfort or pain.

Exclusion criteria were: neurosurgery or orthopedic surgery within the last 6 months, previous exoskeleton training within the last 6 months, any contraindication to RAGT such as severe contractures (i.e. >20° knee extension deficit, >40° hip extension deficit), bone fractures, open skin lesions or vascular disease.

The study fulfilled the ethical principles of the Declaration of Helsinki, and all the subjects and parents received explanations regarding the purpose and procedures of the study. All parents signed an informed consent before the enrollment.

2.2. Measures

Before starting the rehabilitation program, each patient underwent a complete medical and functional examination, and a collection of anthropometric data. To obtain a functional categorization of the patients, the Gross Motor Function Classification System (GMFCS; Palisano et al., 1997) was used. The GMFCS explores activities such as sitting, walking and the use of mobility devices to categorize children with CP into five different levels of functioning, with level I as the best performance.

Study outcomes included clinical scales and RAGT measures that were measured at T0 (i.e., the week before starting rehabilitation) and T1 (i.e., one week after the end of rehabilitation program).

The following standardized clinical scales were applied.

The six-minute walk test (6MWT) assesses the distance walked over 6 minutes as a sub-maximal test of aerobic capacity/endurance (Geiger et al., 2007) and was performed on a 30-meter long corridor with poles at each end.

The modified Ashworth scale (Bohannon & Smith, 1987) was developed to assess the effects of pharmacological interventions on spasticity in multiple sclerosis, then used to measure spasticity in patients with other central nervous system conditions. It is scored from 0 (no increase in muscle tone) to 4 (affected part is rigid in flexion or extension). In the modified version, a 1+ scoring category was added to indicate resistance through less than half of the movement. Thus, scores range from 0 to 4 with 6 possible levels.

RAGT measures included the mean distance for session, the total distance within each rehabilitation program (20 sessions) and the maximal working speed used.

2.3. Rehabilitation program

Each patient performed a multidisciplinary rehabilitation program, consisting of 120 minutes daily sessions designed as follows: conventional physical therapy (60 minutes) and RAGT (60 minutes), the latter performed with an exoskeleton robotic device.

Conventional therapy included passive/active joint mobilization, muscle stretching, exercises for trunk stability, postural exercises in sitting/standing position, postural variation and transfer.

The total duration of the rehabilitation program was five days a week for four weeks accounting for 20 sessions. A maximum of two programs were administered to each patient within the 18–24 months observation period.

2.4. Robotic-assisted gait training

The exoskeleton used in this study was the Lokomat^® Nanos (Hocoma AG, Volketswil, Switzerland) that is composed of two actuated orthoses attached to the child’s limbs by means of cuffs and straps. The geometry (hip width, length of the upper and lower limbs) of the orthoses, and the size and position of leg cuffs were adjusted to the subject’s individual anthropometry, ensuring that walking in the device was as natural and comfortable as possible (Colombo et al., 2000). The hip and knee joints of the Lokomat are actuated by linear drives that move the orthoses through the gait cycle in the sagittal plane (Colombo et al., 2000; Duschau-Wicke et al., 2010; Riener et al., 2010), and guide the child’s limbs to move along a predefined path based on joint movements and derived from trajectories of healthy walkers.

The level of guidance provided by the Lokomat exoskeleton may be set by the therapist through an impedance controller that determines how much limb movements may deviate from the predefined pattern. In the present study, the level of guidance during the ‘Lokomat guided walking’ condition was set to 50%, which allows small deviations and requires more active involvement of the walker compared to fully guided walking.

2.5. Statistical analysis

Data were analyzed using SPSS version 16.0 software. Data are reported as mean and standard deviation. T1–T0 comparisons were tested by means of Wilcoxon Signed-Rank Test. Significance was set at p < 0.05 (two-tailed).

3. Results

Demographic and clinical features for each patient, including GMFCS score, previous surgery, and previous treatments with botulinum toxin, are reported in Table 1. All the patients showed tetraplegia, except for one patient (patient 3) who presented paraplegia. Four patients (patients 3, 7, 9, and 14) showed modified Ashworth scale >2 in at least two segments of the lower limbs (i.e. hip, knee or ankle).

Table 1
Patients clinical features and RAGT measures

Pt	Sex	Age T0	Age T1	Height (cm)		Type	GMFCS	Surgery	BoNT	Total distance (m)		Mean distance (m)		Speed (Km/h)
Pt	Sex	Age T0	Age T1	Height (cm)		Type	GMFCS	Surgery	BoNT	T0	T1	T0	T1	T0	T1
1	M	12.2	13.2	130	Tetraplegia	Hypertonic/Dystonic	III			15,436	15,388	965	943	1.9	1.8
2	M	4.6	5.8	116	Tetraplegia	Hypertonic	V			14,229	14,687	837	864	1.6	1.7
3	F	4.8	6.0	117	Paraplegia	Hypertonic #	I	•	•	16,281	17,381	814	869	1.6	1.7
4	M	5	6.9	110	Tetraplegia	Hypertonic	III	•		15,710	15,716	786	798	1.5	1.5
5	M	9.8	10.9	165	Tetraplegia	Hypertonic	I			22,502	22,504	1072	1123	2.1	2.1
6	M	7.6	9.0	100	Tetraplegia	Hypertonic	II			15,860	17,403	793	870	1.6	1.6
7	F	5.0	6.0	120	Tetraplegia	Hypertonic #	II	•	•	15,648	18,753	824	987	1.6	1.9
8	M	9	10.0	115	Tetraplegia	Hypertonic	V		•	13,354	13,672	668	684	1.4	1.3
9	M	8	9.0	140	Tetraplegia *	Hypertonic #	IV	•	•	15,948	16,814	886	934	1.7	1.7
10	F	15.8	17.2	118	Tetraplegia	Hypertonic	III			14,721	14,729	736	812	1.5	1.5
11	M	6.6	8.0	110	Tetraplegia	Hypertonic	IV		•	14,412	15,371	759	809	1.6	1.5
12	F	8.6	10.3	110	Tetraplegia	Hypertonic	I			15,950	15,954	798	798	1.6	1.6
13	F	8.3	9.3	144	Tetraplegia	Hypertonic	I			17,138	22,372	902	1177	1.8	2.2
14	F	8	9.0	150	Tetraplegia	Hypertonic #	III		•	17,322	20,100	866	1005	1.7	2.0

GMFCS: Gross Motor Function Classification System; BoNT: treated with botulinum neurotoxin injections. ^*Patient was treated with intrathecal baclofen infusion. ^#Patients who showed modified Ashworth scale >2 in at least two segments of the lower limbs.

The mean age was 8.1±3.1 (range 4.6–15.8) years at T0, and 9.3±3.1 (range 5.8–17.2) years at T1.

No clinically significant change in the modified Ashworth scale severity was found between T0 and T1. No statistically significant difference was found in 6 MWT when comparing T1 vs. T0 for those patients who were able to walk without aids (n = 6). At T0, mean 6 MWT distance was 366.7±39.2 m for children functioning at GMFCS level I (n = 4) and 316.7±25.88 m for those with GMFCS level II (n = 2). At T1, mean 6 MWT distance was 363.8±35.5 m for children with GMFCS level I (p = 0.91 for T1 vs. T0 comparison) and 319.3±27.1 m for those with GMFCS level II (p = 0.91).

When comparing T1 to T0, we found a significant change for mean total distance (T0:15,562±1,262 m, T1:17,181±2,806 m; p = 0.006), and mean distance for session (T0:831.4±82.2 m, T1:895.3±134.7 m; p = 0.007), but no significant change for speed (T0:1.7±0.1 Km/h; T1:1.7±0.3 Km/h; p = 0.07).

4. Discussion

To our knowledge, this is the first study that investigated the effects of RAGT on motor performance and endurance in children affected by CP.

Data showed a significant improvement in the mean distance for session and in the mean total distance between T0 and T1, which differed on average 1.2 years.

In this brief report we used indirect indices to quantify motor endurance of patients. This outcome is usually neglected by research on robotic rehabilitation that mainly focuses on other measures of motor performance. However, adequate levels of physical activity or physical fitness are usually recommended in healthy subjects to reach psychological and physiological benefits (Warburton et al., 2006; Trost, 2017). Indeed, in children affected by CP, an active lifestyle is recommended to optimize and maintain physical performance in daily life (Rimmer, 1999) and prevent the development of secondary health problems, such as weight gain, diabetes, and hypertension, later in life (Crespo, 1999). Based on these considerations, RAGT or a similar robotic treatment could be considered in those subjects who were unable to perform an active lifestyle.

In the management of CP, the children characteristics relating to primary impairments, those related to secondary impairments, as well as the interactions between child personality, family ecology, and the health care services, should all be considered (Bartlett and Palisano, 2000). This is particularly true for motor endurance and fitness, whose improvement can modify the quality of life, as reported by many studies on this issue (Fragala-Pinkham et al., 2005; Haney et al., 2014; Maltais et al., 2014).

The main limitations of the present study include its retrospective design, the small sample, and the absence of a control group who underwent conventional treatment but no RAGT. Moreover, metabolic measures, such as oxygen consumption, are lacking, since we considered only indirect measures of endurance.

Data from this study should be considered as exploratory, but they may offer some support for future studies, including randomized controlled trials, to explore the role of RAGT within a multidisciplinary rehabilitation treatment and to compare it to conventional treatment for fitness and endurance in children with CP. Whether virtual reality associated with RAGT (Calabrò et al., 2017) may further improve the outcome in this specific populations of patients should also be tested.

Declaration of interest

The authors report no conflict of interest.

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