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. 2021 Dec 30;70(Suppl 3):S397–S408. doi: 10.33549/physiolres.934840

Gait Changes Following Robot-Assisted Gait Training in Children With Cerebral Palsy

Dragana ŽARKOVIĆ 1,✉, Monika ŠORFOVÁ 1, James J TUFANO 2, Patrik KUTÍLEK 3, Slávka VÍTEČKOVÁ 4, David RAVNIK 5, Katja GROLEGER-SRŠEN 6, Imre CIKAJLO 7, Jakub OTÁHAL 8
PMCID: PMC8884401  PMID: 35099258

Summary

This study investigated changes of gait pattern induced by a 4-week robot-assisted gait training (RAGT) in twelve ambulatory spastic diparesis children with cerebral palsy (CP) aged 10.4±3.2 years old by using computerized gait analysis (CGA). Pre-post intervention CGA data of children with CP was contrasted to the normative data of typically developing children by using cross-correlation and statistically evaluated by a Wilcoxon test. Significant pre-post intervention changes (p<0.01) include: decreased muscle activity of biceps femoris, rectus femoris, and tibialis anterior; a decrease in range of internal hip joint rotation, higher cadence, step length, and increased stride time. This study suggests that RAGT can be used in muscle reeducation and improved hip joint motion range in ambulatory children with CP.

Keywords: Cerebral palsy, Spastic diparesis, Gait cycle, Computerized gait analysis, Robot-assisted gait training

Introduction

Cerebral palsy

Cerebral palsy (CP) is a developmental disability that was first described in the 1840s, yet continues to be one of the most frequent pediatric disabilities with an incidence of 2–3 per 1000 children (Bax et al. 2005, Panteliadis 2004). Most physiotherapy approaches aim to improve movement quality and develop skills necessary to carry out activities of daily living, which often include tasks such as standing and walking (Novak 2014).

Robot-assisted gait training (RAGT)

Although manual assistance can be used to aid children with CP, RAGT allows for more advanced and customizable gait rehabilitation programs. RAGT was introduced 15 years ago and consists of bilateral robotic orthoses, body-weight support (BWS), and a treadmill. Being a computerized system, it is possible to adjust the amount of BWS to maintain extended posture and provide accurate loading of the lower limbs. The robotic orthoses guide a patient’s leg movements throughout repeatable predefined trajectories of the hip- and knee-joints in the sagittal plane, and foot supports maintain passive ankle dorsiflexion, which can aid CP children while walking (Colombo et al. 2000, Riener et al. 2005, Meyer-Heim et al. 2007). The main aim of RAGT is to improve the motor learning process through repetitive stimulation of gait accompanied by audio-visual feedback (Schuler et al. 2011). RAGT provides a simplified and safe therapeutic environment that allows for prolonged training duration with many repetitions of steps while inducing a reproducible, kinematically consistent, symmetrical gait pattern (Colombo et al. 2000). RAGT seems to be a promising method for children with CP in improved selective voluntary motor control (Žarković et al. 2020), increased muscle activity, and inter limb symmetry (Schuler et al. 2011, Schuler et al. 2013, Bonikowski et al. 2012), restricted passive joint range of motion (Vrečar et al. 2013, Žarković et al. 2020), and improved gross motor abilities including improved spatiotemporal gait parameters (Meyer-Heim et al. 2007, Borggraeffe et al. 2010, Knecht et al. 2010, Žarković et al. 2020). Despite that, it is still unknown whether functional motor improvements following RAGT can also contribute to the improved quality of gait patterns. Therefore, the purpose of this experimental study was to investigate changes in gait pattern following RAGT as a monotherapy in ambulatory spastic diparesis children with CP. Knowing that motor learning is critical for neuroplasticity and that children with CP can improve motor function with practice (Hemayattalab et al. 2010, Gordon et al. 2012, Hemayattalab et al. 2013), we hypothesized that RAGT can induce physiological gait changes in lower limbs that can be comparable to the healthy children.

Methods

Ethics Committee approval

The study received ethics committee approvals from participating institutions (No. 120/2015). The parents of the children were informed of the study procedures, risks, and benefits, and provided written informed consent before their children participating in the study.

Children with CP

Inclusion criteria were: CP spastic diparesis with toe walking pattern; Gross Motor Function Classification (GMFCS) I–III; ability to walk independently for at least short distances; age range 5–17 years; femur length at least 21 cm to fit in orthoses of RAGT device; ability to communicate fear, pain, or discomfort; ability to follow simple instructions; no botulinum toxin in the last 3 months before RAGT; no orthopedic surgical intervention in the last 12 months; no severe contractures; and ability to attend 20 RAGT sessions scheduled in 20 consecutive weekdays (Vrečar et al. 2013, Wallard et al. 2018).

Definition of limb impairment

Before the RAGT intervention, an experienced pediatric physiotherapist performed in all children a passive joint range of motion (PROM) goniometry evaluation of lower limbs (Janda et al. 1993), and the Selective Control Assessment for the Lower Extremity (SCALE) (Fowler et al. 2009). SCALE and PROM revealed “more impaired limb” (MIL) and “less impaired limb” (LIL), as well as evaluations excluded patients with severe joint contractures (Fowler et al. 2009, Syczewska and Świecicka 2016). These evaluations had an informatory purpose that was summarized in section results.

Data collection

Computerized gait analysis (CGA)

The CGA included a comprehensive 3D gait analysis consisting of joint kinematics, kinetics, sEMG, and spatiotemporal parameters. The CGA evaluation was performed by 2 well-trained physiotherapists and 2 biomechanics experts. First, the skin was gently abraded, and multi-purpose monitoring electrodes were placed on the following muscles bilaterally according to the SENIAM recommendations (Hermens et al. 1999): tibialis anterior (TA), medial gastrocnemius (MG), rectus femoris (RF), and biceps femoris (BF). A neutral reference electrode was attached to the tensor fascia latae muscle (Schuler et al. 2011). Subsequently, 17 reflective markers (Vicon, Oxford Metrics, Oxford, UK) were attached directly to the skin to ensure a fixed and precise position. Markers were attached bilaterally to the following body areas concerning the Vicon Plug-in-gait model (Davis et al. 1991, Dixon et al. 2014, Flux et al. 2020): second metatarsal joint; middle of the Achilles tendon; malleolus lateralis; center of the tibia; lateral femoral epicondyle; lateral side of the thigh; spina iliaca anterior superior (SIAS); L5; Th10; sternum. All children with CP were told to walk barefoot in the pre-designed 10-meter flat-surface pathway to adapt to space. Afterward, children with CP were appealed to walk barefoot without walking aids at preferred speed and according to physical capacities for a minimum of ten trials on the same pre-designed 10-meter flat-surface pathway in the gait laboratory. Kinematics, kinetics, and sEMG data were collected and recorded simultaneously. 3D kinematic data was recorded by using a 6-camera VICON system (0.3 MPix VICON, Oxford Metrics, Oxford, UK) with a sampling frequency of 50 Hz until the course of three completed trials was obtained. Kinetics was recorded by using AMTI force plates (AMTI OR6, Advanced Mechanical Technology Inc., Watertown, MA) at 1 kHz sampling frequency. Muscle activity was recorded with an 8-channel sEMG sampling frequency at 1 kHz (Noraxon TeleMyo 2400T, Noraxon U.S.A. Inc.).

RAGT intervention

The RAGT device Lokomat Pro (Hocoma AG, Volketswil, Switzerland) was used. The intervention consisted of twenty sessions scheduled for 20 consecutive workdays with a minimum duration of 30 and up to a maximum of 45 min (Vrečar et al. 2013, Wallard et al. 2017). The treadmill speed was synchronized with the movements of the robotic orthoses and set to a comfortable walking speed of every child individually. These parameters were set by following the child’s ability to walk at a certain speed, follow the augmented feedback and maintain an upright posture. All children wore shoes during the RAGT. At the beginning of RAGT program, all children had an initial level of BWS set to 50 % of body weight (Schuler et al. 2013). The BWS was further decreased for every child individually until the knee started to collapse into flexion during the stance phase due to the increased load of body weight. All children walked with augmented biofeedback (Schuler et al. 2011, Schuler et al. 2013, Wallard et al. 2017). For consistency, the same physiotherapist was present at every RAGT session to follow the progression and encourage the child to walk actively and keep an extended posture (Fig. 1).

Fig. 1.

Fig. 1

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A 5-year-old boy with spastic diparesis during RAGT using the Lokomat Pro.

Data evaluation
Data processing

Raw CGA data obtained from overground gait was high-pass filtered by the VICON system (VICON Nexus 1.8.3.) to enable analog data sampling with 1 kHz, and subsequently filtered with a 4th order low-pass Butterworth filter with a cut off frequency of 20 Hz (Kadaba et al. 1989, Baker 2013). The data was normalized and the Vicon Plug-in-Gait model was used to generate kinematic and kinetic data (Davis et al. 1991). Joint angles were calculated based on the 3D coordinates of markers. Internal joint moments and power were calculated based on joint kinematics and ground reaction forces recorded using force plates (Kadaba et al. 1989, MacWilliams et al. 2003, Baker 2013). Force plates measured ground reaction forces and center of pressure (COP) trajectory (Baker 2013). VICON Nexus 1.8.3. and Polygon 3.5.1. softwares (VICON, Oxford Metrics, Oxford, UK) were used to define the gait cycles, spatiotemporal parameters, joint angles, internal joint moments, and power. sEMG data was processed by MyoResearch XP 1.07 Master Edition software (Noraxon Inc., Scottsdale/USA). Raw sEMG signals were high-pass filtered with a bi-directional zero-lag Butterworth at a cut-off frequency of 10 Hz, rectified, and smoothed with a time window of 100 ms to create the linear envelope. The sEMG data was normalized to the maximum EMG recorded during the gait cycle (Fung et al. 1989, Burden and Bartlett 1999, Burden et al. 2003, Bojanic et al. 2011, Aurich-Schuler 2017, Ricklin et al. 2018). As subjects walked for a minimum of ten trials, gait cycles were identified in each trial. Heel strike and toe-off markers were set automatically by the software program and adjusted manually if necessary. The gait cycle starts and ends with a heel strike of the same lower extremity (Perry 2010, Baker 2013). Within the cycles, the mean value of these trials was calculated to obtain 1 gait cycle and separate gait phases. The gait cycle was represented by 51 evenly spaced samples (0–100 % in 2 % steps) that were marked as initial contact (IC), loading response (LR), midstance (MST), terminal stance (TS), pressing (PSW), initial swing (ISW), midswing (MSW), terminal swing (TSW) (Perry et al. 2010). This study aimed to explore whether RAGT can induce physiological gait changes in lower limbs that will be comparable to healthy children. Therefore, all collected CGA variables were contrasted to the normative data (Sutherland 2002, Hof et al. 2005, Winter et al. 2009) assessed in typically developing children, and differences in individual phases of the gait cycle (Perry 2010) were examined to explain the pathological gait mechanism and compensatory movements. Normative data represent an integral part that is built in VICON and Myoresearch softwares. Subsequently, data was used for statistical evaluation by using a custom-written MatLab program (MatLab software processes, MatLab R2010b, Mathworks, Inc., Natick, MA, USA).

Statistical evaluation

Comprehensive CGA resulted in a statistical evaluation of 43 variables embracing sEMG; motion range of thorax, pelvis, hip, knee, and ankle joints in all three planes; joint moments in sagittal/ frontal planes and power of hip, knee, and ankle joints; center of pressure, center of mass and ground reaction forces in all three planes. First, the deviation of CP signals from the normative values was calculated by cross-correlation for every variable and particular phases of the gait cycle. It was performed for LIL and MIL separately pre- and post-intervention. The statistical evaluation was performed to compare the pre- and post-intervention conditions of children with CP. The Shapiro-Wilk test was used to verify data normality. As normal data distribution has been rejected at the 0.05 significance level, the non-parametric Wilcoxon sign rank test was used for further statistical calculation of each variable and gait cycle phase separately (0.05 significance level). The calculation was completed by Bonferroni correction (p<0.01), median values and effect sizes of cross-correlation coefficients (Cohen 1988).

Results

Children with CP

Twelve CP children with spastic diparesis (2 girls; 10 boys) with apparent equinus gait pattern; aged 10.4±3.2 years; GMFCS I–III; with decreased selective voluntary motor control of lower extremities as per SCALE evaluation (total score MIL 5, total score LIL 7 out of max. score 10), and with hip-knee-ankle joint contractures (≤10° for both extremities) completed the RAGT program. The program was well-tolerated by all of the children with CP and no adverse events were reported.

CGA results

Significant improvements contrasted to the normative data were found in bilaterally decreased activity of BF, RF, TA muscles and decreased internal hip joint rotation. There were no significant changes in kinetic variables. Spatiotemporal parameters showed increased cadence and step length, and decrease in time needed for double support and stride. A detailed summary of results is shown in Tables 1–3.

Table 1.

Table shows an overview of Wilcoxon sign rank tests for CGA variables with corrected p-value, median values and effect sizes of cross-correlation coefficients. Statistically significant results (p≤0.01) are bolded and marked with an asterisk (*).

sEMG Gait cycle phases
p-value after Bonferroni correction/effect size of cross-correlation coefficient
IC LR MST TS PSW ISW MSW TSW
BF MIL <0.01/0.54 <0.01/0.52 <0.01 * /0.56 <0.01 * /0.57 <0.01 * /0.56 <0.01/0.51 <0.01/0.52 <0.01 * /0.56
BF LIL <0.01/0.50 <0.01/0.47 <0.01/0.52 <0.01 * /0.57 <0.01/0.36 <0.01 * /0.62 <0.01/0.52 <0.01 * /0.57
RF MIL <0.01 * /0.59 <0.01 * /0.57 <0.01 * /0.62 <0.01 * /0.59 <0.01 * /0.62 <0.01/0.51 <0.01 * /0.56 <0.01 * /0.60
RF LIL <0.01 * /0.59 <0.01 * /0.60 <0.01 * /0.60 <0.01 * /0.62 >0.01/0.20 <0.01/0.43 <0.01/0.43 <0.01/0.51
MG MIL <0.01/0.46 <0.01/0.35 <0.01/0.43 <0.01/0.44 <0.01/0.43 <0.01/0.35 <0.01/0.48 <0.01/0.44
MG LIL <0.01/0.39 >0.01/0.36 >0.01/0.35 <0.01/0.41 >0.01/0.38 <0.01/0.52 <0.01/0.52 <0.01/0.40
TA MIL <0.01/0.46 <0.01/0.48 <0.01/0.35 <0.01/0.38 <0.01/0.43 <0.01/0.40 <0.01/0.28 <0.01/0.43
TA LIL <0.01 * /0.59 <0.01 * /0.62 <0.01 * /0.60 <0.01 * /0.62 <0.01/0.54 <0.01/0.54 <0.01/0.44 <0.01/0.52
Kinematics IC LR MST TS PSW ISW MSW TSW
Pelvic tilt MIL >0.01/0.19 >0.01/0.17 >0.01/0.11 >0.01/0.16 >0.01/0.17 >0.01/0.20 >0.01/0.20 >0.01/0.20
Pelvic tilt LIL >0.01/0.19 >0.01/0.19 >0.01/0.19 >0.01/0.20 >0.01/0.17 >0.01/0.12 >0.01/0.14 >0.01/0.19
Pelvic obliquity MIL 1/0 >0.01/0.01 >0.01/0.20 >0.01/0.35 <0.01/−0.44 >0.01/−0.25 >0.01/−0.04 >0.01/−0.04
Pelvic obliquity LIL <0.01/0.43 >0.01/−0.32 >0.01/−0.19 >0.01/0.01 >0.01/0.06 >0.01/0.17 >0.01/0.35 <0.01/0.43
Pelvic rotation MIL >0.01/−0.09 >0.01/−0.08 >0.01/−0.22 >0.01/0.33 >0.01/0.28 >0.01/0.14 >0.01/0.04 >0.01/0.03
Pelvic rotation LIL >0.01/0.36 >0.01/0.28 >0.01/0.19 >0.01/−0.09 >0.01/−0.01 >0.01/−0.11 >0.01/−0.24 >0.01/−0.25
Hip flexion/ extension MIL >0.01/0.04 >0.01/0.04 >0.01/0.12 >0.01/0.09 >0.01/−0.20 >0.01/0.28 >0.01/0.25 >0.01/0.163
Hip flexion/ extension LIL >0.01/0.22 >0.01/0.25 >0.01/0.33 <0.01/0.44 >0.01/−0.24 >0.01/0.36 >0.01/0.36 >0.01/0.28
Hip abduction/ adduction MIL >0.01/−0.30 >0.01/0.24 >0.01/0.33 >0.01/0.22 >0.01/−0.28 >0.01 /−0.25 >0.01 /−0.22 >0.01/−0.24
Hip abduction/ adduction LIL >0.01/0.28 >0.01/−0.28 >0.01/−0.14 >0.01/−0.11 >0.01/−0.08 >0.01/−0.03 >0.01/−0.03 >0.01/0.19
Hip rotation MIL <0.01 * /0.57 <0.01 * /0.59 <0.01 * /0.62 <0.01 * /0.62 <0.01 * /0.62 <0.01 * /0.62 <0.01 * /0.59 <0.01 * /0.56
Hip rotation LIL >0.01/0.28 >0.01/0.32 <0.01 * /0.56 <0.01 * /0.56 <0.01 * /0.56 <0.01 * /0.56 <0.01 * /0.56 <0.01 * /0.56
Knee flexion/ extension MIL >0.01/−0.16 >0.01/−0.06 >0.01/−0.19 >0.01/−0.27 >0.01/−0.11 >0.01/−0.38 >0.01/−0.24 >0.01/−0.24
Knee flexion/ extension LIL >0.01/0.08 >0.01/0.08 >0.01/0.08 >0.01/0.17 >0.01/0.08 >0.01/0.03 >0.01/−0.04 >0.01/−0.01
Knee abduction/ adduction MIL <0.01/0.43 <0.01/0.43 <0.01/0.40 >0.01/0.33 <0.01/0.43 <0.01/−0.48 <0.01/0.46 <0.01/0.48
Knee abduction/ adduction LIL >0.01/0.22 >0.01/0.22 >0.01/0.27 >0.01/0.09 >0.01/0.25 >0.01/−0.38 >0.01/0.33 <0.01/0.43
Ankle plantar/ dorsal flexion MIL >0.01/0.24 >0.01/0.20 >0.01/0.14 1/0 >0.01/−0.04 >0.01/0.28 >0.01/0.28 >0.01/0.03
Ankle plantar/ dorsal flexion LIL >0.01/0.11 >0.01/0.14 >0.01/−0.01 >0.01/−0.19 >0.01/−0.19 >0.01/0.12 >0.01/0.22 >0.01/0.09
Foot tilt MIL >0.01/−0.21 >0.01/−0.18 >0.01/−0.16 >0.01/0.06 >0.01/0.14 >0.01/−0.04 >0.01/−0.24 >0.01/−0.25
Foot tilt LIL >0.01/0.32 >0.01/0.35 >0.01/0.38 >0.01/0.30 >0.01/0.16 >0.01/0.16 >0.01/0.04 >0.01/0.22
Foot progress MIL <0.01/0.50 <0.01/0.49 <0.01 * /0.56 <0.01 * /0.57 <0.01 /0.49 <0.01 /0.51 <0.01/0.44 <0.01/0.40
Foot progress LIL <0.01 * /0.56 <0.01/0.54 <0.01/0.46 <0.01/−0.60 <0.01/−0.62 >0.01/−0.38 >0.01/−0.32 <0.01/−0.43
Thorax tilt MIS * <0.01/0.39 <0.01/0.39 <0.01/0.39 <0.01/0.46 <0.01/0.48 <0.01/0.48 <0.01/0.41 <0.01/0.43
Thorax tilt LIS * <0.01/0.44 <0.01/0.44 <0.01/0.43 <0.01/0.43 <0.01/0.43 <0.01/0.44 <0.01/0.46 <0.01/0.44
Kinetics IC LR MST TS PSW ISW MSW TSW
Hip flexion/ extension moment MIL >0.01/−0.14 >0.01/−0.46 >0.01/−0.35 >0.01/−0.12 >0.01/0.09 >0.01/0.19 >0.01/−0.28 >0.01/−0.05
Hip flexion/ extension moment LIL >0.01/0.19 >0.01/−0.30 >0.01/0.04 >0.01/0.03 >0.01/−0.16 >0.01/−0.09 >0.01/0.48 >0.01/0.01
Hip abduction/ adduction moment MIL >0.01/0.22 >0.01/−0.17 >0.01/−0.01 >0.01/−0.04 1/0 1/0 >0.01/−0.08 >0.01/−0.07
Hip abduct-tion/adduction moment LIL >0.01/0.27 >0.01/−0.14 >0.01/−0.09 >0.01/−0.09 >0.01/0.11 >0.01/−0.06 >0.01/−0.20 1/0
Hip power MIL >0.01/−0.01 >0.01/0.16 >0.01/−0.08 >0.01/0.08 >0.01/0.22 >0.01/0.21 >0.01/0.01 >0.01/0.36
Hip power LIL >0.01/0.38 >0.01/0.23 >0.01/0.30 >0.01/−0.24 >0.01/−0.30 >0.01/−0.11 >0.01/0.09 >0.01/0.25
Knee flexion/ extension moment MIL >0.01/−0.51 >0.01/−0.17 >0.01/−0.20 >0.01/0.35 >0.01/−0.11 >0.01/−0.09 >0.01/0.04 >0.01/−0.35
Knee flexion/ extension moment LIL >0.01/−0.28 >0.01/−0.52 >0.01/−0.38 >0.01/0.32 >0.01/−0.25 >0.01/−0.20 >0.01/0.09 >0.01/−0.08
Knee valgus/ varus moment MIL >0.01/0.06 >0.01/−0.20 >0.01/−0.38 >0.01/0.06 >0.01/−0.12 >0.01/0.41 >0.01/0.12 >0.01/0.24
Knee valgus/ varus moment LIL >0.01/−0.36 >0.01/−0.01 >0.01/−0.03 >0.01/−0.03 >0.01/0.19 >0.01/−0.14 >0.01/−0.33 >0.01/−0.22
Knee power MIL >0.01/−0.16 >0.01/0.14 >0.01/0.06 >0.01/−0.14 >0.01/−0.13 >0.01/−0.21 >0.01/0.04 >0.01/0.25
Knee power LIL >0.01/−0.01 >0.01/−0.05 >0.01/−0.14 >0.01/−0.28 >0.01/0.29 >0.01/0.36 >0.01/0.01 >0.01/−0.14
Ankle flexion/ extension moment MIL >0.01/−0.08 >0.01/0.04 >0.01/−0.12 >0.01/−0.20 >0.01/0.16 >0.01/0.27 >0.01/−0.20 >0.01/−0.28
Ankle flexion/ extension moment LIL >0.01/0.09 >0.01/0.27 >0.01/−0.01 >0.01/−0.25 >0.01/0.03 >0.01/0.11 >0.01/0.09 >0.01/−0.19
Ankle power MIL >0.01/−0.06 >0.01/−0.41 >0.01/−0.12 >0.01/−0.17 >0.01/−0.03 >0.01/−0.13 >0.01/−0.14 >0.01/−0.09
Ankle power LIL >0.01/0.22 >0.01/−0.01 >0.01/0.12 >0.01/−0.08 >0.01/−0.47 >0.01/0.15 >0.01/−0.14 >0.01/0.04
GRF X MIL >0.01/−0.09 >0.01/−0.30 >0.01/−0.16 >0.01/−0.30 >0.01/0.28
GRF X LIL 1/0 >0.01/−0.32 >0.01/−0.28 >0.01/−0.24 >0.01/−0.25
GRF Y MIL >0.01/−0.16 >0.01/−0.16 >0.01/0.24 >0.01/0.22 >0.01/0.17
GRF Y LIL >0.01/−0.03 >0.01/0.14 >0.01/0.06 >0.01/−0.14 >0.01/−0.03
GRF Z MIL >0.01/0.14 >0.01/0.12 >0.01/−0.01 >0.01/0.12 >0.01/0.11
GRF Z LIL >0.01/0.05 >0.01/0.23 >0.01/0.17 >0.01/−0.01 >0.01/−0.49
COM MIL >0.01/0.05 >0.01/0.01 >0.01/0.24 >0.01/0.09 >0.01/0.03
COM LIL >0.01/0.16 >0.01/0.14 >0.01/0.08 >0.01/0.06 1/0
COP X MIL >0.01/0.12 >0.01/−0.03 1/0 >0.01/−0.24 >0.01/−0.03
COP X LIL >0.01/0.03 >0.01/0.03 >0.01/0.04 >0.01/0.01 >0.01/−0.02
COP Y MIL >0.01/−0.32 >0.01/−0.38 >0.01/−0.30 >0.01/−0.22 >0.01/−0.24
COP Y LIL >0.01/0.18 >0.01/−0.11 >0.01/−0.30 >0.01/−0.22 >0.01/−0.25
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sEMG (surface electromyography); BF (biceps femoris); RF (rectus femoris); TA (tibialis anterior); MG (medial gastrocnemius); MIL (More impaired limb); LIL (Less impaired limb); IC (Initial contact); LR (Loading response); MST (Midstance); TS (Terminal stance); PSW (Preswing); ISW (Initial swing); MSW (Midswing); TSW (Terminal swing).

Table 2.

Table shows an overview of Wilcoxon sign rank tests for spatiotemporal parameters with corrected p-value and median values. Statistically significant results (p≤0.01) are bolded and marked with an asterisk (*).

Spatiotemporal parameters Median MIL pre Median MIL post MIL p-value/ effect size Median LIL pre Median LIL post LIL p-value/ effect size
Cadence (steps/min) 109.04 111.57 <0.01 * /0.62 109.55 112.45 <0.01 * /0.61
Double support (s) 0.36 0.34 <0.01 * /0.63 0.37 0.33 <0.01 * /0.62
Foot off (%) 64.35 64.19 <0.01/0.52 65.04 64.97 <0.01 * /0.61
Opposite foot contact (%) 48.48 48.91 >0.01/0.04 51.67 51.18 >0.01/0.04
Opposite foot off (%) 13.87 13.59 >0.01/0.04 16.66 15.08 >0.01/0.04
Single support (s) 0.39 0.39 >0.01/0.06 0.39 0.39 >0.01/0.04
Step length (m) 0.43 0.46 <0.01 * /0.61 0.43 0.45 <0.01 * /0.60
Step time (s) 0.6 0.58 >0.01/0.05 0.55 0.54 >0.01/0.05
Step width (m) 0.11 0.12 >0.01/0.05 0.11 0.12 >0.01/0.05
Stride length (m) 0.87 0.85 <0.01/0.52 0.87 0.83 <0.01/0.52
Stride time (s) 1.16 1.13 <0.01 * /0.59 1.16 1.12 <0.01 * /0.59
Walking speed (m/s) 0.8 0.87 <0.01/0.52 0.81 0.86 <0.01/0.52
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MIL (More impaired limb); LIL (Less impaired limb).

Table 3.

Table shows an overview of median values for cross-correlation coefficients for CGA variables that were statistically significant (p≤0.01). This optimization was done due to an extensive amount of variables.

EMG Median of cross-correlation Kinematics Median of cross-correlation
Before After Before After
BF MIL MST 1.57E-07 9.74E-08 Hip rotation MIL IC −104.813168 −35.353415
BF MIL TS 4.19E-08 2.18E-08 Hip rotation MIL LR −407.577837 −131.401828
BF LIL TS 5.09E-08 2.63E-08 Hip rotation MIL MST −131.317739 −60.436948
BF MIL PSW 1.07E-08 5.36E-09 Hip rotation LIL MST −56.233293 −11.707981
BF LIL ISW 1.52E-08 1.10E-08 Hip rotation MIL TS −225.096715 −85.055612
BF MIL TSW 1.25E-07 7.77E-08 Hip rotation LIL TS −80.912522 −50.977734
BF LIL TSW 1.33E-07 9.78E-08 Hip rotation MIL PSW −198.098633 −91.203742
RF MIL IC 1.85E-08 1.07E-08 Hip rotation LIL PSW −91.927671 −61.537886
RF LIL IC 1.54E-08 1.15E-08 Hip rotation MIL ISW −100.699038 −35.898468
RF MIL LR 5.83E-08 3.50E-08 Hip rotation LIL ISW −46.63385 −33.898337
RF LIL LR 5.23E-08 4.10E-08 Hip rotation MIL MSW 568.936576 370.747144
RF MIL MST 8.21E-08 4.15E-08 Hip rotation LIL MSW 359.984115 161.270348
RF LIL MST 7.05E-08 5.33E-08 Hip rotation MIL TSW 256.714316 106.666952
RF MIL TS 2.30E-08 1.31E-08 Hip rotation LIL TSW 166.934347 12.34891
RF LIL TS 2.07E-08 1.37E-08 Foot progress LIL IC −53.74 7.65
RF MIL PSW 1.13E-08 6.67E-09 Foot progress MIL MST −80.71 14.77
RF MIL MSW 1.44E-08 9.01E-09 Foot progress MIL TS −81.67 265.39
RF MIL TSW 1.92E-08 1.23E-08
TA LIL IC 1.45E-07 8.02E-08
TA LIL LR 4.23E-07 2.14E-07
TA LIL MST 2.78E-07 1.57E-07
TA LIL TS 5.93E-08 4.08E-08
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sEMG (surface electromyography); BF (biceps femoris); RF (rectus femoris); TA (tibialis anterior); MG (medial gastrocnemius); MIL (More impaired limb); LIL (Less impaired limb); IC (Initial contact); LR (Loading response); MST (Midstance); TS (Terminal stance); PSW (Preswing); ISW (Initial swing); MSW (Midswing); TSW (Terminal swing).

Discussion

Interpretation of sEMG results

Since active training seems to be more effective than passive training for motor learning and cortical reorganization in central motor impairments, RAGT likely improved muscle activation of children with CP due to active training performed with a high-repetition-rate of guided movements (Meyer-Heim et al. 2009, Bonikowski et al. 2012, Aurich-Schuler 2017). Although this research study did not explore spasticity in children with CP, it could be one of the supportive explanations for why RAGT led to the decrease of muscle activity. Cyclic motion has been reported to be effective in decreasing spasticity in stroke patients (Monaghan 2017). In children with CP, the RF muscle tends to be shortened and spastic. This leads to hip joint flexion contractures that do not allow active and controlled knee extension during the stance phase (Foran 2005, Katz 1989, Schuler et al. 2011, Schuler et al. 2013). BF is typically weakened due to the dominant activity of the antagonist RF. Despite that in some children with CP this muscle can be spastic (Goldberg et al. 2012). Although our findings showed the bilaterally decreased activity of both muscles (Bonikowski et al. 2012) almost across all gait cycle phases, it is worth elaborating on increased number of treatments (e.g. up to 40) in a longer period of time such as in the study of Verazaluce-Rodriguez et al. (2014) to explore whether it is possible to induce even more physiological muscle activity. Children with CP often have spastic calf muscles, foot deformities and difficulties performing dorsiflexion and foot inversion resulting in a lack of TA activity (Brunner et al. 2008). In this study, TA muscle was active post-intervention during swing up to the loading response phases as previously shown in studies performed on healthy subjects (Brutsch et al. 2010, Schuler et al. 2013, Schuler et al. 2017). Thus, our findings further support that RAGT can enhance the physiological activity of TA, although the ankle joint during RAGT is only passively positioned to the neutral position (Colombo 2000). MG is a biarticular muscle often considered the main contributor to abnormal gait patterns as it causes Achilles tendon shortening which can result in contracture and foot deformities (Patikas et al. 2007, Perry 2010, Stewart et al. 2010). Therefore, if the MG muscle is influenced, either by stretching, relaxation, or positioning the affected joint in the neutral position, it can contribute to the increased range of motion in the ankle joint, as well as it can reciprocally allow the activation of the antagonist TA muscle (Katz et al. 1989, Colombo et al. 2000, Colombo et al. 2005). This is an interesting finding because it indicates that perhaps the active support and active movement of the proximal musculature may help encourage a similar adaptation in the distal musculature despite a lack of active support (Radziminska et al. 2012, Vrečar et al. 2013).

Interpretation of joint kinematics and kinetics results

Despite the lack of studies that explored the effect of RAGT on joint kinematics and kinetics in children with CP (Druzbicki et al. 2013, Schuler et al. 2017, Wallard et al. 2018), to the best of the authors’ knowledge, this is the first study reporting on changes that followed RAGT in hip joint rotations. It is assumed that RAGT likely decreased internal hip joint rotations due to a high repetition rate of guided movements in joint centered position of the pelvis and lower limbs (Kolář 2002, Žarković and Šorfová 2017). In conditions with impaired motor control, such as in children with CP, joints are in a so-called decentralized position that also contributes to improper muscle function. The centered joint position allows for optimal loading of the joint in both static and dynamic conditions, as well as it enhances physiological muscle patterns. This is an interesting finding because it indicates that the combination of task-specific guided movements in a high-repetition-rate, and centered position of joints resulted in a decreased pathological internal hip joint rotations in ambulatory children with CP. Although RAGT allows very detailed adjustment of gait parameters, it has a fixed strategy to control the motion trajectory of the robotic orthoses and pelvis, which are limited to one degree of freedom in the sagittal plane. Indeed, it is the absence of lateral weight shift to the standing limb, rotational pelvic movements and kinematic variability that may be the main causes of therapy irresponsiveness in lower limb kinematic and kinetic variables. This is also supported by studies that have found that lower limb and pelvic kinematic variability could facilitate the transfer of motor skills from robotic therapy to over-ground walking (Reinkensmeyer et al. 2006, Koopman et al. 2013, Wu et al. 2017).

Interpretation of spatiotemporal parameters

Definition of spatiotemporal parameters allows for an objective definition of where, when, how long, and how rapidly the individual is in contact with the ground (Perry 2010, Baker 2013, Armand et al. 2016). In this research study, the most important changes were observed in increased cadence and step length, and a decrease in time needed for double support and stride. This could potentially contribute to more economic gait pattern in ambulatory children with CP who need to walk farther distances. Similar findings were reported by Meyer-Heim et al. 2007, Knecht et al. 2010, Beretta et al. 2015.

Conclusions

Findings suggest that RAGT as monotherapy can contribute to muscle reeducation and improvement of hip joint motion range in ambulatory children with CP. This is the first research study that extended the explanation of RAGT by centered joint position. Authors are aware of study limitations such as the small sample size, lack of control group and long-term follow-up data. For that, there is no tendency to generalize the study results to a wider spectrum of the CP population. However, this research study provides a foundation on which future studies can be built as RAGT should be investigated over longer periods in different populations to further determine its effectiveness.

Acknowledgements

This study was funded by university student support FTVS SVV 2020–2022-260599 and institutional support “Progress Q41 2017–2021 biological aspects of the investigation of human movement” from Charles University, Prague, Czech Republic. Authors state that there is no conflict of interest.

Footnotes

Conflict of Interest

There is no conflict of interest.

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