Effect of rhythmic auditory cueing on gait in cerebral palsy: a systematic review and meta-analysis
Authors Ghai S, Ghai I, Effenberg AO
Received 2 August 2017
Accepted for publication 19 October 2017
Published 22 December 2017 Volume 2018:14 Pages 43—59
Checked for plagiarism Yes
Review by Single anonymous peer review
Peer reviewer comments 2
Editor who approved publication: Dr Roger Pinder
Shashank Ghai,1 Ishan Ghai,2 Alfred O. Effenberg1
1Institute for Sports Science, Leibniz University Hannover, Hannover, Germany; 2School of Life Sciences, Jacobs University, Bremen, Germany
Abstract: Auditory entrainment can influence gait performance in movement disorders. The entrainment can incite neurophysiological and musculoskeletal changes to enhance motor execution. However, a consensus as to its effects based on gait in people with cerebral palsy is still warranted. A systematic review and meta-analysis were carried out to analyze the effects of rhythmic auditory cueing on spatiotemporal and kinematic parameters of gait in people with cerebral palsy. Systematic identification of published literature was performed adhering to Preferred Reporting Items for Systematic Reviews and Meta-Analyses and American Academy for Cerebral Palsy and Developmental Medicine guidelines, from inception until July 2017, on online databases: Web of Science, PEDro, EBSCO, Medline, Cochrane, Embase and ProQuest. Kinematic and spatiotemporal gait parameters were evaluated in a meta-analysis across studies. Of 547 records, nine studies involving 227 participants (108 children/119 adults) met our inclusion criteria. The qualitative review suggested beneficial effects of rhythmic auditory cueing on gait performance among all included studies. The meta-analysis revealed beneficial effects of rhythmic auditory cueing on gait dynamic index (Hedge’s g=0.9), gait velocity (1.1), cadence (0.3), and stride length (0.5). This review for the first time suggests a converging evidence toward application of rhythmic auditory cueing to enhance gait performance and stability in people with cerebral palsy. This article details underlying neurophysiological mechanisms and use of cueing as an efficient home-based intervention. It bridges gaps in the literature, and suggests translational approaches on how rhythmic auditory cueing can be incorporated in rehabilitation approaches to enhance gait performance in people with cerebral palsy.
Keywords: entrainment, spastic diplegia, hemiplegia, ataxia, rehabilitation, balance
Cerebral palsy is a common developmental disorder.1,2 The global prevalence of cerebral palsy is approximately 1.5–3.5/1,000 children,3,4 and is supposedly growing in developing countries.5 Cerebral palsy is primarily characterized by pre/postnatal damage to the brain,3 often predisposing to grave neuromuscular and psychological disorders.3,6 The treatment of cerebral palsy inflicts substantial costs7 and adversely impacts quality of life.8,9 Typically, motor dysfunction in cerebral palsy is characterized by spastic or extrapyramidal deficits.10 These neuromuscular dysfunctions might cause dyskinesia, dystonia, ataxia, or hypotonia.11,12 Further, these might lead to increased fatigue, reduced dexterity/coordination, postural instability, muscle contracture, and joint subluxation. Also, these neuromuscular disorders progress with aging.11 For instance, lack of mobility and hypertonia often lead to development of muscle and joint contractures and secondary bone deformities. These neuromuscular deficits among both children and older adults with cerebral palsy considerably impair kinetic and kinematic changes, impair locomotion, and predispose to falls. For instance, exaggerated anterior stooping posture associated with increased anterior tilt in the pelvis, hip flexion, adduction, and internal rotation13–15 adversely impact efficiency in energy expenditure16 and spatiotemporal gait parameters.17 Bourgeois et al18 reported reduction in spatiotemporal gait parameters, such as cadence, stride length, and gait velocity associated with considerable enhancement in gait variability, which might predispose severely toward falls.19
In addition to these musculoskeletal changes, Rosenbaum et al2 suggested considerable discrepancies in sensory perceptions, cognition, and behavior. Neuroimaging studies report deficits in the dorsolateral prefrontal cortex, dorsal anterior cingulate gyrus,20 somatosensory cortex,21 and cerebellum22 which might considerably impair intellectual and cognitive performance.22–24 Likewise, deficits in corticospinal, thalamocortical, superior occipitofrontal and superior longitudinal pathways have also been reported.12,20,25 Together, these psychological constraints might also impair motor performance, such as in a dual-task scenario. For instance, Hung et al26 reported drops in gait-performance measures in unilateral cerebral palsy patients while performing a dual task. Studies have suggested that this modification in gait patterns might happen due to an alleviation in “internal” conscious attention toward autonomic control that adversely impacts proprioception and autonomic functioning, possibly because of movement-specific reinvestment.27–29 The theory suggests that directing attention internally to control autonomic movements, such as gait, can have an adverse impact on performance,29 especially in high-stress situations.30 Common treatment strategies to curb motor dysfunctions in cerebral palsy include training with virtual reality,31 biocueing,32 physical/occupational therapy,33 physical exercise,34 treadmill,35 and orthosis.36,37
Recently, several studies have tried to address the sensorimotor deficits in people with cerebral palsy by applying rhythmic auditory entrainment.38–41 Cueing aims to counteract sensory deficits, and has been shown to modulate neuromagnetic β-oscillations,42 cortical reorganization, enhance biological motion perception,43,44 motor imagery,45,46 neural plasticity,48 reduce shape variability in musculoskeletal-activation patterns,47 and movement-specific reinvestment.49 Moreover, as a cheap50 and viable51 treatment strategy, this approach can provide substantial benefits in developing countries, where prevalence of cerebral palsy due to socioeconomic factors is more prominent.52,53 We identified high-quality systematic reviews analyzing the effects of external auditory cueing on gait performance among healthy,121 Parkinsonism54–56,122 and stroke participants.57–59 However, to the best of our knowledge, no systematic or narrative analysis has been carried out to analyze the effects of auditory entrainment on gait in people with cerebral palsy. Therefore, we attempted to develop a state of knowledge for the use of cerebral palsy patients and medical practitioners, where both qualitative and quantitative data from high-quality studies can be interpreted.
Materials and methods
This review was conducted according to the guidelines outlined in the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) statement60 and American Academy for Cerebral Palsy and Developmental Medicine (AACPDM) methodology for systematic reviews.61
Data sources and search strategy
The academic databases Web of Science, PEDro, EBSCO, Medline, Cochrane Central Register of Controlled Trials, Embase and ProQuest were searched from inception until July 2017. A sample-search strategy is provided in Table 1.
Table 1 Sample search strategy – Embase
Upon selection for review, data extracted from each article were study aim, selection criteria, sample size, sample description (sex, age, health status), intervention, characteristics of auditory cueing, dual tasks, outcome measures, results, and conclusions. The data were then summarized and tabulated (Table 2). The inclusion criteria for the studies were: randomized controlled trials, cluster-randomized controlled trials, or controlled clinical trials; reporting reliable and valid spatiotemporal gait and kinematic parameters; including dynamic aspects of gait stability; use of PEDro methodological quality scale (score ≥4); conducted on human participants; published in a peer-reviewed academic journal; and published in English, German, or Korean.
Quality and risk-of-bias assessment
The quality of the studies was assessed using the PEDro methodological quality scale.62 The scale consists of eleven items addressing external validity, internal validity, and interpretability, and can detect potential bias with high reliability,63 and validity.62 A blinded rating of the methodological quality of the studies was carried out by the first (SG), second (IG) and third (AOE) reviewers. Ambiguous issues were discussed between reviewers and consensus was reached. Included studies were rated and interpreted according to scoring of 9–10, 6–8, and 4–5 for “excellent”, “good”, and “fair” quality,64 respectively. Inadequate randomization, nonblinding of assessors, no intention-to-treat analysis, and no measurement of compliance were considered as major threats for biasing.65
This systematic review also included a meta-analysis approach to develop a better understanding of the incorporated interventions.66 Presence and lack of heterogeneity drove the use of either random- or fixed-effect meta-analysis.67 A narrative synthesis of the findings structured according to intervention, population characteristics, methodological quality, and type of outcome is provided (Table 2). A meta-analysis was conducted between pooled studies using Comprehensive Meta-Analysis software (version 2.0; Biostat, Englewood, NJ, USA). Heterogeneity among the studies was assessed using I2 statistics. The data in this review were systematically distributed, and for each available variable pooled, dichotomous data were analyzed and forest plots with 95% CIs reported. Effect sizes were adjusted and reported as Hedge’s g.68 Thresholds for interpretation of effect sizes were as follows: standard mean effect of 0 meant no change, negative effect meant a negative change, and a positive effect meant a positive change.
Mean effect of 0.2 was interpreted as a small effect, 0.5 a medium effect, and 0.8 a large effect.69 Interpretation of heterogeneity via I2 statistics was 25%, 50%,75% as negligible, moderate and substantial heterogeneity, respectively. 75% as negligible, moderate, and substantial heterogeneity, respectively. Meta-analysis reports, including heterogeneity among studies, were evaluated to determine the reason for heterogeneity, and studies included were then pooled separately and analyzed again in a sub-group analysis. The α-level was set at 95%.
Characteristics of studies included
Our initial search across academic databases yielded a total of 387 studies; 175 studies were included from a personal library. After implementing our inclusion/exclusion criteria, nine studies were left (Figure 1). Data from the studies included have been summarized in Table 2. Of the nine studies included, all were controlled clinical trials.
Figure 1 PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) flowchart for inclusion of studies.
A total of 227 participants were analyzed in the incorporated studies. In the studies included, eight studies incorporated mixed-sex patients. Only one study included male participants.70 The studies provided data on 227 participants (n=119 females/108 males). Moreover, in 108 children, the sex distribution was 57 females to 51 males, and for adults 62 females to 57 males. Descriptive statistics relating to the age (means ± SD) of the participants were tabulated across the studies (Table 2).
Risk of bias
To reduce the risks of bias, studies scoring ≥4 on PEDro were included in the review. Moreover, research protocols to be included in the review were limited to gold-standard randomized controlled trials, cluster-randomized controlled trials, and controlled clinical trials. The individual scores attained by studies using the PEDro scale are reported in Table 2, and Table S1. The average PEDro score for the nine studies was 5 of 10, indicating fair quality for studies overall. Three studies scored 7, and six studies scored 4. Risk of bias across the studies is shown in Figure 2.
Figure 2 Risk of bias across studies.
The results provided evidence for a positive impact of rhythmic auditory cueing on spatiotemporal and kinematic gait parameters among adults and children with cerebral palsy. In all studies, significant enhancement in primary spatiotemporal and kinematic gait parameters were reported.
The evaluation of research studies via meta-analysis requires strict inclusion criteria to limit heterogeneity efficiently.71 However, among the pooled group of studies after strict inclusion criteria, some unexplained heterogeneity was still observed. Subgroup analyses were then performed for identical studies to evaluate the cause of the heterogeneity. The parameters evaluated were spatiotemporal gait parameters, such as cadence, stride length, gait velocity, and kinematic parameters. Further analyses were conducted to evaluate the effects of rhythmic auditory cueing at preferred cadence on gait velocity in both adults and children separately. We included a generalized group analysis by first combining all the pooled studies. The studies excluded differed considerably in assessment methods or if descriptive statistics were not mentioned in the manuscript. However, attempts were made to contact the coauthors for the data.
Gait velocity was analyzed in six studies. Here, two studies evaluated the effects of rhythmic auditory cueing on gait velocity in adults38,72 and four in children41,73–75 with cerebral palsy. One study included assessment of gait velocity while using patterned sensory enhancement73 as the mode of auditory feedback. Analysis of studies revealed (Figure 3) a large positive effect (g=1.13, 95% CI 0.33-1.94). Substantial heterogeneity was observed between studies (I2=84%, P>0.01). Subgroup analyses were conducted to explore heterogeneity.
An analysis for effects of rhythmic auditory cueing on gait velocity in children revealed (Figure S1), large positive effect with substantial heterogeneity (g=1.24, 95% CI 0.31–2.17, I2=81%; P<0.01). Here, the heterogeneity could possibly be attributed to different training regimes in the studies, ie, no training was included by one,41 while others73–75 had training regimes for ≥3 weeks. Subgroup analysis revealed (Figure S2) a large positive effect with substantial heterogeneity (g=1.53, 95% CI 1.07–1.98, I2=82%; P<0.01). Moreover, Jiang75 included only one training session per week. Whereas, others performed training for three (Wang et al.73), and five times (Kwak74), per week. Subgroup analysis revealed a large positive effect with negligible heterogeneity (g=2.05, 95% CI 1.5–2.6, I2=0; P>0.05). Finally, subgroup analysis evaluating the effects of rhythmic auditory cueing on gait velocity in adults revealed a large positive effect with negligible heterogeneity (g=0.95, 95% CI −0.95 to 2.85, I2=0; P>0.05).
Stride length was analyzed in five studies. Two and three studies evaluated the effects of rhythmic auditory cueing on stride length in adults38,72 and children,41,73–75 respectively. Analysis revealed (Figure 4) a medium positive effect (g=0.58, 95% CI −0.02 to 1.19). Moderate heterogeneity was observed between studies (I2=65%, P>0.01). Subgroup analyses were conducted to explore the cause of heterogeneity. Analysis for effects of rhythmic auditory cueing on stride length in children revealed (Figure S3) a medium positive effect with negligible heterogeneity (g=0.75, 95% CI 0.01–1.48, I2=0; P>0.05). Subgroup analysis evaluating the effects of rhythmic auditory cueing on stride length in adults revealed a comparably smaller medium effect with negligible heterogeneity (g=0.3, 95% CI −1.07 to 1.67, I2=0; P>0.05).
Cadence was analyzed in five studies, of which two evaluated the effects of rhythmic auditory cueing on cadence in adults38,72 and three in children41,73–75 with cerebral palsy. Analysis of studies revealed (Figure 5) a medium positive effect (g=0.33, 95% CI −0.41 to 1.07). Substantial heterogeneity was observed between studies (I2=79%, P>0.01). Subgroup analyses were conducted to explore heterogeneity. An analysis for effects of rhythmic auditory cueing on cadence in children revealed a small negative effect with negligible heterogeneity (g=−0.11, 95% CI −0.97 to 0.74, I2=0; P>0.05). Subgroup analysis evaluating the effects of rhythmic auditory cueing on cadence in adults revealed a large positive effect with negligible heterogeneity (g=1.04, 95% CI 0.44–1.64, I2=0; P>0.05).
Three studies analyzed the effects of rhythmic auditory cueing on gait-dynamic index (a combined measure of lower-limb kinematic performance). Data for subgroup analysis on the gait dynamic index concerning community and household dwellers were extracted from two studies.38,76 Analysis revealed (Figure 6) a large positive effect (g=0.92, 95% CI 0.07–1.76, I2=0; P<0.01) with negligible heterogeneity. Further, an analysis of gait-dynamic index in community dwellers revealed a small positive effect with negligible heterogeneity (g=0.07, 95% CI −0.66 to 0.8, I2=0; P>0.05). Comparably, analysis of household dwellers revealed a large positive effect with negligible heterogeneity (g=1.11, 95% CI 0.24–1.98, I2=0; P>0.05). Subgroup analysis was also conducted on individual kinematic parameters to specify the magnitude of effects of rhythmic auditory cueing on specific joint kinematics.
Subgroup analysis evaluating changes at the pelvis revealed (Figure S4) small negative effects with negligible heterogeneity (g=−0.23, 95% CI −0.68 to 0.21, I2=0; P>0.05). At the hip joint, medium negative effects with moderate heterogeneity (g=−0.43, 95% CI −0.89 to 0.01, I2=33.5%; P>0.01) were observed (Figure S5). At the knee joint, medium positive effects with negligible heterogeneity (g=0.26, 95% CI −0.18 to 0.71, I2=0; P>0.05) were observed (Figure S6). At the ankle joint, medium positive effects with moderate heterogeneity (g=0.36, 95% CI −0.09 to 0.81, I2=32.7%; P>0.01) were observed (Figure S7). Finally, at the foot, small negative effects with moderate heterogeneity (g=−0.18, 95% CI −0.62 to 0.26, I2=0; P>0.05) were observed (Figure S8).
The primary objective of this systematic review and meta-analysis was to synthesize the current state of knowledge for the effects of rhythmic auditory cueing on gait in people with cerebral palsy. All nine studies reported beneficial effects of rhythmic auditory cueing on gait parameters in children and adults with cerebral palsy. Further, the meta-analysis found significant small–large standardized effects for the benefits of rhythmic auditory cueing on spatiotemporal and kinematic parameters of gait among patients affected with cerebral palsy.
Typically, spatiotemporal parameters of gait may worsen over time in those with cerebral palsy. Deficits in periventricular white matter,12 gray matter,78 cerebellum,79 basal ganglia,80 and thalamus81 have been well documented.12 These neural centers play an integral role in managing stabilization and performance during automated tasks, such as posture and gait.82,83 In addition, increasing psychological stress might be exerted on automated control for posture, gait, and cognitive processing by deficits reported in corticospinal, thalamocortical, superior occipitofrontal, and longitudinal pathways,84–86 possibly also explaining the loss of gait rhythmicity.87 Likewise, increased energy expenditure,88 associated variability in muscle contraction, and force production add to the instability.89 Rhythmic auditory cueing seems to counter these deficits efficiently. The current meta-analysis reported enhancements in gait velocity (1.24) and stride length (0.75) in children and gait velocity (0.95), stride length (0.3), and cadence (1.04) in adults. Beneficial effects were also observed in gross gait-dynamic index (a combined measure of kinematic variables during gait) for adult patients affected with cerebral palsy (0.92).
Several mechanisms have been suggested for the beneficial effects of rhythmic auditory cueing. For instance, auditory entrainment might aid in reducing errors while executing gait by guiding specific movement patterns.90,91 External entrainment might act as guidance for “heel-contact” and “push-off” timing and/or muscle contractions.39 Likewise, such cross-sensory cueing might also reduce information overload in the native sensory modality by directing task-irrelevant information toward the underused sensory modality.92 The application of auditory entrainment is believed to allow enhancement in gait performance by bypassing or facilitating the frontostriatal pathway via alternative pathways.93–95 Cunnington et al96 reaffirmed and suggested that rhythmic cueing might directly serve as an input supplementary motor area, thereby reducing the onset of motor deficits and aiding in performance. Moreover, cueing has been shown to allow modulation of neuromagnetic β-oscillations in the auditory cortex, cerebellum, inferior frontal gyrus, somatosensory area, and sensorimotor cortex42 and reduce hemispheric asymmetry.97 Also, enhanced activation in inferior colliculi,98 cerebellum, brain stem,94,99 and sensorimotor cortex100,101 have been reported. This might also suggest the facilitation of corticocerebellar network reorganization.48 Finally, entrainment has also been shown to reduce variability in electromyographic activity102 and optimize velocity/acceleration profiles of joint motions by scaling movement time,103 thereby allowing stable pattern generation.
Studies have shown that rhythmic auditory cueing might also be an efficient tool to counteract dual-task-associated information-processing constraints.121,122 For instance, Lohnes and Earhart104 suggested that rhythmic entrainment might allow alleviation in gait performance by possibly freeing up cognitive resources for dual-task execution. Although dual-task performance has been shown to reduce performance in people with cerebral palsy,26 we did not identify any study analyzing the effects of rhythmic auditory cueing under higher information-processing constraints. We suggest future studies address this substantial gap in the literature. Moreover, recent studies evaluating the effects of rhythmic entrainment have revealed beneficial effects of action-relevant acoustic input on gait performance105,122,123 as compared to normal isosynchronous cueing.106 Ecologically valid action-related sounds have been suggested to enhance salience of sensory information concerning spatiotemporal information, thereby aiding movement execution.105–107 Moreover, recent research has revealed the possibilities of including emotional,108 motivational,109 and expressiveness110 components in auditory entrainment to portray differential effects on gait parameters. Unfortunately, a lack of pertinent literature concerning the specific type of modified auditory cueing in cerebral palsy limits our interpretation of the type of auditory cueing that might be beneficial in rehabilitation. Therefore, we suggest future studies address this gap.
Finally, we believe that auditory entrainment might be efficient because of its economical nature and high viability.50,51 The rhythmic entrainment factor could be utilized with music in rehabilitation and day-to-day lives. This could allow benefits in psychophysiological domains.111,112 Moreover, it is important to consider that the retention of enhancements in gait parameters relies not only on the training received in the clinic but also largely on how much the patient follows the treatment protocol at home. In the present meta-analyses, enhancements in kinematic gait parameters observed for household ambulators (1.11) were considerably larger compared to community ambulators (0.07). We believe that delivering this type of home-based intervention could be beneficial for people lacking access to medical interventions in developing countries.113 The growing number of smartphone devices in developing countries114 can be used as a delivery tool while using a simple metronome app, such as WalkMate115 or ListenMee,116 which with proper medical guidance might allow curbing of motor deficits associated with aging.117 We also suggest the use of rhythmic auditory cueing as an adjunct to other rehabilitation strategies, eg, assistive devices,16,124,125 swimming, or other aquatic exercise regimes,118 as it might enhance stability-associated quality of life119,120 and rehabilitation progress by focusing on psychophysiological components.
In conclusion, to the best of our knowledge, this review analyzes for the first time the effects of auditory entrainment on adults and children with cerebral palsy. The present findings are in agreement with systematic reviews and meta-analyses carried out to analyze auditory entrainment effects on healthy,121 stroke57 and parkinsonism population groups.54,56,122 This review suggests the incorporation of rhythmic auditory cueing for enhancing gait performance and stability in people with cerebral palsy.
Publication of this article was funded by the Open Access Fund of Leibniz Universität, Hannover.
SG conceptualized the study, carried out the systematic review and statistical analysis, and wrote the paper. IG and AOE were involved in the systematic review process and reviewed the final manuscript. All authors contributed toward data analysis, drafting and revising the paper and agree to be accountable for all aspects of the work.
The authors report no conflicts of interest in this work.
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Table S1 Individual PEDro scores
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