Effect of rhythmic auditory cueing on gait in cerebral palsy: a systematic review and meta-analysis

Figures & data

Table 1 Sample search strategy – Embase

Date	July 10, 2017
Strategy	#1 AND #2 AND #3 AND #4 AND #5 AND #6 AND #7
#1	(“rhythmic auditory cueing” OR “rhythmic acoustic cueing” OR “rhythmic auditory entrainment” OR “metronome cueing” OR “metronome” OR “rhythmic metronome cueing” OR “acoustic stimulus” OR “acoustic cueing” OR “acoustic cueing” OR “external stimuli” OR “external cueing” OR “external cueing” OR “music therapy” OR “Neurological music therapy” OR “tempo” OR “beat” OR “rhythm” OR “RAC” OR “NMT”)/de OR (rhythmic auditory cueing OR rhythmic auditory cueing OR rhythmic acoustic cueing OR rhythmic auditory entrainment OR metronome cueing OR metronome OR rhythmic metronome cueing OR acoustic stimulus OR acoustic cueing OR acoustic cueing OR external stimuli OR external cueing OR external cueing OR music therapy OR Neurological music therapy OR tempo OR beat OR rhythm OR RAC OR NMT)ti,ab
#2	(“CP” OR “Cerebral Palsy” OR “Cerebral Palsy athetoid” OR “Cerebral Palsy congenital” OR “Cerebral Palsy Diplegic infantile” OR “Cerebral Palsy dyskinetic” OR “Cerebral Palsy dystonic-rigid” OR “Cerebral Palsy hypotonic” OR “Cerebral Palsy mixed” OR “Cerebral Palsy monoplegic, infantile” OR “Cerebral Palsy quadriplegic infantile” OR “Cerebral Palsy Rolandic type” OR “Cerebral Palsy Spastic” OR “Congenital Cerebral Palsy” OR “diplegia-spastic” OR “Diplegic infantile cerebral palsy” OR “infantile cerebral palsy-diplegic” OR “infantile cerebral palsy-monoplegic” OR “infantile cerebral palsy-quadriplegic” OR “little disease” OR “little’s disease” OR “Monoplegic cerebral palsy” OR “Monoplegic infantile cerebral palsy” OR “Quadriplegic infantile cerebral palsy” OR “Spastic diplegia”)/de OR (CP OR Cerebral Palsy OR Cerebral Palsy athetoid OR Cerebral Palsy congenital OR Cerebral Palsy Diplegic infantile OR Cerebral Palsy dyskinetic OR Cerebral Palsy dystonic-rigid OR Cerebral Palsy hypotonic OR Cerebral Palsy mixed OR Cerebral Palsy monoplegic, infantile OR Cerebral Palsy quadriplegic infantile OR Cerebral Palsy Rolandic type OR Cerebral Palsy Spastic OR Congenital Cerebral Palsy OR diplegia-spastic OR Diplegic infantile cerebral palsy OR infantile cerebral palsy-diplegic OR infantile cerebral palsy-monoplegic OR infantile cerebral palsy-quadriplegic OR little disease OR little’s disease OR Monoplegic cerebral palsy OR Monoplegic infantile cerebral palsy OR Quadriplegic infantile cerebral palsy OR Spastic diplegia):ti,ab
#3	(“cognitive task” OR “concurrent task” OR “dual task” OR “dual task paradigm” OR “dual task paradigm” OR “cognitive task training” OR “dual task training” OR “dual task training”)/de OR (cognitive task OR concurrent task OR dual task OR dual task OR dual task paradigm OR dual task paradigm OR cognitive task training OR dual task training OR dual task training”):ti,ab
#4	(“walking” OR “gait” OR “locomotion” OR “range of motion” OR “ROM” OR “ambulation” OR “mobility” OR “treadmill gait” OR “balance” OR “stability” OR “stride” OR “gait training” OR “gait rehabilitation”)/de OR (walking OR gait OR locomotion OR range of motion OR ROM OR ambulation OR mobility OR treadmill gait OR balance OR stability OR stride OR gait training OR gait rehabilitation);ti,ab
#5	(“rehabilitation” OR “treatment” OR “rehab” OR “management” OR “therapy” OR “physiotherapy” OR “physical therapy” OR “prevention” OR “risk prevention”)/de OR (rehabilitation OR treatment OR rehab OR management OR therapy OR physiotherapy OR physical therapy OR prevention OR risk prevention);ti,ab
#6	(“age groups” OR “adolescent” OR “young” OR “elderly” OR “old” AND (“gender” OR “male” OR “female”)/de OR (age groups OR adolescent OR young OR elderly OR old AND (gender OR male OR female));ti;ab
#7	(“intervention study” OR “cohort analysis” OR “longitudinal study” OR “cluster analysis” OR “crossover trial” OR “cluster analysis” OR “randomized trial” OR “major clinical study”)/de OR (longitudinal OR cohort OR crossover trial OR cluster analysis OR randomized trial OR clinical trial OR controlled trial);ti,ab

Table 2 Studies analyzing the effects of RAC on gait

Study	Research aim	Sample description, age (years), mean ± SD/range	PEDro score	Assessment tools	Research design	Auditory cueing	Conclusion
Efraimidou et al^Citation70	Effects of RAC on gait in people with CP	Exp: 5M (35.2±13) Ct: 5M (38.8±12.2)	5	Timed up-and-go test, 10 m walk test, BBS, center-of-pressure sway, self-esteem scale, profile of mood states	Pretest, 50-minute session twice a week for 8 weeks with RAC at 70 bpm, and posttest at 90 bpm	Rhythmic music cueing (70–90 bpm), with 4/4 music meter	Significant enhancement in timed up-and-go test, normal and fast gait speed in a 10 m walking test in Exp compared to Ct Significant enhancement in BBS score in Exp compared to Ct Significant reduction in center-of-pressure sway and timing of right- and left-foot synchronization in Exp compared to Ct Significant enhancement in self-esteem score and overall scoring of profile and mood states in Exp compared to Ct
Shin et al^Citation38	Effects of RAC on gait in people with hemiplegia (stroke/CP)	CP: 4F, 3M (30.1±4.1) Stroke: 4F, 7M (44.27)	4	Cadence, gait speed, stride length, stride time, step time, single/double-support time, stance/swing phase (temporospatial deviation and side-to-side comparison), pelvis, hip, knee, ankle, foot kinematics, gait-deviation index	Pretest, gait training with RAC for 30 minutes/session, and three sessions/week for 4 weeks, posttest	RAC by four-chord progression with metronome beat on keyboard at preferred cadence	Significantly reduced ankle plantar flexion at initial contact and push-off Reduced anterior pelvic tilt in sagittal plane after training with auditory cueing Significantly enhanced kinematic improvements in stroke patients compared to CP Significant enhancement in gait-deviation index and kinematics for people with subacute compared to chronic stroke No effect on gait parameters after training from auditory cueing Enhanced side-to-side symmetry after training from auditory cueing Significant enhancement in gait-deviation index, hip adduction in mid-stance, maximal knee flexion in mid-swing, ankle dorsiflexion in terminal stance after training from RAC
Wang et al^Citation73	Effect of auditory feedback on motor capacity, strength, mobility, and gait in people with CP (spastic diplegia)	Exp: 6F, 12M (9±1.9) Ct: 3F, 15M (8.9±2.6)	7	Gross motor-function measure (dimensions D and E), goal-dimension score, gait speed, PEDI, functional skill scale of PEDI, caregiver-assistance scale, one-repetition-maximum load of a loaded sit-to-stand test, gait speed and gait duration for 10 m walking test	Pretest, sit-to-stand exercise at home three times/week for 6 weeks, posttest at 6, 12 weeks Training load progressed 2 weeks upon evaluation of one-repetition-maximum sit-to-stand test, auditory feedback adjusted every 2 weeks upon reassessment	Auditory feedback as patterned sensory enhancement (spatial, temporal, and force cueing) Pitch variations: ascending and descending melodies indicate directions (range of motion cueing) Tempo, meter, and rhythmic pattern (speed and timing of movement) Loudness: strength of muscular contraction	Significant enhancement in goal-dimension score during posttest at 6- and 12-week follow-up in Exp compared to Ct Significant enhancement in dimension D score in first posttest and 6-week follow-up posttest in Exp compared to Ct Enhancement in dimension E, dimension D (12 weeks posttest) scores during 6 and 12-week follow-up posttest in Exp compared to Ct Significant reduction in PEDI for caregiver assistance at 12-week posttest Exp compared to Ct Enhancement in gait speed (posttest and 12-week posttest), and one repetition maximum of sit to stand in posttest and 6- and 12-week posttests in Exp compared to Ct
Jiang^Citation75	Effect of RAC on gait performance in people with CP	5F, 4M (5–12)	7	Gait velocity, cadence, and stride length	Gait training with/without RAC at 0 and +5% of preferred cadence (randomly) for one 30-minute session/week for 3 weeks	RAC by piano, guitar, bass, and percussion, with music in 4/4 beat accented by metronome. Piano superimposed on beat to emphasize rhythm at preferred cadence	Significant enhancement in cadence and gait velocity with training from auditory cueing Enhancement in stride length with auditory cueing Significant enhancement in cadence and gait velocity for people with higher level of gross motor functioning compared to lower levels of gross motor functioning
Varsamis et al^Citation77	Effect of RAC on gait performance in people with CP with mental disabilities	7F, 11M (18.2±3.8)	4	Duration for gait performance, number of steps, steps/minute, pulse/minute, and steps and pulse (intraindividual Standard deviation)	Pretest, gait performance with/without RAC and instruction “do your best”	Rhythmic metronome cueing at preferred cadence	Significant enhancement in duration, number of steps with auditory cueing Significant reduction in steps/minute, pulse/minute, steps and pulse (intraindividual SD) with auditory cueing
Baram and Lenger^Citation41	Effect of real-time auditory feedback on gait performance in people with CP	Visual cueing: 7F, 3M (13.3±6.2) Auditory cueing: 6F, 4M (11.1±6.5) Ct, visual cueing: 3F, 4M (12.4±0.5) Auditory cueing: 4F, 4M (12.6±7.4)	4	Pre- and posttest gait analysis; training performed between tests with visual or auditory cueing	Walking speed, stride length, and cadence	Real-time auditory cueing at preferred cadence	Significant enhancement in walking speed and stride length compared to Ct condition and visual condition alone No effect of auditory feedback on healthy Ct
Kim et al^Citation39	Effect of RAC on gait for people with CP	Exp: 5F, 10M (27.3±2.4) Ct: 6F, 7M (27.3±2.5)	7	Cadence, gait velocity, stride length, step length, stride time, step time, stance phase, swing phase, gait-deviation index, kinematic data for pelvis, hip sagittal plane (anterior tilt/flexion at initial contact, maximal–minimal angle of anterior tilt/flexion), coronal plane (abduction–adduction at initial contact, maximal adduction–abduction angle), transverse plane (internal–external rotation at initial contact, maximal–minimal internal–external rotation), knee sagittal plane (flexion at initial contact, maximal flexion at swing, minimal flexion at stance), ankle sagittal plane (flexion at initial contact, maximal dorsiflexion at stance, minimal plantar flexion at preswing), foot transverse plane (internal–external rotation at initial contact, maximal–minimal internal–external rotation)	Pretest, gait training with RAC (Exp), neurodevelopmental therapy/Bobath therapy (Ct) at preferred cadence for 30-minute session three times/week for 3 weeks posttest	Rhythmic metronome cueing at preferred cadence	Significant enhancement in cadence, gait velocity, stride length, step length, swing phase, gait-deviation index in Exp after training with RAC compared to Ct Significant reduction in stride time, step time, stance phase in Exp as compared to Ct Significant reduction in pelvis: sagittal plane (anterior tilt initial contact, maximal angle of anterior tilt) in Exp as compared to Ct Significant enhancement in pelvis: sagittal plane (minimal angle of anterior tilt) and hip joint: transverse plane (maximal internal rotation) in Exp as compared to Ct Significant reduction in hip joint: sagittal plane (minimal flexion angle) and coronal plane (abduction–adduction at initial contact, maximal adduction–abduction angle) in Exp as compared to Ct
Kim et al^Citation76	Effect of RAC on gait in children with CP	Exp I (community ambulators): 3F, 5M (25.1±8.1) Exp II (household ambulators): 2F, 4M (26.3±6.6) Ct: 15F, 15M (21.5±1.7)	4	Cadence, gait velocity, stride length, step length, stride time, step time, stance phase, swing phase, gait-deviation index, kinematic data for pelvis, hip sagittal plane (anterior tilt/flexion at initial contact, maximal–minimal angle of anterior tilt/flexion), coronal plane (abduction–adduction at initial contact, maximal adduction–abduction angle), transverse plane (internal–external rotation at initial contact, maximal–minimal internal–external rotation), knee sagittal plane (flexion at initial contact, maximal flexion at swing, minimal flexion at stance), ankle sagittal plane (flexion at initial contact, maximal dorsiflexion at stance, minimal plantar flexion at preswing), foot transverse plane (internal–external rotation at initial contact, maximal–minimal internal–external rotation)	Gait performance with/without rhythmic metronome cueing at preferred cadence	Rhythmic metronome cueing at preferred cadence	Significant reduction in pelvis: sagittal plane (anterior tilt initial contact, maximal, minimal angle of anterior tilt) and hip: sagittal plane (maximal, minimal flexion angle) and transverse plane (maximal internal–external rotation) in Exp after training with RAC (Exp I > Exp II) Significant enhancement in gait-deviation index with RAC in Exp (Exp I > Exp II) Significant reduction in step length for household-ambulator group with RAC
Kwak^Citation74	Effect of RAC on gait performance in people with CP	30 (6–20) Exp I: 10 patients Exp II: 10 patients Ct: 10 patients	4	Cadence, stride length, gait velocity, gait cycle, gait symmetry, and foot-contact pattern	Pretest, (Exp I and II) gait training at +5%, +10%, and +15% of preferred cadence in first, second, and third weeks, respectively, training for 30 minutes/session for 5 days/week for 3 weeks posttest Exp I: therapist-guided gait training with RAC (with drum/clap cueing, pattern sensory enhancement, and therapeutic instrument music playing for muscle strengthening) Exp II: therapist-guided gait training, but self-guided training with RAC Ct: conventional training by a therapist without auditory cueing	RAC at +5%, +10%, and +15% of preferred cadence by music, steady-beat pattern with 4/4 meter, ie, 80–120 bpm Input by drum or clap sound in closed and open tone to differentiate acoustics for right and left foot	Significant enhancement in stride length, gait velocity, and gait symmetry for Exp I Enhancement in stride length, gait symmetry, and gait velocity for Exp II compared to Ct Enhancement in cadence for EXP I and II and reduction in cadence for Ct

Abbreviations: BBS, Berg Balance Scale; bpm, beats per minute; CP, cerebral palsy; Ct, control group; Exp, experimental group; F, female; M, male; PEDI, Pediatric Evaluation of Disability Inventory; RAC, rhythmic auditory cueing

Figure 1 PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) flowchart for inclusion of studies.

Figure 2 Risk of bias across studies.

Figure 3 Forest plot illustrating individual studies evaluating the effects of rhythmic auditory cueing on gait velocity in people with cerebral palsy.

Notes: Negative effects indicate reduction in gait velocity, positive effects enhancement in gait velocity. Weighted-effect sizes – Hedge’s g (boxes) and 95% CI (whiskers) – demonstrate repositioning errors for individual studies. The diamond represents pooled effect sizes and 95% CI. Negative mean differences indicate favorable outcomes for control groups, positive mean differences favorable outcomes for experimental groups.
Abbreviations: A, adults; C, children.

Figure 4 Forest plot illustrating individual studies evaluating the effects of rhythmic auditory cueing on stride length in people with cerebral palsy.

Notes: Negative effects indicate reduction in stride length, positive effects enhancement in stride length. Weighted-effect sizes – Hedge’s g (boxes) and 95% CI (whiskers) – demonstrate repositioning errors for individual studies. The diamond represents pooled effect sizes and 95% CI. Negative mean differences indicate favorable outcomes for control groups, positive mean differences favorable outcomes for experimental groups.
Abbreviations: A, adults; C, children.

Figure 5 Forest plot illustrating individual studies evaluating the effects of rhythmic auditory cueing on cadence in people with cerebral palsy.

Notes: Negative effects indicate reduction in step frequency, positive effects enhancement in step frequency. Weighted-effect sizes – Hedge’s g (boxes) and 95% CI (whiskers) – demonstrate repositioning errors for individual studies. The diamond represents pooled effect sizes and 95% CI. Negative mean differences indicate favorable outcomes for control groups, positive mean differences favorable outcomes for experimental groups.
Abbreviations: A, adults; C, children.

Figure 6 Forest plot illustrating individual studies evaluating the effects of rhythmic auditory cueing on gait-dynamic index in people with cerebral palsy.

Notes: Negative effects indicate reduction in gait-dynamic index, positive effects enhancement in gait-dynamic index. Weighted effect sizes – Hedge’s g (boxes) and 95% CI (whiskers) – demonstrate repositioning errors for individual studies. The diamond represents pooled effect sizes and 95% CI. Negative mean differences indicate a favorable outcome for control groups, positive mean differences a favorable outcome for experimental groups.
Abbreviations: A, adults; C, children; H, household dwellers.

Figure S1 Forest plot illustrating individual studies evaluating the effects of rhythmic auditory cueing on gait velocity in children with cerebral palsy.

Notes: Negative effects indicate reduction in gait velocity, positive effects enhancement in gait velocity. Weighted-effect sizes – Hedge’s g (boxes) and 95% CI (whiskers) – demonstrate repositioning errors for individual studies. The diamond represents pooled effect sizes and 95% CI. Negative mean differences indicate favorable outcomes for control groups, positive mean differences favorable outcomes for experimental groups.

Abbreviation: C, children.

Figure S2 Forest plot illustrating individual studies evaluating the effects of rhythmic auditory cueing on gait velocity in children with cerebral palsy posttraining.

Notes: Negative effects indicate reduction in gait velocity, positive effect sizes enhancement in gait velocity. Weighted-effect sizes – Hedge’s g (boxes) and 95% CI (whiskers) – demonstrate repositioning errors for individual studies. The diamond represents pooled effect sizes and 95% CI. Negative mean differences indicate favorable outcomes for control groups, positive mean differences favorable outcomes for experimental groups.

Abbreviation: C, children.

Figure S3 Forest plot illustrating individual studies evaluating the effects of rhythmic auditory cueing on stride length in children with cerebral palsy.

Notes: Negative effects indicate reduction in stride length, positive effects enhancement in stride length. Weighted-effect sizes – Hedge’s g (boxes) and 95% CI (whiskers) – demonstrate repositioning errors for individual studies. The diamond represents pooled effect sizes and 95% CI. Negative mean difference indicate favorable outcomes for control groups, positive mean difference favorable outcomes for experimental groups.

Abbreviation: C, children.

Figure S4 Forest plot illustrating individual studies evaluating the effects of rhythmic auditory cueing on pelvic kinematics in adults with cerebral palsy.

Notes: Negative effects indicate reduction in pelvic kinematics, positive effects enhancement in pelvic kinematics. Weighted-effect sizes – Hedge’s g (boxes) and 95% CI (whiskers) – demonstrate repositioning errors for individual studies. The diamond represents pooled effect sizes and 95% CI. Negative mean differences indicates favorable outcomes for control groups, positive mean differences favorable outcomes for experimental groups.

Figure S5 Forest plot illustrating individual studies evaluating the effects of rhythmic auditory cueing on hip kinematics in adults with cerebral palsy.

Notes: Negative effects indicate reduction in hip kinematics, positive effects enhancement in hip kinematics. Weighted-effect sizes – Hedge’s g (boxes) and 95% CI (whiskers) – demonstrate repositioning errors for individual studies. The diamond represents pooled effect sizes and 95% CI. Negative mean differences indicate favorable outcomes for control groups, positive mean differences favorable outcomes for experimental groups.

Figure S6 Forest plot illustrating individual studies evaluating the effects of rhythmic auditory cueing on knee kinematics in adults with cerebral palsy.

Notes: Negative effects indicate reduction in knee kinematics, positive effects enhancement in knee kinematics. Weighted-effect sizes – Hedge’s g (boxes) and 95% CI (whiskers) – demonstrate repositioning errors for individual studies. The diamond represents pooled effect sizes and 95% CI. Negative mean differences indicate favorable outcomes for control groups, positive mean differences favorable outcomes for experimental groups.

Figure S7 Forest plot illustrating individual studies evaluating the effects of rhythmic auditory cueing on ankle kinematics in adults with cerebral palsy.

Notes: Negative effect sizes indicate reduction in ankle kinematics, positive effects enhancement in ankle kinematics. Weighted-effect sizes – Hedge’s g (boxes) and 95% CI (whiskers) – demonstrating repositioning errors for individual studies. The diamond represents pooled effect sizes and 95% CI. Negative mean differences indicate favorable outcomes for control groups, positive mean difference favorable outcomes for experimental groups.

Figure S8 Forest plot illustrating individual studies evaluating the effects of rhythmic auditory cueing on foot kinematics in adults with cerebral palsy.

Notes: Negative effects indicated reduction in foot kinematics, positive effects enhancement in foot kinematics. Weighted-effect sizes – Hedge’s g (boxes) and 95% CI (whiskers) – demonstrate repositioning errors for individual studies. The diamond represents pooled effect sizes and 95% CI. Negative mean differences indicate favorable outcomes for control groups, positive mean differences favorable outcomes for experimental groups.

Table S1 Individual PEDro scores

Study	PEDro	Point estimates and variability	Between-group comparison	Intention to treat	Adequate follow-up	Blinded assessors	Blinded therapists	Blinded subjects	Baseline comparability	Concealed allocation	Random allocation	Eligibility criteria
Efraimidou et al^Citation70	4	1	1	0	1	0	0	0	0	0	1	1
Shin et al^Citation38	4	1	1	0	1	0	0	0	0	0	1	1
Wang et al^Citation73	7	1	1	0	1	1	0	0	1	1	1	1
Jiang^Citation75	7	1	1	0	1	1	0	0	1	1	1	1
Baram and Lenger^Citation41	4	1	1	0	1	0	0	0	0	0	1	1
Varsamis et al^Citation77	4	1	1	0	1	0	0	0	0	0	1	1
Kim et al^Citation39	7	1	1	0	1	1	0	0	1	1	1	1
Kim et al^Citation76	4	1	1	0	1	0	0	0	0	0	1	1
Kwak^Citation74	4	1	1	0	1	0	0	0	0	0	1	1

EfraimidouVTsimarasVProiosMThe effect of a music and movement program on gait, balance and psychological parameters of adults with cerebral palsyJ Phys Educ Sport201616413571364

 Google Scholar

ShinYKChongHJKimSJChoSREffect of rhythmic auditory stimulation on hemiplegic gait patternsYonsei Med J20155661703171326446657

 PubMed Web of Science ®Google Scholar

WangTHPengYCChenYLA home-based program using patterned sensory enhancement improves resistance exercise effects for children with cerebral palsy: a randomized controlled trialNeurorehabil Neural Repair201327868469423757295

 PubMed Web of Science ®Google Scholar

JiangAThe Effect of Rhythmic Auditory Stimulation on Gait in Young Children with Spastic Cerebral Palsy [master’s thesis]MiamiUniversity of Miami2013

 Google Scholar

VarsamisPStaikopoulosKKartasidouLEffect of rhythmic auditory stimulation on controlling stepping cadence of individuals with mental retardation and cerebral palsyInt J Spec Educ20122736875

 Google Scholar

BaramYLengerRGait improvement in patients with cerebral palsy by visual and auditory feedbackNeuromodulation2012151485222151772

 PubMed Web of Science ®Google Scholar

KimSJKwakEEParkESChoSRDifferential effects of rhythmic auditory stimulation and neurodevelopmental treatment/Bobath on gait patterns in adults with cerebral palsy: a randomized controlled trialClin Rehabil2012261090491422308559

 PubMed Web of Science ®Google Scholar

KimSJKwakEEParkESChanges in gait patterns with rhythmic auditory stimulation in adults with cerebral palsyNeurorehabilitation201129323324122142756

 PubMed Web of Science ®Google Scholar

KwakEEEffect of rhythmic auditory stimulation on gait performance in children with spastic cerebral palsyJ Music Ther200744319821617645385

 PubMed Web of Science ®Google Scholar