Clinical Rehabilitation

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Effects of external rhythmical cueing on gait in patients with Parkinson's disease: a

systematic review
I Lim, E van Wegen, C de Goede, M Deutekom, A Nieuwboer, A Willems, D Jones, L Rochester and G
Kwakkel
Clin Rehabil 2005 19: 695
DOI: 10.1191/0269215505cr906oa

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Clmnica! Rehabilitation 2005; 19: 695 ---713

Effects of external rhythmical cueing on gait in

patients with Parkinson's disease: a systematic
review
I Lim, E van Wegen, C de Goede Department of Physiotherapy, VU University Medical Center, M Deutekom Department
of Clinical Epidemiology and Biostatistics, Academic Medical Center, Amsterdam, The Netherlands, A Nieuwboer, A Willems
Department of Rehabilitation Sciences, Faculty of Physical Education and Physiotherapy, Katholieke Universiteit Leuven,
Belgium, D Jones, L Rochester School of Health, Community and Education Studies, Northumbria University, Newcastle
upon Tyne, UK and G Kwakkel Department of Physiotherapy, VU University Medical Center, Amsterdam, The Netherlands
Received 7th February 2005; returned for revisions 28th April 2005; revised manuscript accepted 26th May 2005.

Objective: To critically review studies evaluating the effects of external rhythmical

cueing on gait in patients with Parkinson's disease.
Methods: Articles published from 1966 to January 2005 were searched by two
physiotherapists in MEDLINE, PiCarta, PEDRo, Cochrane, DocOnline, CINAHL and
SUMSEARCH. To be included, articles had to investigate the effects of external
rhythmical cueing (i.e., auditory, visual or tactile cueing) on gait parameters in patients
with idiopathic Parkinson's disease. Both controlled and noncontrolled studies were
included. Based on the type of design and methodological quality a meta-analysis or
best-evidence synthesis was applied.
Results: lwenty-four studies (total number of patients = 626) out of the 1 59
screened studies were evaluated in this systematic review. Two out of 24 were
randomized controlled trails (RCT), both of high methodological quality. One RCT did
not focus specifically on external rhythmical cueing of individual patients with
Parkinson's disease, but on group exercises in general, including walking with cues.
All other studies were pre-experimental studies. Best-evidence synthesis showed
strong evidence for improving walking speed with the help of auditory cues.
Insufficient evidence was found for the effectiveness of visual and somatosensory
cueing.
Conclusion: Only one high-quality study, specifically focused on the effects of
auditory rhythmical cueing, suggesting that the walking speed of patients with
Parkinson's disease can be positively influenced. However, it is unclear whether
positive effects identified in the laboratory can be generalized to improved activities
of daily living (ADLs) and reduced frequency of falls in the community. In addition, the
sustainability of a cueing training programme remains uncertain.

Address for correspondence: LIIK Lim, Department of

Physiother-apy, VU University Medical Center, De Boeleluan
11 17, PO Box 7057, 1007 MB Amsterdam, The Netherlands.
e-mail: i.lirm
1vumc.nl
r(') 2005 Edward Arnold (Publishers) Ltd 10.1 19I/0269215505ci-906oa

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696 I Lirn et al.

Introduction cueing on gait in Parkinson's disease. They con-

cluded that external cueing can significantly im-
Parkinson's disease is a progressive neurological prove gait and gait-related activities in patients
disorder, with a prevalence increasing with advan- with Parkinson's disease.
cing age. In Europe, 1.8 per 100 inhabitants over The precise definition of a cue is problematic
the age of 65 are diagnosed with Parkinson's and intervention based on external rhythmical
disease, whereas in the age category of 65-69 years cueing has not been clearly described. According
2.4 per 100 inhabitants are affected. For the age to Cools,23 cues are 'contextual or spatial stimuli
group of 85-89 years, the prevalence increases up
which are associated with behaviour to be exe-
to 2.6 per 100 inhabitants.'
cuted, through past experience'. Horstink et al.24
The idiopathic form of Parkinson's disease distinguish between cues and stimuli, stating that
results from a degeneration of dopamine-produ- cues give information on how an action should be
cing cells in the substantia nigra which leads to carried out and are hence more specific than
clinical symptoms such as hypokinesia, bradykine- simple stimuli'. Based on the observations of
sia, postural instability, rigidity and tremor.24 Cools23 and Horstink et al.,24 and given the fact
These symptoms are accompanied by difficulties that parkinsonian symptoms particularly affect
in motor performance such as gait problems and
complex and sequential movements, for the pur-
falls.4- 7 poses of this review external rhythmical cueing is
Despite optimal medication therapy, gait pro- operationally defined as 'applying temporal (rhyth-
blems associated with Parkinson's disease are often mical) or spatial stimuli associated with the initia-
characterized by a decreased stride length8 and tion and ongoing facilitation of motor activity
walking speed, an increased cadence and double (gait)'
limb support, 2'6 shuffling gait, gait festination and The aim of the present systematic review is to
freezing.9- t Physiotherapy is reported to be a low- add to the literature a systematic review based on
cost2 -14 treatment and an useful addition to
(1) a qualitative synthesis method and (2) the
standard medication. 15- 19 De Goede et al. 16
above-mentioned, prestated definition of cueing.
demonstrated small but significant improvements
in activities of daily living (ADLs), walking speed
and stride length in a meta-analysis on the effects
of physiotherapy on Parkinson's disease using a Methods and materials
fixed effects model. Deane et al. conducted a
Cochrane review on the effects of physiotherapy Literature search
on Parkinson's disease. They were not able to draw Articles were compiled for this study from a
firm conclusions regarding the efficacy of phy- number of sources. Two physiotherapists (SB/OD)
siotherapy, because of methodological weaknesses independently performed a search in the databases
and due to the small number of trials at the time of of MEDLINE (1966-2004), PiCarta, PEDro,
their review. Recently, Gage et al. 18 reported Cochrane, DocOnline, CINAHL and SUM-
positive effects of physiotherapy on motor perfor- SEARCH using the following keywords and their
mance, gait, ADLs and cardiovascular fitness in combinations: Parkinson, Parkinson's disease, Par-
their narrative review of the effects of multidisci- kinson disease, cue, cueing, physical therapy,
plinary rehabilitation on Parkinson's disease. All physiotherapy, exercise, locomotion, gait, optical
reviews included studies in which intervention was flow field, visual, auditory, sensory, tactile, beha-
offered with the help of external rhythmic stimula- vioural, external, rhythmic, stimulus, stimuli and
tion or external rhythmic cueing. Facilitation of walking.
gait of patients with Parkinson's disease with the Studies were accepted when: (1) they investi-
help of cueing has been reported since 1942.21) The gated the effects of external rhythmical cueing on
first detailed analysis of external cueing on gait gait in patients with idiopathic Parkinson's disease;
was performed by Martin in 1967.21 Two non- (2) the intervention was applied to improve gait
systematic reviews by Rubinstein et (1l.17 and performance; (3) they were published in a peer-
Darmon et 6X/.22 evaluated the effects of external reviewed journal and (4) they were written in

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 Cueing in patients );vith Parkinson's disease 697
English, German, French or Dutch. Single-case descriptive and two statistical criteria. A study
studies were excluded. with a noncontrolled design was considered to be
of sufficient quality if at least four internal validity
Intervention types criteria, two descriptive criteria and one statistical
For the present review, the external rhythmical criterion were rated positively (see Appendix 2).
intervention was classified into four types of RCTs and noncontrolled studies who did not meet
cueing: (1) auditory cueing; (2) visual cueing; (3) the above-stated criteria were considered to be of
tactile cueing; and (4) a combination of above- low quality.
mentioned types of cueing.

Data analysis Results

If appropriate, quantative analysis of the results
was performed separately for each intervention Overview of literature and rating of the studies
and restricted to RCTs. When these RCTs were Based on abstracts and titles, a total of 159
comparable in terms of intervention, patient char- articles was identified and 40 of these candidate
acteristics and outcome measures, statistical pool- studies investigated the effects of external rhythmi-
ing was considered. In case of heterogeneity, with cal cueing. Twenty-four studies, with a total
respect to intervention and measurements of out- number of 626 patients included, matched all
come, or lack of RCTs, a best-evidence synthesis inclusion criteria and were selected for qualitative
was applied. The method for applying a best- analysis. 332-53
evidence synthesis was based on the list proposed General characteristics of the different studies
by van Tulder et al.26 and modified by Steultjens concerning design of the study, type of cueing,
et al.27 (see Appendix 1). The design of the studies number of subjects, characteristics of the subjects,
and the methodological quality was taken into type and dose of intervention, outcome measure-
account when rating the levels of evidence. The ments and ratings of results are presented in
methodological quality of all studies was evaluated Table 1.
by two independent reviewers (IL, MD). Disagree- The methodological quality was assessed for two
ments were resolved by discussion. If no consensus RCTs and 22 pre-experimental studies. None of
was met a third reviewer (GK) made the final these studies were controlled clinical trials (CCTs).
decision. A kappa statistic for inter-rater agree- One publication3 presented three independent
ment was calculated. studies. These studies are separately rated on
A list of methodological criteria recommended methodological quality. In two publications48'53
by Van Tulder et al.6 was used to rate the more than one study was presented. As the effects
methodological quality of RCTs. This list, contain- of cueing were investigated in only one study per
ing all the criteria proposed by Jadad et a.28 and publication, only those studies were taken into
Verhagen et al.,29 consists of 11 criteria for internalaccount for analysis.
validity, six for descriptive criteria and two for The two RCTs32,33 were of high methodological
statistical criteria (see Appendix 2). One modifica- quality, five pre-experimental studies were of
tion was made regarding the specification of the sufficient methodological quality,36 '52 and
eligibility criterion: this involved the addition of all other studies were of low methodological
the Hoehn and Yahr stage.30 Studies were con- quality (Appendix 2). A kappa statistic of 0.84
sidered to be of high quality if at least six criteria was calculated for inter-rater agreement on scoring
for internal validity, three descriptive criteria, and the list for methodological quality.27 Applying a
one statistical criterion were met.26 quantitative analysis was not possible due to the
To rate the methodological quality of the studies lack of RCTs, therefore a best-evidence synthesis
with another design than controlled trials (i.e., pre- has been applied on all intervention types.
experimental studies31) the same methodological
scorings list was used, with an adaptation made by Auditory cueing
Steultjens et al.27 This adapted scorings list Fourteen studies, two RCTs3'33 and 13 studies
includes seven criteria for internal validity, five with a pre-experimental design37 39I4245 48.5051,53

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708 I Lim et al.

investigated the effects of auditory cueing (music, synthesis. Stride length was measured in two
metronome) on gait (Table 1). Both RCTs were of studies of sufficient methodological quality36 l2
high methodological quality and three studies with and 10 studies of low quality.33435444849,l 53
a pre-experimental design were of sufficient meth- One of the 2 studies with sufficient quality52
odological quality,4'142'47 all other studies were of reported positive effects of floor markers on
low methodological quality 37 9,40,45,46,48,503,51.53 stride length. In the other studies,36 no changes
were found and therefore insufficient evidence
Measurement outcomes was shown. Insufficient evidence was found
Walking speed was measured in two RCTs32 33 for the effect of floor markers on ca-
and in 10 studies with a pre-experimental dence, 3,34.3 5.44.48,49,51.5 3 step length, stride time,
design 39'41'42'45 -47,50,51,53 Both RCTs found single support36 and double support,3'36'38 due to
significant improvement on walking speed as the low quality of the studies measuring these
an outcome measurement and therefore strong parameters.
evidence was shown in a best-evidence synthesis. Several studies investigated the effect of other
Stride length and cadence were measured visual cues than floor markers (e.g., (modified)
in one RCT32 and 11 pre-experimental walking sticks,38'43 a rhythmic flashing light,
studies. 39,411,42,45 -4850,5 1.53 As significant improve- mounted on the spectacles of the subjects52 or a
ments were found for stride length and cadence as subject-mounted light device.44 Insufficient evi-
outcome measurements in one RCT, limited evi- dence was found for all of these visual cues,
dence was available for these parameters. Step applying best-evidence synthesis.
length, step-extremity ratio, double support, cycle
time and base of support4 were assessed in one Tactile cueing
pre-experimental study of sufficient quality. Step to One pre-experimental study of low quality411
step variability was assessed in one pre-experimen- studied the effects of tactile cueing (shoulder
tal study of sufficient quality and in one Vre- taps) (Table 1). Best-evidence synthesis showed
experimental study of low quality.47'54 Time-740 insufficient evidence for rhythmical shoulder taps
and number of steps40 needed to complete a on the time and number of steps needed to
complex track with freezing-inducing elements complete a complex track.
(e.g., turns and doorways) were assessed in studies
of low quality. Therefore, insufficient evidence was Combination of auditory and visual cueing
found for these gait parameters after applying a One pre-experimental study of low quality-'
best-evidence synthesis. investigated the effects of a combination of audi-
tory cueing and floor markers (Table 1). Insuffi-
Visual cueing cient evidence was found for this on walking speed,
Fourteen studies3 34a36,38-43,4448.49.51 -5 m stride length and cadence, applying a best-evidence
sured the effect of visual cueing on gait in synthesis.
Parkinson's disease (Table 1), however no
RCTs were found investigating the effects of visual
cueing on gait. Two studies showed sufficient
methodological quality,36'52 whereas 12 stu- Discussion
dies3'34'35'3 .43.44.48.49.5 1 ,were of low methodo-
logical quality. This is the first systematic review of the literature
using an explicit analysis method that explored the
Measurement outcomes effects of external cueing on the gait of patients
Ten studies3'34'35'44'48,49.51.53 investigated the with Parkinson's disease. Two RCTs and 24 studies
effect of floor markers on walking, by using stripes with a noncontrolled design were identified inves-
on the floor, perpendicular to the walking direc- tigating four different types of cueing and 13
tion. All but one36 of these studies were of low different measurements of outcome. Unfortu-
methodological quality. Therefore, insufficient evi- nately, only one study investigated the effects
dence was found, when applying a best-evidence of tactile cueing on parkinsonian gait. Strong

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 Cueing in patients wvith Parkinson's disease 709
Although strong evidence was found in favour of
Clinical messages auditory cueing, the interpretation of reported
effects on walking speed needs further considera-
* There is strong evidence that rhythmical tion. First most studies were executed in a labora-
auditory cueing enhances walking speed in tory setting and focused on instantaneous effects
patients with Parkinson's disease. only, whereas four intervention studies were re-
* However, generalization of reported effects ported in which patients were taught to take
measured in a gait laboratory to gait-related advantage of auditory rhythms by systematic
ADLs and patients' own home situations training.32"33'37'54 In three studies an exercise
remains unclear. programme was applied39 33 and in two studies
the subjects were able to practise using the cues in
their own home situation.32'37 Although these
evidence was found for effects with the use of studies showed positive results for auditory cue-
auditory cueing on walking speed in Parkinson's ing,32'33 the impact of reported effects measured in
disease. Limited evidence was available for improv- a laboratory setting is difficult to generalize to the
ing stride length and cadence with the use of home. It is known that patients with Parkinson's
auditory cueing, applying best-evidence synthesis. disease have severe problems apply the learned
Insufficient evidence was found for improving gait skills in a clinical setting to their home situation.55
of patients with Parkinson's disease with the help For this reason it is preferable for intervention and
of visual cueing (i.e., floor markers, walking sticks, assessments to be carried out in the patient's own
subject-mounted laser beams or a flashing light home environment.
mounted on the spectacles of the subject), tactile Secondly, the impact of walking speed on ADLs
cueing (shoulder taps) or a combination of audi- and extended ADLs remains unclear. In particular
tory and visual cueing (an auditory rhythm and the carry-over effects of external cues on symptoms
floor markers). Although external rhythmical cue- such as freezing and falling needs further investi-
ing is often used in rehabilitation of patients with gation.
Parkinson's disease, only two RCTs investigated Thirdly, it is not clear how the external cues need
the effects of auditory cueing on gait. However, in to be presented to the patient with Parkinson's
the RCT of Ellis et al.,33 auditory cueing was only disease to obtain maximum effect. Both instanta-
a third part of an exercise programme given to neous effects and training effects were found in the
patients with Parkinson's disease (Table 1). It is current review. Future studies should focus on the
therefore not clear whether the improved walking best way to use the cues in the clinical setting.
speed was a result of external rhythmical cueing or A possible explanation for the uncertainty about
due to other elements in this group exercise the best way to present cues and to assess the
programme. Leaving this study out, the evidence effects on gait is the lack of an uniform definition
for improving gait in Parkinson's disease with the for external cueing. For this review, a definition
help of auditory cueing was reduced to limited was formulated based on the descriptions of cues
evidence for walking speed, stride length and by Cools 3 and Horstink.24 In addition the me-
cadence. chanism behind external cueing remains unclear.
Although many studies have found significant The present study has some limitations. The
improvements of gait, evidence for this can not be review based itself on a restricted number of
established, due to the low methodological quality languages within a limited number of electronic
of these studies, therefore pooling of the studies for databases. Some relevant studies may therefore
quantitative meta-analysis was not possible. Steult- have been missed. In addition, the precise way of
jens et al.27 compared effect-sizes with the levels of cueing as well as appended instruction to the cued
evidence found for the different interventions in patient was not always clear in found studies. This
their study and concluded that the levels of might have resulted in misclassification of the
evidence confirmed the findings found with a intervention type. Further studies should evaluate
meta-analysis, underpinning the reliability of the the effects of different types of cueing on gait-
method used in the current study. related activities in the patient's own home situa-

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710 I Lini et al.

tion and community, in a well-conducted RCT, onset of freezing in Parkinson's disease. Mot Disord
including measurements related to ADLs, falling, 2001; 16: 1066-75.
freezing and perceived quality of life in general. 12 Keranen T, Kaakkola SR Sotaniemi K et ad.
Economic burden and quality of life impairment
increase with severity of PD. Parkoinsonism Re/it
Di6sord 2003; 9: 163 68.
Acknowledgements 1 Findley L, Aujla M, Bain PG e a. Direct economic
This research project was supported by a grant impact of Parkinson's disease: a research survey in
the United Kingdom. Mo1 Disord 2003; 18: 1139
from the European Commission (QLK6-CT-2001- 45.
00120; Rehabilitation in Parkinson's Disease: Stra- 14 Keller 5, Kessler T, Meuser T, Fogel V, Bremen D,
tegies for Cueing). We would like to thank Jost WH. [Analysis of direct costs in therapy of
0 Drummel and S Bleek for doing the literature Parkinson disease]. Nervenar:t 2003; 74: 1105609.
searches. 15 Dean KOH, Jones D, Ellis-Hill C, Clarke CE,
Playford ED, Ben-Shlomo Y A comparison of
physiotherapy techniques for patients with
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Appendix 1 - Best-evidence synthesis

Strong evidence Provided by consistent, statistically significant findings in outcome measures in at
least two high-quality RCTs'
Moderate evidence Provided by consistent, statistically significant findings in outcome measures in at
least one high-quality RCT and at least one low-quality RCT or high-quality CCT'
Limited evidence Provided by consistent, statistically significant findings in outcome measures in at
least one high-quality RCT
or
Provided by consistent, statistically significant findings in oatcotie measures in at
least two high-quality RCTs (in absence of high-quality RCTs)

Indicative findings Provided by consistent, statistically significant findings in outcome and/or process
measures in at least one high-quality CCT or low-quality RCTV'(in the absence of
high-quality RCTs)
or
Provided by consistent, statistically significant findings in outcome and/or process
measures in at least two noncontrolled studies with sufficient quality (in absence of
RCTs and CCTs)
No or insufficient In the case that results of eligible studies do not meet the criteria for the above
evidence stated levels of evidence
In the case of conflicting results (statistically significant positive and statistically
significant negative) results among RCTs and CCTs
In the case of no eligible studies
RCT, randomized controlled trial; CCT, controlled clinical trial.
'If the number of studies that show evidence is < 50%o of the total number of studies found within the
same category of methodological quality and study design (RCTs, CCTs or noncontrolled studies), no
evidence will be stated.

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 Cueing in patients ivith Parkinson's disease 7 1-

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