The Effect of Visual and Auditory Cueing Walker on

Gait in İndividuals with Parkinson's Disease

Experiencing Freezing of Gait
Neslihan Altuntaş YILMAZ

Necmettin Erbakan University

Muazzez Betigül ÇORBACIOĞLU
Necmettin Erbakan University
Ahmet Can YETİM
Necmettin Erbakan University
Abdurrahman Talat ARSLAN
Necmettin Erbakan University
İrem KARAKÜLAH
Necmettin Erbakan University

Research Article

Keywords: Auditory and Visual cue, Gait, Parkinson's disease, Walker

Posted Date: April 9th, 2024

DOI: https://doi.org/10.21203/rs.3.rs-4206782/v1

License:   This work is licensed under a Creative Commons Attribution 4.0 International License.
Read Full License

Additional Declarations: No competing interests reported.

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Abstract
Objective
The aim of this study was to investigate the effects of a visual and auditory cueing walker on freezing of
gait during walking in patients with Parkinson's disease (PDF), compared to Parkinson patients without
freezing of gait (PDNF). Design: Eighteen PDF and 12 PDNF were included in the study. Participants
walked back and forth on a 7-meter walking path under two different conditions: without cues and with a
walker providing visual and auditory cues. To assess the risk of falls in both groups, the "Tinetti Balance
and Gait Assessment" was conducted. Additionally, the "Dynamic Gait Index" was used to evaluate the
ability to adapt walking to varying task demands, and the Timed Up and Go Test (TUGT) was employed
to determine walking speed.

Results
In the PDF group, visual and auditory cueing walker significantly decreased walking speed, but improved
fall risk and walking adaptation. However, for the PDNF group, fall risk was unaffected, walking speed
decreased, yet walking adaptation improved. When compared between the two groups, the visual and
auditory cueing walker had a more positive effect on the PDF group.

Conclusions
This study suggests that a walker providing visual and auditory cues may improve daily walking in
patients with Parkinson's disease with freezing of gait (PDF) and reduce the risk of falls in patients with
Parkinson's disease without freezing of gait (PDNF) who exhibit hypokinetic gait patterns.

Introduction
One of the most significant issues experienced by Parkinson's disease (PD) patients is gait disturbance1.
This disturbance is characterized in various ways: (1) short and rapid stepping with dragging of the feet,
(2) decreased swinging of the arms with the trunk flexed forward, (3) difficulty initiating or changing
walking, freezing of gait2. As the disease progresses, walking speed gradually decreases 3.

Especially as the disease progresses, freezing of gait (FOG) can lead to injuries in Parkinson's patients4.
Research on the pathophysiology and treatment of FOG has recently intensified. However, evaluating it is
challenging due to its unpredictable and intermittent nature, making it very difficult to capture true
spontaneous freezing. FOG most commonly occurs at home, during unobserved behaviors, and in
response to specific environmental triggers, and rarely manifests in walking laboratories 5.

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Typically, freezing of gait (FOG) lasts for a few seconds, but this transient episode can sometimes exceed
30 seconds6. In rare cases, the patient may be unable to take any effective steps for several minutes or
longer until compensatory strategies such as cueing are provided 7. FOG leads to significant falls in
patients with Parkinson's disease (PD)8, which deeply diminishes their independence and mobility,
significantly impairing their quality of life 9.

Recent studies have demonstrated that external stimuli such as visual or auditory cues reduce freezing of
gait (FOG) in Parkinson's patients 10–12. These approaches are based on teaching patients to shift their
walking control from a "habitual" control to a "goal-directed" control in order to reduce and overcome FOG
episodes 13.

It was found that visual cues improved the hypokinetic spatiotemporal walking pattern in individuals with
Parkinson's disease (PH). Freezing of gait (FOG) attacks occur more frequently when step length is
shortened 14. Additionally, studies have indicated positive effects on reducing freezing when the
frequency of auditory signals is reduced 15. Despite these positive outcomes demonstrating the
improvement of gait disturbances in Parkinson's patients with FOG using visual and auditory cues, we did
not come across research comparing the effectiveness of combined visual and auditory cues in the
"freezing" and "non-freezing" groups. Therefore, there is a need to compare the effectiveness of goal-
directed visual and auditory cues between patients with Parkinson's disease with freezing of gait (PDF)
and without freezing of gait (PDNF).

The aim of this study is to compare the effects of a walker providing visual and auditory cues on PDNF
with PDF. We quantitatively compared the risk of falls, walking speed, and the ability to adapt walking to
varying task demands between PDF and PDNF.

Methods
Design
This is an interventional, single-blinded study. Written informed consent was obtained from all
participants before the procedures started. This study conforms to all CONSORT guidelines and reports
the required information accordingly. Sample size was calculated to detect a difference of 0.37 m/sec on
mean velocity, with a deviation of 0.3 m/sec, two-sided 5% significance level, and power of 90%.
Considering the expected 10% dropout rate, twelve subjects were included.

Researcher R1 determined whether the subject was eligible for inclusion in the trial and researcher R2
carried out the gait analysis. Both examiners were unaware of group allocation. An independent
researcher (R3) performed the clinical evaluation before the procedures started.

Participants

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Thirty Parkinson's patients were referred from the XXX Medical Center to the Parkinsonism and Other
Movement Disorders Center of XX. The diagnosis of PH was established by three specialists from the
Neurology Department based on the United Kingdom Parkinson's Disease Society Brain Bank criteria16.
Patients with secondary parkinsonism, severe systemic diseases, psychiatric illness, cognitive
impairment (Mini-Mental State Examination score < 24), hearing and vision loss, musculoskeletal
problems, or symptoms suggestive of cerebellar dysfunction were excluded from the study. Patients with
any abnormal signal changes or focal atrophy detected on brain magnetic resonance imaging were also
excluded. Those with a Hoehn-Yahr classification between 2.5 and 4 were included in the study.

The 30 PD patients consisted of 18 PDF (7 men, 11women; mean age, 62.7 ± 8.6 yrs) and 12 PDNF (7
men, 5women; mean age, 61.6 ± 5.8yrs). The diagnosis of FOG was based on patient history, responses
on the FOG questionnaire 17 and scoring on the Unified Parkinson's Disease Rating Scale (UPDRS) part II
18, and Hoehn & Yahr staging was also conducted for patients19.

A levodopa equivalent dose was calculated as follows: levodopa equivalent dose = (standard levodopa
dose × 1) + (slow-release levodopa dose × 0.75) + (bromocriptine dose × 10) + (ropinirole dose × 20) +
(pergolide dose × 100) + (pramipexole dose × 100). If entacapone was used, the levodopa equivalent
dose was the standard levodopa dose + (slow-release levodopa dose × 0.75). This study was approved
by the ethics committee of our institute, and all subjects provided written informed consent.

Interventions
A visual and auditory sensor-equipped walker was designed. Sensors were placed on all four contact
surfaces of the walker. When all four sensors come into contact with the ground, a simultaneous "beep"
sound and a red light placed on the front of the walker illuminate. Therefore, participants were instructed
to ensure that all four legs of the walker make contact with the ground. To reduce the gait disturbance
and balance issues resulting from festinating gait (FG) characteristic of Parkinson's patients, where step
width decreases (amplitude) and step frequency increases, four sensors were placed on all feet of the
walker. Thus, participants were aimed to take steps with auditory and visual cues only after placing all
feet of the walker on the ground (Fig. 1).

All subjects completed gait cycles defined as walking back-and-forth once between two points spaced 7
meters apart. This was performed under two different conditions: initially without cues, and then with a
walker providing visual and auditory cues.

Before the test, subjects were given the opportunity to experience each condition. In each condition, the
total duration per cycle was recorded by the researcher20. All patients were on stable medication use and
were tested during the "off" phase of medication cycles because higher frequency of freezing in open
spaces in PD patients was reported during the "off" phase21.
Evaluation

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All subjects underwent the "Tinetti Balance and Gait Assessment" (TBGA) to measure the risk of falls for
both conditions22. Additionally, the " Functional Gait Assessment” (FGA) was used to evaluate the ability
to adapt walking to varying task demands 23, and the “Timed Up and Go Test” (TUGT) was conducted to
determine walking speed 23.

TBGA; this scale consists of two sections assessing gait and balance. The first nine questions concern
balance, and the following seven concern gait. The total possible score is 28 with 12 points in the gait
scale and 16 in the balance scale. Low scores are predictive of balance and gait disorders and an
associated risk of falls 24.

FGA was used to assess gait. The FGA consists of 10 items in which the patient walks under increasingly
difficult conditions, such as pivoting or walking with eyes closed. Each item is scored from zero to 3, in
which a score of zero indicates an inability to perform the task, while 3 is normal. According to the FGA,
the best score is the maximum of 30 25.

TUGT is conducted as follows: Let the patient seated in a chair with armrests stand up independently,
walk forward 3 m, walk back to the chair, and sit down, while being timed. A total of 3 tests are conducted
at an interval of 1 min, and the mean time is used. The test is done independently under guardianship.
Guardians do not make any physical contact with the patient to avoid giving any practical assistance. In
2013, a systematic review26 indicated that the TUGT is a sensitive assessment for gait and balance
evaluation. A previous study also found that the TUGT had high reliability (ICC > 0.87) for assessing
balance in people with PD 27.
Statistical Analysis
The data obtained were analyzed using the Statistical Package for the Social Sciences (IBM SPSS
Statistics for Windows, IBM Corp., Armonk, NY, United States) software, version 21.0. The Mean, standard
deviation, median, maximum, and minimum values were calculated for all parameters. The Shapiro-Wilk
test was first applied to analyze the normality of the distribution between the two groups. Nonparametric
data was analyzed with using the Wilcoxon signed-rank test to investigate difference within the groups,
and the paired sample t-test was used to compare intragroup changes in normally-distributed variables.
Two independent t-tests were used to compare the means between the groups for the normally-
distributed data. The nonparametric Mann-Whitney U test was used to investigate potential differences
between the groups regarding nonparametric variables without normal distribution. The results were
evaluated using a 95% confidence interval and values of p < 0.05 were considered statistically significant.

Results
Thirty subjects from two groups (18 PDF, 12 PDNF) completed the walking cycle under two different
conditions: without the device, and with the visual and auditory cueing walker. There was a difference
between the two groups in terms of Levodopa dose (mg) and freezing scores (P < 0.001), while no
difference was found in other initial evaluation parameters (P > 0.05) (Table 1).
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 Table 1
Shows the demographic characteristics of all subjects.
PDF (n = 18) PDNF (n = 12) P

Age ,yrs 63.7 ± 7.8 61.9 ± 4.5 0.213

Sex, M/F 12:6 8:4 0.348

Height, cm 168.2 ± 4.1 163.8 ± 3.7 0.548

Weight, kg 66.8 ± 5.8 64.7 ± 4.2 0.476

Hoehn and Yahr Grade 3.98 ± 0.79 2.77 ± 0.69 0.248

Disease duration, yrs 8.2 ± 2.5 4.2 ± 3.2 0.076

UPDRS II score 13.7 ± 3.8 5.7 ± 3.6 0.006

UPDRS III score 18.6 ± 7.4 16.8 ± 7.2 0.589

Levodopa dose,mg 576.4 ± 184.7 245.0 ± 186.4 ˂0.001

Freezing score 11.7 ± 4.5 2.7 ± 1.2 ˂0.001

Value are expressed as mean ± SD, PDF, Parkinson disease with freezing of gait ; PDNF, Parkinson
disease wirhout freezing of gait; UPDRS, Unified Parkinson Disease Rating Scale.

The evaluation conducted with the visual and auditory cueing walker revealed significant differences in
fall risk, walking adaptation, and walking speed in the PDF group (p < 0.05), while significant increases
were found in walking speed and walking adaptation in the PDNF group (p < 0.05). When comparing the
scores of both groups in assessments with and without the walker, only the PDF group showed favorable
results in terms of fall risk (Table 2).

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 Table 2
Comparisons of results between the 2 groups (mean ± SD).
PDF (n = 18) PDNF (n = 12) P

TBGA Walker with 20.31 ± 1.02 22.23 ± 2.30 0.031b

Without walker 23.44 ± 2.03 23.70 ± 2.14

P 0.031a 0.064a

TUGT Walker with 24.11 ± 5.12 22.07 ± 3.16 0.487b

Without walker 28.64 ± 4.02 26.37 ± 4.11

P 0.021a 0.041a

FGA Walker with 15.68 ± 2.63 17.35 ± 3.42 0.151b

Without walker 21.31 ± 4.12 19.21 ± 2.54

P 0.011a 0.037a

a:Wilcoxon signed-rank test; b:Mann-Whitney U test. TBGA– Tinetti Balance and Gait Assessment;
TUGT – Timed ‘Up and Go’ Test; FGA; Functional Gait Assessment

Discussion
This study demonstrated that the visual and auditory sensor-equipped walker designed for patients with
Parkinson's disease freezing of gait (PDF) improved walking and balance. The results showed
improvement in the Tinetti Balance and Gait Assessment (TBGA) score and Functional Gait Assessment
(FGA) score in the FOG group, while there was an increase in the Timed Up and Go Test (TUGT) time. In
Parkinson's disease patients without freezing of gait (PDNF), improvement in the Functional Gait
Assessment (FGA) score was observed, accompanied by an increase in walking time in this group.

The existing studies have separately evaluated auditory and visual stimuli in the PDF group, finding that
both stimuli contribute to improving walking levels 28–31. Taking these studies into consideration, we
have developed a walker for PH that provides these two stimuli and also reduces the risk of falling in
daily life.

Technological advancements provide opportunities not only to change the way cues are delivered but
also to adapt the content of cues. There is a study reporting that auditory cues are ineffective in
individuals with Parkinson's disease experiencing freezing of gait if they do not mimic real walking
sounds 32. Therefore, we aimed to provide both

In a study conducted with wearable sensor-equipped garments (smart verbal cues), it has been tested on
patients with freezing episodes, indicating that these patients showed less gait deviation 33. However, it

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has been reported that patients do not particularly prefer to use this smart verbal cue system. Especially,
it has been reported that the smart verbal cue system causes fatigue in patients 34. Similarly, in our study,
although the cue was found to reduce the risk of falls in patients and increase their ability to adapt to
different movements along with walking, it may have caused patients to slow down their walking speed,
which could be a reason for them not to use this developed walker.

Postural control and balance 35 were affected more significantly in PD patients with FOG compared with
non-FOG group. FOG often occurs when turning also suggests that the postural control impairment
probably contributes to freezing. However, whether balance impairment is an accompanying symptom of
FOG or a risk factor of FOG remains unclear. We found that the walker we developed reduced the risk of
falls in both PDF and PDNF patients, where the risk of falling is a concern.

Janssen et al. (2020) reported that visual stimuli provided through virtual reality did not affect patients'
freezing of gait (FOG) and even prolonged turning duration36. Our study similarly found that walking
speed decreased in all Parkinson's patients, supporting this finding.

The effect of walking cues in patients with Parkinson's disease has been evaluated in the literature.
However, there are few studies that assess the combined effect of both cues. One such study conducted
by Suteerawattananon et al. (2004) reported that cues improved walking in Parkinson's disease patients,
with visual cues alone improving step length, auditory cues alone improving walking pace, and the
combination of both cues being much more effective than cues given individually1. However, this study
was not conducted in patients with freezing. Another study conducted in patients with freezing37
evaluated walking by stimulating patients' feet with mechanical pressure applied to the sole, resulting in
sensory feedback upon contact with the ground. This study indicated that peripheral stimulation
improved walking parameters in patients with freezing.

Conclusions
It has been determined that the visual and auditory sensor-equipped walker designed for Parkinson's
patients has a positive effect on reducing the risk of falls and the ability to adapt to different tasks during
walking, but it reduces walking speed.

In patients with PD, we found that the visual and auditory cueing walker reduced the risk of falls,
improved walking adaptation, but decreased walking speed, indicating an increase in walking duration.
However, in patients with PDNF, we determined that this cueing walker had no effect on fall risk, only
benefiting walking adaptation, but increasing walking duration.

The first limitation of this study is that participants were not selected based on known cue sensitivity. The
fact that our participants may not be accustomed to using cues could be due to their unfamiliarity with
cues, and it may also be related to a resistance they have previously experienced to cue effects. Selecting
only those patients with a recognized response to cues would increase the potency of experimental cues,

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but reduce generalizability of the results to patients with an unknown response to cues. A second
limitation to this study is the relatively small sample size. The impact size of Walker's visual and auditory
cues may be smaller than anticipated and may require a larger sample size to detect statistically
significant differences.

This study found that providing goal-oriented visual and auditory cues together is beneficial for walking
safety in freezing of gait (FOG) patients. However, it may influence patient preference due to its effect of
slowing down walking speed. Nevertheless, especially in patients with Hoehn & Yahr stages 4 and above,
the use of a walker designed for safety should be recommended.

Declarations
Ethics approval and consent to participate

This study was conducted in accordance with the rules of the Helsinki Declaration (1964), approved by
the Medical Ethics Committee (Necmettin Erbakan University-Health Sciences Scientific Research Ethics
Committee), and registered in the research registry (2022/339: ID 12168). Written informed consent was
obtained from all participants before they were included in the study.

Consent for publication

Not applicable

Availability of data and materials

The data presented in this study are available on appropriate request from the corresponding author. The
data are not publicly available as the privacy of the human subjects must be ensured.

Competing interests

The authors have no conficts of interest.

Funding

We would like to thank the Publikationsfond of the Turkish Scientific and Technological Research Council
for funding the publication of this paper.

Authors' contributions

NAY and MBÇ were involved in the conception and design of the study, the acquisition, analysis, and
interpretation of the data, writing of the manuscript, and editing of the final manuscript for submission.
ACY, ATA, İK were involved in the design and building of the walker. NAY, İR were involved in the analysis
of the data and critical appraisal of the manuscript. MBÇ critically appraised the manuscript. NAY and İK
were involved in the conceptual design and setup of this study, the analysis and interpretation of the data,

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critical revision of the manuscript, and supervision over the study. All authors read and approved the final
manuscript.

Acknowledgments

We would like to individually thank all our participants, and we also extend our gratitude to the Hospital
administration for their support in this study. We thank TÜBİTAK (The Scientific and Technological
Research Council of Turkey) for their funding support in the design of the walker.

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Figures

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Figure 1

A. 4 contact-sensitive sensors. B. Placement of sensors on the walker. C. Representation of the buzzer

sound circuit, power source, and the light on the front panel.

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