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Abstract and Figures

Study of balance and gait deficits associated with vestibulopathy is important for improving clinical care and is critical to our understanding of the vestibular contributions to gait and balance control. Previous studies report a speed-dependency of the vestibular contributions to gait, so we examined the walking speed effects on gait variability in healthy young and older adults and in adults with bilateral vestibulopathy (BVP). Forty-four people with BVP, 12 healthy young adults and 12 healthy older adults completed walking trials at 0.4m/s to 1.6m/s in 0.2m/s intervals on a dual belt, instrumented treadmill. Using a motion capture system and kinematic data, the means and coefficients of variation for step length, time, width and double support time were calculated. The BVP group also completed a video head impulse test and examinations of ocular and cervical vestibular evoked myogenic potentials and dynamic visual acuity. Walking speed significantly affected all assessed gait parameters. Step length variability at slower speeds and step width variability at faster speeds were the most distinguishing parameters between the healthy participants and people with BVP, and within people with BVP with different locomotor capacities. We observed for step width variability, specifically, an apparent persistent importance of vestibular function at increasing speeds. Gait variability was not associated with the clinical vestibular tests. Our results indicate that gait variability at multiple walking speeds has potential as an assessment tool for vestibular interventions. New & Noteworthy Walking speed significantly but differentially affects gait variability in healthy adults and in adults with bilateral vestibulopathy. Gait variability at different speeds distinguishes between participants with and without bilateral vestibulopathy, but also between more and less able walkers with bilateral vestibulopathy. Specifically, for step width variability, an apparent persistent importance of vestibular function at increasing walking speeds was observed. Gait variability was generally not correlated with clinical tests of vestibular function.
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Is faster always better? The walking speed-dependency of gait
variability in bilateral vestibulopathy
Christopher McCrum1,2*, Florence Lucieer3, Raymond van de Berg3,4, Paul Willems1, Angélica
Pérez Fornos5, Nils Guinand5, Kiros Karamanidis6, Herman Kingma3,4, Kenneth Meijer1
1Department of Nutrition and Movement Sciences, NUTRIM School of Nutrition and Translational Research in
Metabolism, Maastricht University Medical Centre+, Maastricht, The Netherlands
2Institute of Movement and Sport Gerontology, German Sport University Cologne, Germany
3Division of Balance Disorders, Department of Otolaryngology, Head and Neck Surgery, Maastricht University
Medical Centre+, Maastricht, The Netherlands
4Faculty of Physics, Tomsk State University, Tomsk, Russian Federation
5Service of Otorhinolaryngology and Head and Neck Surgery, Department of Clinical Neurosciences, Geneva
University Hospitals, Geneva, Switzerland
6Sport and Exercise Science Research Centre, School of Applied Sciences, London South Bank University,
London, UK
Running head: Gait variability in bilateral vestibulopathy
*Correspondence:
Christopher McCrum
Department of Nutrition and Movement Sciences
Maastricht University,
PO Box 616, Maastricht, 6200 MD, The Netherlands
chris.mccrum@maastrichtuniversity.nl
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Abstract
Study of balance and gait deficits associated with vestibulopathy is important for improving clinical care and is
critical to our understanding of the vestibular contributions to gait and balance control. Previous studies report a
speed-dependency of the vestibular contributions to gait, so we examined the walking speed effects on gait
variability in healthy adults and in adults with bilateral vestibulopathy (BVP). Forty four people with BVP and 12
healthy adults completed walking trials at 0.4m/s to 1.6m/s in 0.2m/s intervals on a dual belt, instrumented
treadmill. Using a motion capture system and kinematic data, the means and coefficients of variation for step
length, time, width and double support time were calculated. The BVP group also completed a video head impulse
test and examinations of ocular and cervical vestibular evoked myogenic potentials and dynamic visual acuity.
Walking speed significantly affected all assessed parameters when considering all participants with BVP who
completed the protocol (26 participants), as well as when only considering the slower speeds (except for mean step
width). Step time and length variability at slower speeds and step width variability at faster speeds distinguished
between the healthy and BVP group that completed the measurements, and the BVP group that partially completed
the measurements. We observed for step width variability, specifically, an apparent persistent importance of
vestibular function at increasing speeds. Gait variability was not associated with the clinical vestibular tests. Our
results indicate that gait variability at multiple walking speeds has potential as an assessment tool for vestibular
interventions.
New & Noteworthy: Walking speed significantly but differentially affects gait variability in healthy adults and in
adults with bilateral vestibulopathy. Gait variability at different speeds distinguishes between participants with and
without bilateral vestibulopathy, but also between more and less able walkers with bilateral vestibulopathy.
Specifically for step width variability, an apparent persistent importance of vestibular function at increasing
walking speeds was observed. Gait variability was generally not correlated with clinical tests of vestibular function.
Keywords: locomotion, bilateral vestibulopathy, vestibular diseases, gait variability, falls
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Introduction
Ever since a chance observation of a dog with acute unilateral vestibulopathy who demonstrated less imbalance
during running than during walking (Brandt et al. 1999), the interactions of gait velocity, imbalance and vestibular
symptoms in people with vestibulopathy have become a topic of great interest. Inspired by the observation in the
dog, Brandt et al. (1999) demonstrated with a simple setup that humans with acute unilateral vestibulopathy could
run with less deviation to the affected side than while walking. Since then, three studies have reported reductions
in temporal gait variability and reductions in stride length variability in bilateral vestibulopathy (BVP) during
faster, compared to slower walking (Schniepp et al. 2017; Schniepp et al. 2012; Wuehr et al. 2016). However, the
same studies revealed that patients with BVP do not self-select walking speeds that minimize temporal or spatial
gait variability (Schniepp et al. 2017; Schniepp et al. 2012; Wuehr et al. 2016), which may suggest that these are
not the only source of instability or inefficiency with which people with BVP must cope. BVP, a severe bilateral
reduction of vestibular function that results in severe balance deficits and an increased risk of falls (Guinand et al.
2012a; Horak et al. 2016; Lucieer et al. 2016; Schlick et al. 2016; Sprenger et al. 2017; van de Berg et al. 2015),
was recently defined by the Bárány Society (Strupp et al. 2017) and represents one of the most debilitating
vestibular disorders. The study of the severe balance and gait deficits in people with BVP is both important for
improving clinical care and for objective quantification of the effects of novel interventions, such as vestibular
implants (Guyot et al. 2016; Lewis 2016). Furthermore, it is fundamental to our understanding of the vestibular
contributions to gait and balance control.
There are a number of changes in the control of gait with changes in walking speed that partly explain the
above described findings and will affect walking speed selection in people with vestibulopathy. The reduction in
sagittal plane spatial variability with increasing speed can partly be explained by passive dynamics (Collins et al.
2005; Kuo 2007; McGeer 1993). Additionally, changes in muscle activation (den Otter et al. 2004; Murley et al.
2014; Raffalt et al. 2017; Savelberg et al. 2010) and modular locomotor control (Ogawa et al. 2015; Yokoyama et
al. 2016; Yokoyama et al. 2017) with changes in walking speed have been observed. Furthermore, less utilization
of real-time sensory feedback at faster walking speeds may also affect changes in gait variability; visual (Jahn et
al. 2001; Wuehr et al. 2013) and vestibular (Fitzpatrick et al. 1999; Jahn et al. 2000) perturbations have less impact
on direction and variability at higher speeds, with the exception of step width variability, which appears to be more
affected by visual perturbation at faster walking speeds (Wuehr et al. 2013). It has also been reported that the
vestibular influence on lower limb muscles is selectively suppressed with increased cadence and speed during
walking (Dakin et al. 2013; Forbes et al. 2017), purported to be related to a shift in the control mechanisms of
mediolateral stability with increasing walking speeds from active stabilization at the lower limb joints during the
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stance phase to foot placement (Bauby and Kuo 2000; Dakin et al. 2013). Despite selective suppression of the
vestibular influence on some lower limb muscles at faster walking speeds, significant increases in frontal spatial
variability with increasing walking speeds have been reported in BVP (Wuehr et al. 2016), suggesting that
vestibular information remains important for mediolateral stability during gait at faster speeds.
In order to further investigate the walking speed dependency of gait variability in vestibulopathy, this
study analyzed the gait of people with BVP and of healthy control participants. We aimed to determine the effects
of systematic increases in walking speed on spatiotemporal gait parameters and their variability in these participant
groups. Secondly, we aimed to assess if these parameters would differentiate between healthy participants, and
participants with BVP who could and could not complete all of the planned walking speed trials (used here as a
simple proxy of locomotor capacity; see Methods). We hypothesized that, for all participants, temporal and sagittal
plane spatial gait variability would systematically reduce with increases in walking speed, whereas frontal plane
spatial gait variability would systematically increase, in agreement with previous work. We further postulated that
temporal and sagittal plane spatial gait variability at slower walking speeds would be most distinguishing between
the healthy control participants, the patients with BVP that could complete the measurement protocol, and the
patients with BVP that could only partially complete the measurement protocol, whereas frontal plane spatial gait
variability would be most distinguishing between all three groups at faster walking speeds. Gait variability in BVP
was generally not correlated with the clinical tests of vestibular function. The current findings indicate that analysis
of gait variability at multiple speeds has potential as an assessment tool for vestibular interventions.
Materials and Methods
Participants
Forty four people with BVP participated in this study (22 males, 22 females; age: 57.6±11.5 years; height:
174.5±9.7cm; weight: 80.4±17kg). Inclusion criteria were a prior diagnosis of bilateral vestibular hypofunction at
the Maastricht University Medical Centre+ (imbalance and/or oscillopsia during locomotion and summated slow
phase mean peak velocity of the nystagmus of less than 20°/s during bithermal caloric tests) and the self-reported
ability to walk independently without assistance. Please note that this study began prior to the publication of the
Bárány Society guidelines (Strupp et al. 2017), which are slightly different. Potential participants were not included
if they were unable or unwilling to stop taking anxiety or depression medication for the week before the
measurements. In addition, a healthy control group comprised of 12 healthy adults (5 males, 7 females; 25.1±2.8
years; 174.9±7.3cm; 72.6±13.5kg) with no history of balance or gait difficulties and no history of dizziness
participated in this study. The study was explained before obtaining written informed consent, was conducted in
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accordance with the Declaration of Helsinki and was approved by the Maastricht University Medical Centre
medical ethics committee (gait measurements: NL58205.068.16; vestibular tests: NL52768.068.15).
Gait Analysis Setup, Data Processing and Procedure
The gait measurements were conducted using the Computer Assisted Rehabilitation Environment Extended
(CAREN; Motekforce Link, Amsterdam, The Netherlands), which includes a dual-belt force plate-instrumented
treadmill (Motekforce Link, Amsterdam, The Netherlands; 1000Hz), a 12 camera motion capture system (100Hz;
Vicon Motion Systems, Oxford, UK) and a virtual environment (city-style street with passing objects and
structures) projected onto a 180 degrees curved screen (note that optic flow was turned off for the participants with
BVP to prevent dizziness and nausea). For all measurement sessions, a safety harness connected to an overhead
frame was used. At the request of some of the participants with BVP, a handrail was also positioned on the
treadmill, the use of which was monitored and recorded. Six retroreflective markers were attached to anatomical
landmarks (C7, sacrum, left and right trochanter and left and right hallux) and were tracked by the motion capture
system. Marker tracks were filtered using a low pass second order Butterworth filter (zero-phase) with a 12Hz cut-
off frequency. Foot touchdown was determined using combined force plate (50N threshold) and foot marker data
(Zeni et al. 2008). This combined method was used to be able to accurately account for foot touchdowns and toe-
offs occurring in the center of the treadmill triggering both force plates simultaneously. For these steps, the foot
marker method was used and then corrected based on the average discrepancy between the force plate method and
the marker method timing for all steps that contacted only one force plate. The spatiotemporal gait parameters of
interest were step length (anteroposterior distance between the hallux markers at foot touchdown), step time (time
from touchdown of one foot to touchdown of the next foot), step width (mediolateral distance between the hallux
markers at foot touchdown) and double support time (time spent with both feet on the ground). Means, standard
deviations and coefficients of variation (CV) were determined for each speed for each participant.
Each session began with walking familiarization trials at 0.4m/s up to 1.6m/s in 0.2m/s intervals. At least
60s were used for each speed, and further time was provided to familiarize to each speed if deemed necessary by
either the participant, the CAREN operator or the research clinician. At the end of each speed trial, the decision to
continue to the next (faster) speed was made in a similar manner. If the patient was not comfortable progressing
to the next speed or if the CAREN operator or research clinician did not think it was safe or feasible to progress,
then the participant continued at the current speed instead. Participants were then given sufficient rest before
continuing with the measurements. Single two-to-three minute long measurements (to ensure a minimum of 60
strides per speed) were then conducted at each prescribed speed that was completed during familiarization.
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Multiple set walking speeds were used as opposed to the majority of previous studies which have used either
percentages of preferred walking speeds or self-perceived slow, normal and fast walking speeds, in order to have
more control over the walking speed condition.
Clinical Vestibular Function Tests Setup and Procedures
We aimed to conduct an explorative analysis in the patient groups by examining correlations between the outcomes
of the most distinguishing gait parameters identified and clinical vestibular tests (video head impulse test [vHIT],
ocular and cervical vestibular evoked myogenic potentials [oVEMP and cVEMP] and dynamic visual acuity
[DVA]) that are indicative of vestibular functional integrity.
The vHIT was performed with the EyeSeeCam system (EyeSeeCam VOG; Munich, Germany) and the
ICS Impulse system (GN Otometrics A/S, Denmark). Both systems measured the movement of the right eye. The
distance of the back of the static chair was 2 meters to the point of fixation. The point of fixation consisted of a
green dot on the wall, produced by a laser on a tripod. If necessary, adhesive plasters were used to lift the upper
eyelid a little to secure the visibility of the pupil for the camera in all directions. Goggle movement was minimized
by adjusting the strap of the goggles to every subject. The vHIT system was calibrated according to the protocol
of the system. After calibration, the subject was instructed to not touch their head including the goggles. The
examiner stood behind the participant with two hands firmly on top of the participant’s head without touching the
strap of the goggles. The examiner then applied head impulses in six different movements to test each canal
(McGarvie et al. 2015). The horizontal head impulses comprised a peak velocity of > 150°/s and the vertical head
impulses a peak head velocity of > 100°/s. The amplitude of the movements was 10-20°. Only outward impulses
were used (van Dooren et al. 2018). The vHIT was defined as abnormal if the VOR-gain was below 0.7 and/or if
covert saccades were observed in 50% or more of the traces (McGarvie et al. 2015; Yip et al. 2016).
DVA was assessed on a regular treadmill (1210 model, SportsArt, Inc., Tainan, Taiwan, China.) with the
participant positioned 2.8 meters from a computer screen. Firstly, the static visual acuity was determined during
stance, followed by the assessment of the DVA during walking at 2, 4 and 6 km/h. One letter at a time was
randomly displayed on the screen from a chart of Sloan letters (CDHKNORSVZ; Sloan 1959). Starting at a
logMAR (log of the Minimum Angle of Resolution; (Bailey and Lovie 1976)) of 1.0, five random letters were
shown at each logMAR (decreasing in steps of 0.1 logMAR). When four out of five letters were correctly
identified, the corresponding logMAR was considered achieved. The outcome of the DVA was the difference
between the static logMAR and the logMAR for each of the three walking speeds. The result was omitted if the
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subject needed a handrail to walk at that speed or if it wasn’t possible to walk at that speed at all (Guinand et al.
2012b).
cVEMP and oVEMP were assessed with the Neuro-Audio system (v2010, Neurosoft, Ivanovo, Russia).
A monaural stimulation with in-ear earphones was used with air conduction tone bursts at 500Hz and a stimulation
rate of 13Hz using a blackman window function with a two-cycle rise/fall and no plateau phase. Tone bursts of
maximum 130dB sound pressure level (SPL) were used. A stepwise approach was used to determine the threshold
with a precision of 5dB SPL (van Tilburg et al. 2016). Positive (P1) and negative (N1) peaks in the recorded
biphasic waveform were marked for both cVEMPs and oVEMPs. The thresholds were determined as the lowest
stimulus intensities to elicit recognizable peaks. If it wasn’t possible to find a VEMP response, it was defined as a
threshold of >130dB SPL. For the cVEMP, the participant was positioned lying down with the back positioned at
a 30° angle above the horizontal plane and was asked to turn their head towards the non-measured side and lift
there head during the measurement. The cVEMP was recorded at the ipsilateral sternocleidomastoid muscle. Two
electrodes were placed on the sternocleidomastoid muscles, the reference electrode on the sternum, and the earth
electrode on the forehead. Electrode impedances of 5 kΩ or lower were accepted and otherwise the electrode was
replaced. To ensure correct muscle contraction, a feedback system using a screen was provided. An average of
200 EMG traces with a minimum mean rectified voltage (MRV) of 65µV and a maximum MRV of 205µV was
accepted (Brantberg and Lofqvist 2007; Fujimoto et al. 2009). The oVEMP was recorded at the contralateral
inferior oblique muscle. Five electrodes were used: the recording electrodes beneath the eyelid, just lateral of the
pupil when gazing forward and centrally, the reference electrodes beneath the recording electrode and the earth
electrode on the forehead. The participant was asked to keep their gaze at a focus point placed at a 30 degrees
angle behind the head. An average of at least 300 EMG traces was accepted (Govender et al. 2011; Piker et al.
2013; Valko et al. 2016).
Statistics
From the 44 participants with BVP that started the study, three groups were formed. One group was able to
complete all of the gait measurements without assistance (BVP All Gait; n=26), the second was only able to
complete some of the speeds without assistance (BVP Part Gait; n=12; all of this group were able to complete the
measurements at least up to 0.8m/s) and the final group (BVP No Gait; n=6) did not start the recorded gait trials
(see “Results” for details on this group).
To investigate the effects of walking speed on gait and this effect’s potential interaction with vestibular
function, a two way repeated measures ANOVA with walking speed (0.4 to 1.6m/s) and group (healthy control
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and BVP All Gait) as factors was conducted for the means and CVs of step time and length, step width and double
support time. To further investigate the potential of the gait parameters to distinguish between groups, a two way
repeated measures ANOVA with walking speed (0.4 to 0.8m/s) and group (healthy control, BVP All Gait and BVP
Part Gait) as factors was conducted for the means and CVs of step time and length, step width and double support
time. Bonferroni post hoc tests were performed when significant effects or interactions were found with the
ANOVAs.
The vHIT testing revealed abnormal canal function in all or most directions for almost all of the
participants with BVP (i.e. exceptions were two participants with BVP who had only one abnormal result out of
six). As almost all outcomes were abnormal and there was no possibility to distinguish between groups, analysis
of the vHIT results in relation to gait was not taken further. For all completed DVA trials with a logMAR change
value during the three walking speeds compared to standing and when oVEMP or cVEMP thresholds were
detected, these values were grouped and Pearson correlations with the gait parameters that were most
distinguishing between the groups were conducted (see Results). Age, height, weight and body mass index (BMI)
were compared across the three BVP groups (BVP All Gait, BVP Part Gait, BVP No Gait) using one way
ANOVAs with Bonferroni corrections for multiple comparisons.
Results
Twenty six participants with BVP were able to complete all of the gait measurements without assistance (BVP All
Gait). Twelve participants with BVP were only able to complete some of the speeds (BVP Part Gait), of which
one participant stopped after 0.8m/s, one after 1.0m/s, four after 1.2m/s and six after 1.4m/s. Six participants with
BVP were assigned to the BVP No Gait group for the following reasons: one participant became dizzy and
nauseated during familiarization and could not continue; three participants were not able to walk during
familiarization without handrail support; two participants found treadmill walking too challenging and could not
continue. The demographic data of these three groups, as well as the healthy control group can be found in Table
1. No significant differences in demographics were found between the BVP groups.
Table 1. Participant Group Characteristics
n
Age (y)
Height (cm)
Weight (kg)
Body Mass Index
Healthy
12 (7 female)
25.1 ± 2.8
174.9 ± 7.3
72.6 ± 13.5
23.6 ± 2.8
BVP All Gait
26 (10 female)
55.1 ± 11.4
176.8 ± 9.9
80.3 ± 17.8
25.4 ± 3.8
BVP Part Gait
12 (10 female)
59.2 ± 9
169.7 ± 9
79.9 ± 18
27.6 ± 4.7
BVP No Gait
6 (2 female)
65.3 ± 13.6
174 ± 6.9
82.4 ± 13.4
27.2 ± 3.8
Values are means ± SD
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The two way repeated measures ANOVA with walking speed (0.4 to 1.6m/s) and group (healthy control
and BVP All Gait) as factors revealed significant walking speed effects for the means and CV of step time and
length, step width and double support time (P<0.0001), significant group effects for all parameters except step
width means (P≤0.0068) and significant walking speed by group interactions for the means of step time, double
support time and step width (P≤0.001) and the CV of step width (P<0.0001). The ANOVA results and between-
group Bonferroni post-hoc test results are displayed in Fig. 1.
Fig. 1. Median and 95% confidence interval bands of the BVP All Gait (blue circles) and Healthy (green squares)
groups for the individual means (top row) and coefficients of variations (bottom row) for step time, step length,
double support time and step width across all conducted walking speeds. S: Speed Effect. G: Group Effect. I:
Speed by Group Interaction. *,**,***,****: Statistically significant group difference (P<0.05, P<0.01, P<0.001
and P<0.0001, respectively).
The two way repeated measures ANOVA with walking speed (0.4 to 0.8m/s) and group (healthy control,
BVP All Gait and BVP Part Gait) as factors revealed significant effects of walking speed for the means of step
time and length, and double support time, as well as the CV of all parameters (P<0.0001). Significant group effects
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were found for the means and CV of step time, step length and double support time (P≤0.0013) and significant
walking speed by group interactions were found for the means of step time, double support time and step width
(P≤0.006) and the CV of step width (P=0.0016). The ANOVA results, as well as the between group Bonferroni
post hoc results are displayed in Fig. 2.
Fig. 2. Median and 95% confidence intervals of the BVP All Gait (blue circles), BVP Part Gait (black triangles)
and Healthy (green squares) groups for the individual means (top row) and coefficients of variations (bottom row)
for step time, step length, double support time and step width across 0.4 to 0.8m/s. I: Speed by Group Interaction.
S: Speed Effect. G: Group Effect. *,**,***,****: Statistically significant differences between BVP All Gait and
Healthy groups; #, ##, ###, ####: Statistically significant differences between Healthy and BVP Part Gait groups;
v, v v, v v v , v v v v: Statistically significant differences between BVP All Gait and BVP Part Gait groups (all
P<0.05, P<0.01, P<0.001 and P<0.0001, respectively).
When cVEMP and oVEMP thresholds were detected, and when a speed of the DVA was completed, these
values were taken and Pearson correlations were conducted with the CVs of step time, step length and double
support time at 0.4m/s and the CV of step width at 1.6m/s, being the most distinguishing gait parameters from the
previous analysis. These results can be seen in Table 2.
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Table 2: Pearson correlations between the cVEMP and oVEMP thresholds, the change in logMAR scores during
each of the three DVA walking speeds and the gait parameters.
Step Time CV
0.4m/s
Step Length CV
0.4m/s
Double Support
Time CV 0.4m/s
Step Width CV
1.6m/s
r
0.08987
0.3259
0.2576
-0.3501
95% CI
-0.3935 to 0.5343
-0.1662 to 0.6881
-0.2379 to 0.6467
-0.7554 to 0.2489
P (two-tailed)
0.7229
0.1868
0.302
0.241
n
18
18
18
13
r
-0.2425
0.1195
-0.1732
-0.5043
95% CI
-0.659 to 0.2878
-0.3999 to 0.5808
-0.616 to 0.3528
-0.8362 to 0.09795
P (two-tailed)
0.3655
0.6595
0.5212
0.0945
n
16
16
16
12
r
0.4653
0.561
0.286
0.4649
95% CI
-0.7074 to 0.9554
-0.6361 to 0.9654
-0.7975 to 0.9329
-0.7076 to 0.9553
P (two-tailed)
0.4297
0.3251
0.6408
0.4301
n
5
5
5
5
r
-0.04995
0.7914
0.08001
-0.3605
95% CI
-0.6911 to 0.6352
0.2684 to 0.9541
-0.6169 to 0.7066
-0.8494 to 0.4614
P (two-tailed)
0.8985
0.0111
0.8379
0.3803
n
9
9
9
8
r
-0.1244
0.01669
-0.2151
-0.09623
95% CI
-0.4271 to 0.2034
-0.3046 to 0.3346
-0.5004 to 0.1123
-0.4662 to 0.3024
P (two-tailed)
0.4568
0.9208
0.1947
0.6401
n
38
38
38
26
r
0.06088
-0.1711
0.03413
0.2422
95% CI
-0.2639 to 0.3733
-0.4654 to 0.1572
-0.2887 to 0.35
-0.1602 to 0.5756
P (two-tailed)
0.7166
0.3043
0.8388
0.2332
n
38
38
38
26
r
-0.3145
-0.3199
-0.4338
-0.06129
95% CI
-0.6371 to 0.1018
-0.6406 to 0.09588
-0.7125 to -0.0369
-0.4803 to 0.3805
P (two-tailed)
0.1345
0.1275
0.0342
0.7918
n
24
24
24
21
Post-hoc Analysis of Gait Data based on VEMP Results
In order to further investigate differences within the patient group, we conducted an analysis of the gait data of the
participants with and without at least one detected VEMP threshold and compared these to the healthy participant
data for the same four parameters as the correlations: the CVs of step time, step length and double support time at
0.4m/s and the CV of step width at 1.6m/s. Given that all of the participants with no VEMP threshold detected
also had abnormal outcomes on the vHIT for most or all of the six directions tested, the purpose of this analysis
was to compare the gait of participants with and without detectable canal and otolith function. One way ANOVAs
with Bonferroni corrections did not reveal any significant differences between the participants with and without at
least one detectable VEMP threshold (0.2526<P<0.9999).
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Discussion
In this study, we aimed to determine the effects of systematic increases in walking speed on spatiotemporal gait
parameters and their variability in people with BVP. Specifically, we investigated if these parameters would
distinguish between healthy participants and participants with BVP who could and could not complete all of the
planned walking speed trials (a simple proxy of locomotor capacity). Our hypothesis, that temporal and sagittal
plane spatial gait variability would systematically reduce with increases in walking speed, whereas frontal plane
spatial gait variability would systematically increase, was confirmed as significant effects of walking speed were
found both when considering all of the assessed speeds in those participants who completed the protocol, as well
as when only considering the three slowest walking speeds. We additionally hypothesized that temporal and
sagittal plane spatial gait variability at slower walking speeds would be most distinguishing between the healthy
control participants, the patients with BVP that could complete the measurement protocol, and the patients with
BVP that could only partially complete the measurement protocol, whereas frontal plane spatial gait variability
would be most distinguishing between these groups at faster walking speeds. This hypothesis was also confirmed,
although frontal plane spatial variability was more distinguishing in the analysis including the faster walking
speeds.
Our secondary aim was to conduct an explorative analysis in the patient groups by examining correlations
between the outcomes of four clinical vestibular tests (vHIT, oVEMP, cVEMP, DVA) and the most distinguishing
gait parameters identified. Only one significant correlations between the change in logMAR scores during the
DVA and the gait parameters were found (6km/h and Double Support CV; Table 2). One significant correlation
of 16 was found between the VEMP thresholds and the gait parameters, but only nine pairs of data were included
in this test and if a Bonferroni correction is made for the p values of these 16 tests, it is no longer significant
(oVEMP Left and Step Length CV at 0.4m/s; Table 2). Even though this study clearly demonstrates the significant
contribution of vestibular function to gait (difference between healthy and BVP groups), our exploratory analysis
confirms the complex contribution of vestibular information during every-day activities and the difficulty in
translating current objective clinical measures to highly relevant patient symptoms.
Determining meaningful and distinguishing gait parameters in BVP is vital for the development of
interventions, as is using tasks that sufficiently replicate the day-to-day challenges of these patients, in order to
determine candidates for intervention and to assess the effect of those interventions. Two promising interventions
currently under development and investigation include noisy galvanic vestibular stimulation (nGVS) and
vestibular implants (Guinand et al. 2015; Guyot et al. 2016; Lewis 2016; Perez Fornos et al. 2017; Wuehr et al.
2017). Discussions of these treatment options can be found elsewhere (Guyot et al. 2016; Wuehr et al. 2017), but
13
in the context of this study, it is important to note that both options show early signs of utility for improving the
gait of people with BVP (McCrum et al. 2016; Wuehr et al. 2016). However, it remains to be seen if improvement
due to nGVS or a vestibular implant in steady state gait would likewise be seen in more dynamic locomotor task
performance, where even unilateral vestibulopathy leads to significantly poorer stability performance (McCrum et
al. 2014). Related to this, it should be noted that while this study examined spatiotemporal variability, differences
in dynamic gait stability were not directly assessed and the two are not necessarily equivalent (Bruijn et al. 2013;
Dingwell et al. 2001; Perry and Srinivasan 2017). The parameters presented here represent the amount of
variability in particular gait parameters, but do not necessarily indicate the overall stability of the participants.
Therefore, future work should investigate how dynamic gait stability is altered in BVP and how this is affected by
changes in walking speed.
The current study confirmed previous findings of reductions in temporal gait variability and reductions
in sagittal plane spatial gait variability in vestibulopathy during faster, compared to slower walking (Schniepp et
al. 2017; Schniepp et al. 2012; Wuehr et al. 2016). We extend these previous findings as the current study employed
fixed (not self-selected) speeds that were systematically increased, with 120 steps analyzed per speed, thereby
improving the reliability of the outcomes. Importantly, the current results further the previous findings by
additionally showing that these parameters are related to the locomotor capacities of people with BVP.
We also confirmed previously reported increases in frontal plane spatial variability with increasing
walking speeds in people with BVP (Wuehr et al. 2016). Previous studies have shown that vestibular perturbations
have less impact on direction and variability at higher walking speeds (Fitzpatrick et al. 1999; Jahn et al. 2000)
and that the vestibular influence on lower limb muscles is selectively suppressed with increased cadence and speed
during walking (Dakin et al. 2013; Forbes et al. 2017). However, the current step width variability results,
combined with those of (Wuehr et al. 2016) suggest that vestibular information remains important for mediolateral
stabilization at increased walking speeds. These results also provide some explanation as to why people with BVP
do not self-select walking speeds that minimize temporal or sagittal plane spatial gait variability (Schniepp et al.
2017; Schniepp et al. 2012; Wuehr et al. 2016). Dramatic increases in step width variability may be undesirable
due to reduced stability control or increased energetic costs of mediolateral stabilization (Dean et al. 2007; Donelan
et al. 2004; O'Connor et al. 2012). Based on the current results, either reason is plausible, as some of the participants
in the BVP Part Gait group did not continue to the faster speeds due to instability, while others could not continue
due to being unable to keep up with the speed of the treadmill (implying an energetic or physiological limitation,
not a stability-related one). The vestibular influence on gait economy has not yet, to our knowledge, been
thoroughly investigated, and is therefore an area for future research.
14
The healthy control group in this study was not age matched with the BVP group and there were non-
significant age differences between the three BVP groups. However, we do not think that this would influence our
findings as a number of studies have shown that gait variability (the focus of the current study) in healthy young
and older adults is not significantly affected by (healthy) ageing (Herssens et al. 2018; Hollman et al. 2011).
However, other limitations in the current study should be kept in mind. Caution should be taken in comparing the
CV of step width to studies of overground walking, as it has been shown previously in healthy participants that
walking on the CAREN results in increased step width variability compared to overground walking (Gates et al.
2012). Additionally, treadmill walking appears to be more challenging than overground walking for people with
BVP, evidenced by the fact that the BVP No Gait group were not able to successfully complete the familiarization
period, despite reporting being able to walking independently without assistance. We would therefore caution a
direct comparison of treadmill-derived gait results with overground gait results in BVP. Regarding the fact that
the healthy group walked with optic flow and the BVP group walked with the virtual environment fixed (so as to
provide the same lighting), we do not expect that this difference would have altered our results, as two previous
studies found no, or negligible, differences in the parameters assessed here between fixed speed walking with and
without virtual reality (Katsavelis et al. 2010; Sloot et al. 2014).
We also acknowledge that our division of participants into the BVP All Gait and BVP Part Gait groups
is based on a rather simple criterion. Of the 12 participants in the BVP Part Gait group, one participant stopped
after 0.8m/s, one after 1.0m/s, four after 1.2m/s and six after 1.4m/s and therefore, the range of locomotor capacities
within this group is likely broad. Reasons for lack of completion also varied across the participants, with some
stopping due to lack of stability control (too much lateral deviation with a risk of stepping off the treadmill) and
others unable to keep up with a faster belt speed. However, these two groups demonstrated differences in the CVs
of step time, step length and double support time (Fig. 2), strengthening the findings from the healthy control and
BVP All Gait comparison, in that these parameters not only distinguished between healthy and BVP groups, but
also within the BVP groups.
In conclusion, spatiotemporal gait parameters and their variability show speed-dependency in people with
BVP and in healthy adults, and this was seen both when considering all of the assessed speeds in those participants
who completed the protocol, as well as when only considering the three slowest walking speeds. Temporal and
sagittal plane spatial gait variability at slower walking speeds and frontal plane spatial gait variability at faster
walking speeds were the most distinguishing parameters between the healthy participants and people with BVP
who have different locomotor capacities. Gait variability in BVP was generally not correlated with the clinical
15
tests of vestibular function. The current findings indicate that analysis of gait variability at multiple speeds has
potential as an assessment tool for vestibular interventions.
Acknowledgements
The authors thank Wouter Bijnens, Rachel Senden and Rik Marcellis for their support with the measurements.
Grants
CM was funded by the Kootstra Talent Fellowship awarded by the Centre for Research Innovation, Support and
Policy (CRISP) and by the NUTRIM Graduate Programme, both of Maastricht University Medical Center+. FL
was financially supported by MED-EL.
Disclosures
The authors declare no competing interests.
Author Contributions
Conception of the study: CM, RvdB, KK, HK, KM. Data Collection: CM, FL. Data Analysis: CM, PW, FL.
Interpreted results: All authors. Prepared Figures: CM. Drafted the article: CM. Reviewed and revised the article:
All authors. Approved final version: All authors.
References
Bailey IL, and Lovie JE. New design principles for visual acuity letter charts. Am J Optom Physiol Opt 53: 740-
745, 1976.
Bauby CE, and Kuo AD. Active control of lateral balance in human walking. J Biomech 33: 1433-1440, 2000.
Brandt T, Strupp M, and Benson J. You are better off running than walking with acute vestibulopathy. Lancet
354: 746, 1999.
Brantberg K, and Lofqvist L. Preserved vestibular evoked myogenic potentials (VEMP) in some patients with
walking-induced oscillopsia due to bilateral vestibulopathy. J Vestib Res 17: 33-38, 2007.
Bruijn SM, Meijer OG, Beek PJ, and van Dieen JH. Assessing the stability of human locomotion: a review of
current measures. J R Soc Interface 10: 20120999, 2013.
Collins S, Ruina A, Tedrake R, and Wisse M. Efficient bipedal robots based on passive-dynamic walkers.
Science 307: 1082-1085, 2005.
Dakin CJ, Inglis JT, Chua R, and Blouin JS. Muscle-specific modulation of vestibular reflexes with increased
locomotor velocity and cadence. J Neurophysiol 110: 86-94, 2013.
Dean JC, Alexander NB, and Kuo AD. The effect of lateral stabilization on walking in young and old adults.
IEEE Trans Biomed Eng 54: 1919-1926, 2007.
den Otter AR, Geurts AC, Mulder T, and Duysens J. Speed related changes in muscle activity from normal to
very slow walking speeds. Gait Posture 19: 270-278, 2004.
Dingwell JB, Cusumano JP, Cavanagh PR, and Sternad D. Local dynamic stability versus kinematic variability
of continuous overground and treadmill walking. J Biomech Eng 123: 27-32, 2001.
Donelan JM, Shipman DW, Kram R, and Kuo AD. Mechanical and metabolic requirements for active lateral
stabilization in human walking. J Biomech 37: 827-835, 2004.
16
Fitzpatrick RC, Wardman DL, and Taylor JL. Effects of galvanic vestibular stimulation during human walking.
J Physiol 517 ( Pt 3): 931-939, 1999.
Forbes PA, Vlutters M, Dakin CJ, van der Kooij H, Blouin JS, and Schouten AC. Rapid limb-specific
modulation of vestibular contributions to ankle muscle activity during locomotion. J Physiol 595: 2175-2195,
2017.
Fujimoto C, Murofushi T, Chihara Y, Suzuki M, Yamasoba T, and Iwasaki S. Novel subtype of idiopathic
bilateral vestibulopathy: bilateral absence of vestibular evoked myogenic potentials in the presence of normal
caloric responses. J Neurol 256: 1488-1492, 2009.
Gates DH, Darter BJ, Dingwell JB, and Wilken JM. Comparison of walking overground and in a Computer
Assisted Rehabilitation Environment (CAREN) in individuals with and without transtibial amputation. J Neuroeng
Rehabil 9: 81, 2012. Doi: 10.1186/1743-0003-9-81
Govender S, Rosengren SM, and Colebatch JG. Vestibular neuritis has selective effects on air- and bone-
conducted cervical and ocular vestibular evoked myogenic potentials. Clin Neurophysiol 122: 1246-1255, 2011.
Guinand N, Boselie F, Guyot JP, and Kingma H. Quality of life of patients with bilateral vestibulopathy. Ann
Otol Rhinol Laryngol 121: 471-477, 2012a.
Guinand N, Pijnenburg M, Janssen M, and Kingma H. Visual Acuity While Walking and Oscillopsia Severity
in Healthy Subjects and Patients With Unilateral and Bilateral Vestibular Function Loss. Arch Otolaryngol Head
Neck Surg 138: 301-306, 2012b.
Guinand N, van de Berg R, Cavuscens S, Stokroos RJ, Ranieri M, Pelizzone M, Kingma H, Guyot JP, and
Perez-Fornos A. Vestibular Implants: 8 Years of Experience with Electrical Stimulation of the Vestibular Nerve
in 11 Patients with Bilateral Vestibular Loss. ORL J Otorhinolaryngol Relat Spec 77: 227-240, 2015.
Guyot JP, Perez Fornos A, Guinand N, van de Berg R, Stokroos R, and Kingma H. Vestibular assistance
systems: promises and challenges. J Neurol 263 Suppl 1: S30-35, 2016.
Herssens N, Verbecque E, Hallemans A, Vereeck L, Van Rompaey V, and Saeys W. Do spatiotemporal
parameters and gait variability differ across the lifespan of healthy adults? A systematic review. Gait Posture 64:
181-190, 2018.
Hollman JH, McDade EM, and Petersen RC. Normative spatiotemporal gait parameters in older adults. Gait
Posture 34: 111-118, 2011.
Horak FB, Kluzik J, and Hlavacka F. Velocity dependence of vestibular information for postural control on
tilting surfaces. J Neurophysiol 116: 1468-1479, 2016.
Jahn K, Strupp M, Schneider E, Dieterich M, and Brandt T. Differential effects of vestibular stimulation on
walking and running. Neuroreport 11: 1745-1748, 2000.
Jahn K, Strupp M, Schneider E, Dieterich M, and Brandt T. Visually induced gait deviations during different
locomotion speeds. Exp Brain Res 141: 370-374, 2001.
Katsavelis D, Mukherjee M, Decker L, and Stergiou N. The effect of virtual reality on gait variability.
Nonlinear Dynamics Psychol Life Sci 14: 239-256, 2010.
Kuo AD. The six determinants of gait and the inverted pendulum analogy: A dynamic walking perspective. Hum
Mov Sci 26: 617-656, 2007.
Lewis RF. Vestibular implants studied in animal models: clinical and scientific implications. J Neurophysiol 116:
2777-2788, 2016.
Lucieer F, Vonk P, Guinand N, Stokroos R, Kingma H, and van de Berg R. Bilateral Vestibular Hypofunction:
Insights in Etiologies, Clinical Subtypes, and Diagnostics. Front Neurol 7: 26, 2016. Doi:
10.3389/fneur.2016.00026
McCrum C, Eysel-Gosepath K, Epro G, Meijer K, Savelberg HH, Brüggemann GP, and Karamanidis K.
Deficient recovery response and adaptive feedback potential in dynamic gait stability in unilateral peripheral
vestibular disorder patients. Physiol Rep 2: e12222, 2014. Doi: 10.14814/phy2.12222
McCrum C, Willems P, van de Berg R, Cavuscens S, Guinand N, Guyot JP, Perez Fornos A, Marcellis R,
Ranieri M, Senden R, Stokroos R, Zijlstra W, Karamanidis K, Meijer K, and Kingma H. Preliminary
observations of the acute effects of vestibular nerve stimulation on stride length and time in two patients with
bilateral vestibular hypofunction. Gait Posture 49: 124, 2016. Doi: 10.1016/j.gaitpost.2016.07.179
McGarvie LA, MacDougall HG, Halmagyi GM, Burgess AM, Weber KP, and Curthoys IS. The Video Head
Impulse Test (vHIT) of Semicircular Canal Function - Age-Dependent Normative Values of VOR Gain in Healthy
Subjects. Front Neurol 6: 154, 2015.
McGeer T. Dynamics and control of bipedal locomotion. J Theor Biol 163: 277-314, 1993.
Murley GS, Menz HB, and Landorf KB. Electromyographic patterns of tibialis posterior and related muscles
when walking at different speeds. Gait Posture 39: 1080-1085, 2014.
O'Connor SM, Xu HZ, and Kuo AD. Energetic cost of walking with increased step variability. Gait Posture 36:
102-107, 2012.
Ogawa T, Kawashima N, Obata H, Kanosue K, and Nakazawa K. Mode-dependent control of human walking
and running as revealed by split-belt locomotor adaptation. J Exp Biol 218: 3192-3198, 2015.
17
Perez Fornos A, Cavuscens S, Ranieri M, van de Berg R, Stokroos R, Kingma H, Guyot JP, and Guinand
N. The vestibular implant: A probe in orbit around the human balance system. J Vestib Res 27: 51-61, 2017.
Perry JA, and Srinivasan M. Walking with wider steps changes foot placement control, increases kinematic
variability and does not improve linear stability. Roy Soc Open Sci 4: 160627, 2017.
Piker EG, Jacobson GP, Burkard RF, McCaslin DL, and Hood LJ. Effects of age on the tuning of the cVEMP
and oVEMP. Ear Hear 34: e65-73, 2013.
Raffalt PC, Guul MK, Nielsen AN, Puthusserypady S, and Alkjaer T. Economy, Movement Dynamics, and
Muscle Activity of Human Walking at Different Speeds. Sci Rep 7: 43986, 2017.
Savelberg HH, Ilgin D, Angin S, Willems PJ, Schaper NC, and Meijer K. Prolonged activity of knee extensors
and dorsal flexors is associated with adaptations in gait in diabetes and diabetic polyneuropathy. Clin Biomech 25:
468-475, 2010.
Schlick C, Schniepp R, Loidl V, Wuehr M, Hesselbarth K, and Jahn K. Falls and fear of falling in vertigo and
balance disorders: A controlled cross-sectional study. J Vestib Res 25: 241-251, 2016.
Schniepp R, Schlick C, Schenkel F, Pradhan C, Jahn K, Brandt T, and Wuehr M. Clinical and
neurophysiological risk factors for falls in patients with bilateral vestibulopathy. J Neurol 264: 277-283, 2017.
Schniepp R, Wuehr M, Neuhaeusser M, Kamenova M, Dimitriadis K, Klopstock T, Strupp M, Brandt T,
and Jahn K. Locomotion speed determines gait variability in cerebellar ataxia and vestibular failure. Mov Disord
27: 125-131, 2012.
Sloan LL. New test charts for the measurement of visual acuity at far and near distances. Am J Ophthalmol 48:
807-813, 1959.
Sloot LH, van der Krogt MM, and Harlaar J. Effects of adding a virtual reality environment to different modes
of treadmill walking. Gait Posture 39: 939-945, 2014.
Sprenger A, Wojak JF, Jandl NM, and Helmchen C. Postural Control in Bilateral Vestibular Failure: Its
Relation to Visual, Proprioceptive, Vestibular, and Cognitive Input. Front Neurol 8: 444, 2017.
Strupp M, Kim JS, Murofushi T, Straumann D, Jen JC, Rosengren SM, Della Santina CC, and Kingma H.
Bilateral vestibulopathy: Diagnostic criteria Consensus document of the Classification Committee of the Barany
Society. J Vestib Res 27: 177-189, 2017.
Valko Y, Rosengren SM, Jung HH, Straumann D, Landau K, and Weber KP. Ocular vestibular evoked
myogenic potentials as a test for myasthenia gravis. Neurology 86: 660-668, 2016.
van de Berg R, van Tilburg M, and Kingma H. Bilateral Vestibular Hypofunction: Challenges in Establishing
the Diagnosis in Adults. ORL J Otorhinolaryngol Relat Spec 77: 197-218, 2015.
van Dooren TS, Lucieer FMP, Janssen AML, Kingma H, and van de Berg R. The Video Head Impulse Test
and the Influence of Daily Use of Spectacles to Correct a Refractive Error. Front Neurol 9: 125, 2018. Doi:
10.3389/fneur.2018.00125
van Tilburg MJ, Herrmann BS, Guinan JJ, Jr., and Rauch SD. Increasing the Stimulation Rate Reduces
cVEMP Testing Time by More Than Half With No Significant Difference in Threshold. Otol Neurotol 37: 933-
936, 2016.
Wuehr M, Decker J, and Schniepp R. Noisy galvanic vestibular stimulation: an emerging treatment option for
bilateral vestibulopathy. J Neurol 264: 81-86, 2017.
Wuehr M, Nusser E, Decker J, Krafczyk S, Straube A, Brandt T, Jahn K, and Schniepp R. Noisy vestibular
stimulation improves dynamic walking stability in bilateral vestibulopathy. Neurology 86: 2196-202, 2016.
Wuehr M, Schniepp R, Pradhan C, Ilmberger J, Strupp M, Brandt T, and Jahn K. Differential effects of
absent visual feedback control on gait variability during different locomotion speeds. Exp Brain Res 224: 287-294,
2013.
Yip CW, Glaser M, Frenzel C, Bayer O, and Strupp M. Comparison of the Bedside Head-Impulse Test with
the Video Head-Impulse Test in a Clinical Practice Setting: A Prospective Study of 500 Outpatients. Front Neurol
7: 58, 2016.
Yokoyama H, Ogawa T, Kawashima N, Shinya M, and Nakazawa K. Distinct sets of locomotor modules
control the speed and modes of human locomotion. Sci Rep 6: 36275, 2016.
Yokoyama H, Ogawa T, Shinya M, Kawashima N, and Nakazawa K. Speed dependency in alpha-motoneuron
activity and locomotor modules in human locomotion: indirect evidence for phylogenetically conserved spinal
circuits. Proc Biol Sci 284: 20170290, 2017.
Zeni JA, Jr., Richards JG, and Higginson JS. Two simple methods for determining gait events during treadmill
and overground walking using kinematic data. Gait Posture 27: 710-714, 2008.
... Others have pointed to neurological deficiencies associated with slower walking, without referring to stability directly. Anson et al. (2019) have shown vestibular function loss causes people to walk with longer, slower steps, contradicting findings by McCrum et al. (2018) who found people with vestibular loss adapt by taking shorter, faster steps. Menz et al. (2004) have shown people with peripheral neuropathy reduced walking speed and cadence. ...
... Another body of literature suggests fast walking is beneficial. Variability, which is often attributed to greater instability, lessens with increased velocity (Donker and Beek, 2002), even in people with bilateral vestibular loss (Schniepp et al., 2012(Schniepp et al., , 2017Wuehr et al., 2016;McCrum et al., 2018). Studies have also used the mediolateral margin of stability to quantify overall stability, which increases with speed Gates et al., 2013). ...
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This dissertation aimed to further our understanding of how old age might affect gait stability and adaptability, with the perspective that this knowledge could improve the effectiveness and specificity of exercise-based falls reduction interventions for both healthy and clinical populations at an increased risk of falls. Part One of this dissertation reviewed the incidence, causes and consequences of falls among older adults. Humans are living longer than ever before and the percentage of older people in our populations will continue to rise for the foreseeable future. As a result, age-related health risks and disease are becoming a larger and larger burden on our older populations and our societies as a whole. Falls and their consequences are one of the most common risks to health, mobility and quality of life among older adults and the number of injuries and hospital admissions because of falls have been increasing in recent years. In particular, mechanical perturbations such as trips und slips during walking present a significant risk for falls in older adults. Therefore, Part One concluded that examination of the stability and adaptation of gait during such mechanical perturbations may help improve the effectiveness of interventions aimed at reducing falls, by identifying specific mechanisms of gait adaptation that can be exploited. Part Two of this dissertation examined gait variability and stability during walking tasks targeting predominantly predictive control during unperturbed and perturbed gait. Chapter 2.1 assessed the gait of young and older healthy adults, as well as adults with bilateral vestibulopathy, during multiple walking speeds, to elucidate the potential role of the vestibular system in unperturbed gait control. The findings demonstrated that walking speed significantly affects multiple gait parameters and their variability in all the participant groups, and potentially influences the vestibular contribution to locomotor control. Chapter 2.2 used a sustained resistance perturbation to explore the predictive adaptation of gait to control stability in young, middle-aged and older adults, to investigate how such control might change across the adult lifespan. Following a certain number of repeated perturbations, the older adults could achieve similar stability values to younger adults, but the rate of adaptation to a sustained perturbation was found to be slower in the older adults. Part Three of this dissertation examined methodological aspects of reactive gait stability assessment using perturbations and how we might improve our experimental procedures to better understand how people control and adapt their gait on exposure to unexpected perturbations. Chapter 3.1 reviewed previous studies and their methodologies for examining reactive gait stability during unexpected perturbations in older adults and made suggestions regarding what methodological aspects required further investigation and regarding considerations for future research. In response to the outcomes of the literature review, Chapter 3.2 confirmed that walking speed significantly affects the stability of the body configuration during walking and presented a method to reduce interindividual differences in gait stability prior to experiencing a perturbation, allowing a theoretically more accurate examination of responses to gait perturbations and any subsequent adaptations in gait. Part Four of this dissertation subsequently applied the improved methodology to examine how young humans adapt, retain and transfer adaptations in gait stability to controlled gait perturbations (Chapter 4.1) and whether or not the processes of adaptation and transfer are altered in older adults (Chapter 4.2). Furthermore, Chapter 4.2 investigated whether or not having young and older participants walk with equivalent gait stability using the methods presented in Chapter 3.2 would lead to different conclusions than those previously reported in the literature regarding age-related differences in gait stability. The results demonstrated that the relationship between walking speed and stability varies from person to person in both young (Chapter 4.1) and older adults (Chapter 4.2) and that older adults could demonstrate interlimb transfer of adaptations to sudden perturbations (Chapter 4.2) when younger adults did not (Chapter 4.1). 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Several challenges in improving the fall risk of people with bilateral vestibulopathy and other neurological disorders exist related to their residual function and capacity to respond to physical exercise interventions. To this end, the effects of ever-improving technical therapeutic interventions, as well as task specific exercise-based training on balance and gait in these patients should continue to be investigated.
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Objective: Assessing the effect of a higher stimulation rate in cervical vestibular evoked myogenic potential (cVEMP) outcome measurements. Study design: Prospective cohort study. Setting: Large specialty hospital, Department of otolaryngology. Subjects: Eleven healthy subjects were used in this study. Intervention: All subjects underwent a cervical vestibular evoked myogenic potential test at 500, 750, and 1000 Hz using 5 and 13 Hz stimulation rates. Main outcome measures: Threshold, peak-to-peak (PP) amplitude, and interaural asymmetry ratio (IAR). Results: PP cVEMP amplitudes were larger at 5/s than at 13/s. The 5/s to 13/s differences were statistically significant at 500 and 750 Hz (p < 0.02). The coefficient of variation in PP amplitudes across subjects, was not significantly different at any frequency for 5/s versus 13/s stimuli. No significant difference was found in the IAR at any frequency. The cVEMP thresholds were similar between stimulation rates. Conclusion: In healthy young subjects no significant differences in threshold were found between 5/s and 13/s stimulation rates, though intrasubject PP amplitude was significantly lower at the faster stimulation rate. Increasing stimulation rate reduces test time and burden. Additional studies are needed to verify that these conclusions are also true for patients.