Clin Physiol Funct Imaging (2010) 30, pp51–56 doi: 10.1111/j.1475-097X.2009.00903.

Gait analysis in elderly adult patients with mild cognitive

impairment and patients with mild Alzheimers disease:
simple versus dual task: a preliminary report
D. Maquet1, F. Lekeu2,3, E. Warzee2, S. Gillain2, V. Wojtasik2,3, E. Salmon3, J. Petermans2 and J. L. Croisier1
1
Department of Motricity Sciences, University and CHU of Liege, 2Department of Geriatrics, CHU Liege, and 3Department of Neurology, CHU Liege, Belgium

Summary

Correspondence Background ⁄ Aims: The aim of this study was to assess gait characteristics during simple
Didier Maquet, PhD, Department of Motricity and dual task in patients with mild cognitive impairment (MCI) and compare them
Sciences, University of Liege, ISEPK – B21 – Allée
with those of healthy elderly subjects and mild Alzheimers disease (AD) patients.
des Sports 4, B-4000 Liege, Belgium
E-mail: d.maquet@ulg.ac.be
Methods: We proposed a gait analysis to appreciate walking (simple task and dual
task) in 14 MCI, 14 controls and six AD subjects who walked at their preferred
Accepted for publication
speed. A 20-second period of stabilized walking was used to calculated stride
Received 31 March 2009;
accepted 1 September 2009
frequency, stride length, symmetry and regularity. Speed walking was measured by
electrical photocells.
Key words Results: Variables measured during simple and dual tasks showed an alteration of
Alzheimer disease; dual task; gait; mild cognitive motor function as well in mild AD patients as in MCI patients.
impairment; walking Conclusion: At the end of this preliminary study, we defined a specific gait pattern for
each cognitive profile. Further researches appear necessary to enlarge the study
cohort.

fulfil criteria for dementia (Morris, 1993). The progression rate

Introduction
Walking is one of the most universal of all human activities and
the primary exercise recommended by public health authorities.
Gait characteristics appear frequently altered in different
pathologies. New tools enable the study of human locomotion
(Andriacchi & Alexander, 2000). One of the most recent
quantitative methods for analysing human gait is based on
recording tri-axial accelerations, with a specific accelerometer, at
a point close to the body centre of gravity (Auvinet et al., 2002).
This method allows a fast and functional analysis of gait. Patients
with Alzheimers disease (AD), the most common dementia,
present greater risk of falls (Buchner & Larson, 1987; Morris
et al., 1987). These patients generally have shorter step lengths,
reduced gait speed, lower stepping frequency, and greater step-
to-step variability than healthy elderly subjects (Visser, 1983;
Buchner & Larson, 1987; Alexander et al., 1995; OKeeffe et al.,
1996). The specific nature of the dual task deficit in AD, despite
the limited impact in healthy elderly subjects, offers relevant
potential for developing walking protocols to aid diagnosis, to
appreciate the evolution of this disease and to objectify the
effectiveness of some treatments (Sala & Logie, 2001).
The transitional state between normal ageing and the early
stages of AD has been designated as mild cognitive impairment
(MCI) (Petersen et al., 2001). Patients with MCI suffer from
impaired cognition, especially memory, to a greater extent than
would be expected for a given age and education, but do not
 2009 The Authors
Journal compilation  2009 Scandinavian Society of Clinical Physiology and Nuclear Medicine 30, 1, 51–56
to dementia is higher for patients with MCI compared with
controls. However, the progression of this disease to AD remains
uncertain. The aim of this study was to assess gait characteristics
during simple and dual task in patients with MCI and compare
them with those of healthy ageing (with no cognitive
impairment) and mild AD patients.
Methods
Subjects
Fourteen patients with MCI, 14 healthy control subjects and six
patients with mild AD were included in the present study
(Table 1).
All control subjects (to check that none of the healthy
volunteers presented any memory impairments) and patients
(AD and MCI) underwent a medical evaluation and a neuro-
psychological assessment.
Medical evaluation
The medical evaluation included an interview (to establish the
subjects full personal medical history) and a comprehensive
clinical examination (height, weight and a cardiorespiratory,
abdominal and above all neurological examination), the goal of
which was to check for the absence of exclusion criteria. For the
51
52 Gait analysis during simple and dual tasks, D. Maquet et al.
Healthy controls MCI patients
n = 14 n = 14
(7 females–7 males) (7 females–7 males) (3 females–3 males)
mean ± SD mean ± SD
Age (years) 74 ± 5 73 ± 4
Height (cm) 165 ± 6 167 ± 10
Weight (kg) 74 ± 10 67 ± 15
Distance between 76 ± 5 77 ± 7
great trochanter and
external malleolus (cm)
MCI, mild cognitive impairment; AD, Alzheimers disease.
AD patients, family members and ⁄ or carers were questioned on
living conditions, falls and medications; if required, we
performed a telephone interview with the patients family
doctor or consulting physician.
Neuropsychological assessment
The evaluation performed by each subject included:
1 The Mini-Mental State Examination (MMSE) (Enzensberger
et al., 1997) for orientation, learning, working memory (via
mental arithmetic and word spelling), object naming, under-
standing simple instructions and copying a drawing. The
30-point score has a cognitive impairment cut-off at 24
(26 for subjects having received higher education).
2 The Mattis scale (Mattis, 1976) is another set of global
cognitive evaluations which complements the MMSE. It inves-
tigates frontal and subcorticofrontal functions more broadly and
can thus detect types of dementia other than AD. It explores
attention, memory, verbal and motor initiation, conceptual
abilities and visuoconstructive praxis. The cognitive impairment
cut-off is 123 out of 144, which can be modulated depending
on the subjects education level.
3 A French version of the Grober and Buschke 16-item free
recall ⁄ cued recall test (Van der Linden et al., 2004), which
examines episodic memory.
4 Reys complex figure test (Rey et al., 1991) in order to evaluate
visuoconstructive and visuospatial organization abilities. Scoring
is both qualitative and quantitative (out of 36) and
5 The computerized alertness and divided attention sub-tests
from the Test for Attentional Performance (TAP) battery
(Zimmermann & Fimm, 2006).
Mild cognitive impairment patients had memory problems
without any significant impairment in daily living activities or
global cognitive deterioration. The patients had undergone
neurological, neuropsychological and structural neuroimaging
evaluations, and were classified as MCI since they had a Clinical
Dementia Rating (CDR) score of 0Æ5 (Morris, 1993). They met
the criteria for either amnestic MCI (with at least one memory
test performance that were 1Æ5 standard deviations below the
mean for age-matched controls) or multiple domain MCI (when
cognitive performance was also decreased in another, non-
memory domain) (Petersen et al., 2001; Winblad et al., 2004).
Journal compilation  2009 Scandinavian Society of Clinical Physiology and Nuclear Medicine 30, 1, 51–56
Table 1 Demographic and morphological
AD patients characteristics of healthy control subjects, mild
n=6 cognitive impairment (MCI) patients and
Alzheimers disease (AD) patients.
mean ± SD
74 ± 4
168 ± 11
69 ± 12
79 ± 8
Exclusion criteria were: mental retardation, less than four years
of education, brain trauma, epilepsy, cancer, depression, any
major systemic disease or any substance abuse. At the time of
inclusion, all patients were free of medication that could
noticeably affect brain function. All MCI patients had MMSE
scores of minimum 24 arbitrary units (a.u.) at baseline
evaluation (Folstein et al., 1975).
Patients with dementia were diagnosed as probable AD as
defined by the National Institute of Neurological and Commu-
nicative Disorders and Stroke ⁄ Alzheimer Disease and Related
Disorders Association criteria (McKhann et al., 1984). The
exclusion criteria were the same as those used for MCI patients,
and their CDR score reached 1. All AD patients had MMSE scores
of 20 or over at baseline evaluation (Folstein et al., 1975),
reflecting a mild stage of dementia.
The 14 healthy elderly adults (control subjects) were
cognitively and neurologically intact. They lived in the
community and were recruited by word of mouth. The
exclusion criteria were the same as those used for the patients,
and the NC had a zero CDR score.
All participants were 65 or older, with no story of fall or
hospitalisation in the last 6 months. None of them had a history
of musculo-skeletal disorder or orthopaedic problems. All of
them were living at home.
The local Ethics Committee approved the study and all
subjects gave their informed consent.
Gait analysis procedure
The gait analysis system used in this study (Locométrix;
Centaure-Metrix, Evry Cedex, France) includes an acceleration
sensor, a recording device, and a computer program for
processing the acceleration signals. The sensor is composed of
two accelerometers placed perpendicularly to each other and
housed in a moulded box (40 · 18 · 18 mm). The sensor is
incorporated into a semi-elastic belt, which is fastened around
the subjects waist, so that the sensor is over the L3–L4 inter-
vertebral space. One accelerometer is aligned with the median-
lateral axis of the body, the other with the cranial–caudal axis.
Signals from the sensor were recorded by a portable data logger
with an acquisition frequency of 50 Hz. This device weighs
140 g and is housed in a box (65 · 22 · 12 mm). The
 2009 The Authors
 Gait analysis during simple and dual tasks, D. Maquet et al. 53

recorded signals are transferred to a laptop computer using a possible relationships between gait parameters and some specific
transfer program operated under WINDOWS 98, formatted in tests of cognitive function memory and attention. All the
files and analyzed by software developed in the MATLAB 5 statistical analyses were performed using Statistical Analysis
environment (Mathworks, France). System 9Æ1 (SAS Institute Inc., Cary, NC, USA). A P-value of 0Æ05
The tests were carried out with subject walking at his ⁄ her was considered as statistically significant.
comfortable speed down and back along a 45 m straight
hospital corridor. No prompting signals were used. All subjects
Results
wore their usual walking shoes avoiding high heels or hard-
soled shoes. Walking speed was measured by a system with Subjects
electrical photocells developed in our University.
The demographic and morphological data on the subjects are
A period of steady state walking of 20Æ48 s was selected from
given in Table 1. There was no statistical difference between the
the recording of each subject. This period contained about 1024
three groups. The same sex ratio was observed (50% males and
acceleration measurements and provided an optimal calculation
50% females) for the three groups.
time.
We calculated the following variables during simple and dual
tasks: Gait variables
1 Comfortable walking speed (m s)1).
Simple task (Table 2)
2 Stride frequency (SF, in Hz): SF Movements of the left and
right sides are identical from one cycle to the next in normal All subjects performed the walking test in simple task conditions
walking. Walking at a constant speed can, therefore, be without stop. Walking speed, SL and Reg were significantly
considered to be the sum of a series of periodic stationary lower in AD patients in comparison with control subjects and
movements. Our analysis program used a Fast Fourier Trans- MCI patients. In contrast, SF was significantly reduced in MCI
formation (FFT) to convert the cranial–caudal acceleration signal patients compared to healthy controls.
to the step frequency (the fundamental frequency of periodic
movement). By definition, a complete stride includes two steps;
Dual task (Table 3)
thus SF corresponds to one half of the fundamental frequency
and is expressed in Hz or stride per s. During the dual task, the walking speed appeared significantly
3 Stride length (SL, in m) was calculated from the average speed different between the three groups. Walking speed was the
(m s)1) divided by the SF (Hz). lowest in AD patients. None stop was observed in controls in
4 Step symmetry (Sym, in arbitrary units) and stride regularity contrast with some MCI and AD patients.
(Reg, in arbitrary units) were derived from two coefficients of
correlation, C1 and C2, obtained by calculating the autocorre- Comparison of gait analysis during simple and dual tasks
lation function of the vertical acceleration signal. We applied a All control subjects performed the two walking conditions
Fischer Z transformation z(x) = 0Æ5 log [(1 + x) ⁄ (1)x)] to the without stop. In these subjects, changes of walking speed and SF
coefficients C1 and C2 to obtain normal distributions (C1z and (dual versus simple task) were significant (Table 4).
C2z). Since the symmetry index is the ratio of the two In contrast, during dual task, results showed that the Sym was
coefficients (C1z and C2z), we used a logarithmic transformation significantly better in healthy controls than in both patient
to obtain a normal distribution (Symtz LN). Stride symmetry groups.
describes the similarity of left and right cranial–caudal move-
ments and is independent of fluctuations in the successive
cranial–caudal movements of each limb. Reg describes the
Table 2 Comparison of gait variables between three groups during
similarity of vertical movements over successive strides. Sym- simple task.
metry and regularity are dimensionless and
5 Number of stops during walking in simple and dual tasks. Healthy MCI
Two walking conditions were randomized: simple task controls patients AD patients
(walking) and dual task (walking with simultaneous backward mean ± SD mean ± SD mean ± SD
counting). The stops and errors during dual task were measured. Walking speed (m s)1) 1Æ4 ± 0Æ13a 1Æ22 ± 0Æ15a,b 1Æ02 ± 0Æ36b
Stride frequency (Hz) 1 ± 0Æ08a 0Æ9 ± 0Æ05b 0Æ95 ± 0Æ17a,b
Stride length (m) 1Æ41 ± 0Æ1a 1Æ36 ± 0Æ13a,b 1Æ13 ± 0Æ45b
Statistical analysis Symmetry (a.u.) 202 ± 31a 224 ± 25a 209 ± 77a
a a
Results are reported as mean ± SD. Since data were skewed, Regularity (a.u.) 276 ± 35 287 ± 29 227 ± 82b
Stops (a.u.) 0 ± 0a 0 ± 0a 0 ± 0a
non-parametric statistics were used. Kruskal-Wallis ANOVA by
ranks was used for multiple comparisons between the different MCI, mild cognitive impairment; AD, Alzheimers disease; a.u., arbitrary
groups. Categorical data were also analysed using Chi-square units.
test. Spearman rank order correlation was used to explore Different letters represent a significant statistical difference (P<0Æ05).
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Journal compilation  2009 Scandinavian Society of Clinical Physiology and Nuclear Medicine 30, 1, 51–56
54 Gait analysis during simple and dual tasks, D. Maquet et al.

Table 3 Comparison of gait variables between three groups during memory. Furthermore, age-related changes in gait parameters
dual task. have been associated with an increased risk of falling and an
adaptation to a safer gait (Maki, 1997). Our results showed
Healthy MCI that changes of walking speed and SF (dual versus simple task)
controls patients AD patients
mean ± SD mean ± SD mean ± SD
were significant in the healthy elderly subjects. Hollman et al.
(2007) reported a decrease in walking speed and an increase
Walking speed (m s)1) 1Æ3 ± 0Æ14a 1Æ05 ± 0Æ21b 0Æ74 ± 0Æ26c of step-to-step variability under a dual task condition in elderly
Stride frequency (Hz) 0Æ94 ± 0Æ07a 0Æ81 ± 0Æ13b 0Æ81 ± 0Æ23a,b
subjects. Beauchet et al. (2003) showed also that cognitive
Stride length (m) 1Æ38 ± 0Æ15a 1Æ3 ± 0Æ12a 1 ± 0Æ42b
Symmetry (a.u.) 250 ± 35a 216 ± 21a 206 ± 61a activity during walking reduces gait velocity and increases
Regularity (a.u.) 258 ± 38a 224 ± 47a 206 ± 61b variability in stride velocity in well-elderly women. Walking is,
Stops (a.u.) 0 ± 0a 0Æ07 ± 0Æ27a 0Æ17 ± 0Æ41a in normal conditions, a highly automated and rhythmic motor
Errors (a.u.) 0Æ5 ± 1Æ16a 0Æ36 ± 1Æ08a 2Æ16 ± 3Æ92b behaviour that is mostly controlled by subcortical locomotor
brain regions (Nutt et al., 1993). In elderly subjects, the
MCI, mild cognitive impairment; AD, Alzheimers disease; a.u., arbitrary
dual task interfered with gait parameters suggesting the
units.
Different letters represent a significant statistical difference (P<0Æ05). involvement of higher cortical regions for the motor control
of gait in this population (Beauchet et al., 2003). Furthermore,
walking requires more attention and thus more cortical
Table 4 Comparison of gait variables during simple versus dual task. involvement with increasing age (Woollacott & Shumway-
Cook, 2002).
Simple task Dual task
We reported an intriguing finding with regard to the
mean ± SD mean ± SD P
improvement of Sym during dual task walking in healthy
Healthy controls elderly subjects. Sym describes the similarity of left and right
Walking speed (m s)1) 1Æ4 ± 0Æ13 1Æ3 ± 0Æ14 <0Æ05 cranio-caudal movements. This parameter was determined by
Stride frequency (Hz) 1 ± 0Æ08 0Æ94 ± 0Æ07 <0Æ05
calculating the two coefficients of correlation obtained by
Stride length (m) 1Æ41 ± 0Æ1 1Æ38 ± 0Æ15 ns
Symmetry (a.u.) 202 ± 31 250 ± 35 ns measuring the autocorrelation function of the vertical accele-
Regularity (a.u.) 276 ± 35 258 ± 38 ns ration signal. Further researches are needed to confirm this
Stops (a.u.) 0 ± 0 0 ± 0 ns observation that might be related to the rhythmic stimulation
MCI patients produced during backward counting in healthy subjects.
Walking speed (m s)1) 1Æ22 ± 0Æ15 1Æ05 ± 0Æ21 <0Æ05
Stride frequency (Hz) 0Æ9 ± 0Æ05 0Æ81 ± 0Æ13 <0Æ05
Accordingly, Thaut et al. (1996) and Enzensberger et al.
Stride length (m) 1Æ36 ± 0Æ13 1Æ3 ± 0Æ12 <0Æ05 (1997) have reported the positive effect of metronome
Symmetry (a.u.) 224 ± 25 216 ± 21 <0Æ05 stimulation during walking in patients with Parkinson disease.
Regularity (a.u.) 287 ± 29 224 ± 47 ns Our results in AD patients confirmed data previously
Stops (a.u.) 0 ± 0 0Æ07 ± 0Æ27 ns published in literature (Visser, 1983; Buchner & Larson,
AD patients
Walking speed (m s)1) 1Æ02 ± 0Æ36 0Æ74 ± 0Æ26 ns
1987; Alexander et al., 1995; OKeeffe et al., 1996). We showed
Stride frequency (Hz) 0Æ95 ± 0Æ17 0Æ81 ± 0Æ23 <0Æ05 that AD patients present shorter SL, reduced walking speed and
Stride length (m) 1Æ13 ± 0Æ45 1 ± 0Æ42 ns lower Reg, particularly during dual task conditions. Further-
Symmetry (a.u.) 209 ± 77 206 ± 61 ns more, AD patients presented a significant increase of errors
Regularity (a.u.) 227 ± 82 206 ± 61 ns during backward counting. Cocchini et al. (2004) reported that
Stops (a.u.) 0 ± 0 0Æ17 ± 0Æ41 ns
dual task effects of walking (when talking in AD patients)
MCI, mild cognitive impairment; AD, Alzheimers disease; a.u., arbitrary
display a deficit of executive functions in these patients. We
units; ns, not significant. observed no significant difference in errors measured during
backward counting between MCI and control groups.
In the MCI group, changes of walking speed, SF, SL and Reg Our results demonstrated that SF during simple and dual tasks
(dual versus simple task) were significant (Table 4). conditions appears significantly lower in MCI patients than in
Results of AD patients showed that changes of SF (dual versus healthy elderly subjects. Furthermore, during dual task walking,
simple task) were significant (Table 4). MCI patients showed a walking speed significantly different, not
only from normal control subjects but also from AD patients.
Correlations between gait variables and neuropsychological variables These findings strongly suggest that the gait analysis protocol
In MCI patients, significant correlations between gait variables proposed in our study could contribute to distinguish the
and neuropsychological variables were reported (Table 5). performances of the healthy elderly subjects, MCI patients and
AD patients.
Conversely, Pettersson et al. (2005) reported that motor
Discussion
function was affected in very mild AD but not in MCI
The subjects ability to perform more than one task at a time patients. Such difference might be caused by the experimental
has been a topic in the literature on human attention and protocol proposed to assess muscle function. These authors
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Journal compilation  2009 Scandinavian Society of Clinical Physiology and Nuclear Medicine 30, 1, 51–56
 Gait analysis during simple and dual tasks, D. Maquet et al. 55

Table 5 Correlations between neuropsychological variables and gait variables in mild cognitive impairment (MCI) patients.

Mean time in a divided

MMSE Overall Mattis score Mattis initiation subscore attention task

Gait variables Simple task Dual task Simple task Dual task Simple task Dual task Simple task Dual task

Speed r = 0Æ51* r = 0Æ55* r = 0Æ40 r = 0Æ48 r = 0Æ40 r = 0Æ36 r = )0Æ66* r = )0Æ27*

Stride length r = 0Æ59* r = 0Æ65* r = 0Æ15 r = 0Æ39 r = 0Æ04 r = 0Æ25 r = )0Æ36* r = )0Æ22*
Stride frequency r = 0Æ28 r = 0Æ28 r = 0Æ57* r = 0Æ27* r = 0Æ63* r = 0Æ35* r = )0Æ78 r = )0Æ19
Regularity r = 0Æ42 r = 0Æ20 r = 0Æ17 r = )0Æ02 r = 0Æ01 r = )0Æ05 r = )0Æ47 r = )0Æ17
Symmetry r = 0Æ46 r = )0Æ20 r = 0Æ32 r = )0Æ24 r = 0Æ36 r = )0Æ36 r = )0Æ48 r = 0Æ40
Symmetry (dual task r = )0Æ45 r = )0Æ41 r = )0Æ51 r = 0Æ58*
versus simple task)

*P-value <0Æ05.

used clinical performance-based tests: Bergs Balance Scale

(Berg et al., 1992a,b; Berg et al., 1995), Falls Efficacy Scale
(Tinetti et al., 1990; Hellstrom et al., 2002), Timed up and Go
(Podsiadlo & Richardson, 1991), talking while walking with a
measure of time difference between the two conditions and
Tinetti gait protocol (Tinetti, 1986). While our data recording
remains simple and fast in the clinical use, we proposed, in
the present study, a gait analysis with more quantitative
measurements.
This study also explored the possible relationship between
gait parameters and neuropsychological tests (dedicated to
cognitive function, memory and attention) that all control
subjects and patients had underwent before the gait analysis. A
positive correlation (P<0Æ05) was observed between walking
speed and total MMSE score in MCI patients which suggests that
the higher the global cognitive level, the faster the gait.
Furthermore, the SF was positively correlated with the overall
Mattis score and the Mattis initiation subscore. This seems to
imply that the higher the overall cognitive performance level,
the higher the SF. Gait speed and SF thus appear to be related to
global cognitive function. Stride frequency is also related to
executive function.
Moreover, change in stride symmetry between simple and
dual tasks is positively correlated with the lengthening of the
reaction time in divided attention sub-tests included in the
attentional performance battery. Hence, the greater the difficulty
subjects have in sharing their attentional resources between two
tasks (i.e., visual and auditory tasks), the higher the coefficient
of variation of symmetry and the stronger the decrease in
symmetry when moving to a dual task. These results prompt a
hypothesis whereby gait symmetry is not automatic but, in fact,
requires attentional resources.
The main study limitation we faced is related to the limited
number of AD patients. Our study cohort appears too small for
definite conclusions. However, the detection of gait abnormal-
ities in MCI and AD patients seems essential because different
researches have shown that impaired motor function may
restrict activities, induce risk of falls and even predict death
(Murphy et al., 2002; Guralnik & Ferrucci, 2003).
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Journal compilation  2009 Scandinavian Society of Clinical Physiology and Nuclear Medicine 30, 1, 51–56
Conclusion
The aim of this preliminary study was to propose an original
tool for the evaluation of gait parameters. We demonstrate that
this protocol is able to define a specific gait pattern for each
cognitive profile. Further researches appear necessary and could
contribute to identify one or several gait parameters in MCI
patients, which could serve as predictive clinical factors of
progression towards dementia in this population.
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