Downloaded free from http://www.ijpm.info on Friday, March 31, 2017, IP: 202.177.173.189] Original Article
Quantitative Balance and Gait Measurement
in Patients with Frontotemporal Dementia and
Alzheimer Diseases: A Pilot Study
Selva Ganapathy Velayutham, Sadanandavalli Retnaswami Chandra1, Srikala Bharath2,
Ravi Girikamatha Shankar3 ABSTRACT
Introduction: Alzhiemers disease and Frontotemporal dementia are common neurodegenerative dementias with a
wide prevalence. Falls are a common cause of morbidity in these patients. Identifying subclinical involvement of these
parameters might serve as a tool in differential analysis of these distinct parameters involved in these conditions and
also help in planning preventive strategies to prevent falls. Patients and Methods: Eight patients in age and gender
matched patients in each group were compared with normal controls. Standardizes methods of gait and balance aseesment
were done in all persons. Results: Results revealed subclinical involvement of gait and balancesin all groups specially
during divided attention. The parameters were significantly more affected in patients. Patients with AD and FTD had
involement of over all ambulation index balance more affected in AD patients FTD patients showed step cycle, stride
length abnormalities. Discussion: There is balance and gait involvement in normal ageing as well as patients with AD and
FTD. The pattern of involvement in AD correlates with WHERE pathway involvement and FTD with frontal subcortical
circuits involvement. Conclusion: Identification the differential patterns of involvement in subclinical stage might help
to differentiate normal ageing and the different types of cortical dementias. This could serve as an additional biomarker
and also assist in initiating appropriate training methods to prevent future falls.
Key words: Alzheimer disease, balance impairment, frontotemporal dementia, gait impairment, posturography INTRODUCTION
Alzheimer disease (AD) is a neurodegenerative
disorder characterized by progressive loss of recent
and episodic memory and other cognitive functions,
Access this article online
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10.4103/0253-7176.203132 Quick Response Code affects 35 million people worldwide. [1] Early
diagnosis is important to initiate early treatment
strategies to improve disability adjusted life years
This is an open access article distributed under the terms of the
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How to cite this article: Velayutham SG, Chandra SR, Bharath S,
Shankar RG. Quantitative balance and gait measurement in patients with
frontotemporal dementia and Alzheimer diseases: A pilot study. Indian J
Psychol Med 2017;39:176-82. Departments of Neurological Rehabilitation, 1Neurology and 3Biostatistics, National Institute of Mental Health and
Neurosciences, Bengaluru, Karnataka, India, 2South Asian Division, Royal College of Psychiatrists, London, UK
Address for correspondence: Dr. Sadanandavalli Retnaswami Chandra
Faculty Block, Neurocentre, National Institute of Mental Health and Neurosciences, Bengaluru ‑ 560 029, Karnataka, India.
E‑mail: drchandrasasi@yahoo.com
176 © 2017 Indian Psychiatric Society | Published by Wolters Kluwer - Medknow [Downloaded free from http://www.ijpm.info on Friday, March 31, 2017, IP: 202.177.173.189]
Velayutham, et al.: Gait and balance in cortical dementia and reduce caregiver burden. The other type of
cortical dementia is frontotemporal dementia (FTD)
which manifests little more early and manifests often
with neuropsychiatric manifestations. These two
conditions are often misdiagnosed as each other or as
purely psychiatric illness which delays the diagnosis.
Morbidity and mortality are often due to secondary
factors than the disease itself. Cortical structures
are wired to subcortex by various functional circuits
and therefore there is a possibility that subcortical
signs which are easier to measure may be involved
subclinically and if any differential pattern is
observed it might help as an additional biomarker
in early specific diagnosis as AD or FTD and also
initiate appropriate treatments to delay progression
to serious disability.
Gait and balance are the product of successful
integration of various posture control mechanisms
and locomotion. Neurological disorders at any level
can compromise the biomechanics of the same as
it involves several complex mechanisms. Posture
control needs maintaining the center of mass over
the BOS all through the gait cycle. Dynamic balance
needs cerebellum, vestibular system, and unconscious
reactive reflexes such as long loop reflexes. Standing
balance needs sensory information with reference to
environment generated by vision, proprioception, and
vestibular system. Because of the frontal‑subcortical
circuits breaking down in FTD and  WHERE dorsal
pathway dysfunction in Ad, both these disorders are
likely to have gait and balance‑related problems.
Older persons with cognitive dysfunction are especially
vulnerable for gait and balance problems resulting
in repeated falls because of the associated multiaxial
“dysfunction involving not only cognition but also,
joints, ligaments, tendons, vision, and hearing.” [2]
Patients with attention and cognitive disorders are at
risk of disequilibrium in this automatic, unconscious
act of walking due to inability to concentrate in dual
tasking.[3‑14] There is evidence for abnormal equilibrium
in Ad and motor dysfunction in FTD.[15‑17] This can
increase morbidity significantly in these patients.[18‑22]
The changes are expected to be subclinical in the early
phase, and hence quantitative measurements will be
of great help in understanding the pattern which apart
from probably serving as a easily accessible biomarker,
might also serve in initiating rehabilitatory tools early
in the course of disease. PATIENTS AND METHODS
Twenty‑four male subjects with 50–70 years of age,
8 in each group of probable bvFTD diagnosed by
revised consensus criteria,[23] probable AD, diagnosed by ADs association criteria,[24] and healthy volunteers as
controls. The FTD and AD groups were recruited from
Outpatient Department of Neurology and Geriatric
Clinic, controls from the community. Informed consent
was obtained from all and ethical clearance received
from the Institute Ethical Committee. Subjects with
orthopedic, visual deficit, other neurological conditions,
and cardiovascular ailments were excluded. All
demographic factors including age, gender, and height,
weight are recorded.
The balance was measured by  Biodex Balance Master
Incorp., USA, using dynamic posturography, in single
and dual tasks and gait with Biodex Gait Trainer.
T h e e q u i p m e n t h a s a p o s t u ro g r a p h y ‑ b a s e d
force platform which provides objective balance
measurements in two situations, i.e., (1) dynamic
balance and (2) limits of stability (LOS). It has a
circular platform and a display monitor kept in front
of the subject to see and get the feedback about their
status of standing. The platform becomes unstable and
the subject’s experience wobbling. The change in the
center of pressure due to this will be displayed in the
monitor as a biofeedback as the cursor moves from the
epicenter of the grid.
Each subjects “base of support” requirement for the
perturbed stand is tested, and subjects are asked to
adjust their BOS making the tilted platform to the
neutral and stable position. They can utilize the
feedback about their stand position from the display
monitor and instructed to target at the innermost circle
or epicenter of the grid. At the end, BOS is recorded
including measurement of the angle of foot deviations
and during the process.
Dynamic balance ‑ Single task
Three trials each of 20 s duration are done. The
amount of deviation from original BOS and direction of
deviation were recorded without using handrail support.
The test results contain overall balance index (OBI),
anteroposterior index (API), i.e., amount of front to
back sway, mediolateral index (MLI), i.e., side to side
sway. Higher the score indicates poorer the balance.
Limits of stability ‑ Single task
In the second part of balance test, the subjects ability to
come back to the original BOS after a self‑initiated sway
in eight different direction, namely, (1) forward (F),
(2) backward, (3) right, (4) left, (5) forward right,
(6) forward left, (7) backward right, and (8) backward
left was tested. The maximum overall score, individual
direction score was 100 with the maximum time of
300 s. Higher the score and shorter the time taken
indicates better the balance. Indian Journal of Psychological Medicine | Volume 39 | Issue 2 | March-April 2017 177 [Downloaded free from http://www.ijpm.info on Friday, March 31, 2017, IP: 202.177.173.189]
Velayutham, et al.: Gait and balance in cortical dementia Procedure The platform becomes unstable, and the subject sees a
square box in the display monitor, the subjects has to
shift the body weight toward the direction of the box so
that the cursor moves and get inside the box and hold
for 2 s. Then move to the direction where the next box
appears. The display of the boxes appears in such a way
that the subject needs to come back to the first box after
completing the individual box in a different direction.
The maximum time to complete the task is 300 s. The
result generated consists of overall balance, forward,
backward, forward right, forward left, backward right,
backward left, and time take to complete the test.
Dual task In dual task, the subject performs dynamic balance, LOS
task along with cognitive task and repeated after a rest
period for 2 min from the single task. The cognitive task
includes digital subtraction of 3, 2, from 100 in dynamic
balance, LOS tasks, respectively.[25,26] The patients are
expected to utilize the visual feedback to obtain balance.
A safety harness protects the subject from falling.
Gait assessment
The subjects gait was measured by Biodex Gait Trainer  USA
Incorp. The persons recruited had to walk for 2 min in
a sensor‑based treadmill at a comfortable speed. A safety
harness was provided to protect the person from falling.
Kinematic data includes gait speed, stride and step length,
coefficient variation of the steps (CV) were gathered. After
a rest period of about 2 min, the test was administered for
the second time for a dual task where the subject counted
backward from 100 as a cognitive task[27] while walking
on a treadmill. The result contains total walking distance,
average walking speed, average step cycle, average step
length, CV of the right and left leg. Higher the score in gait
parameter indicates better gait stability, however, increased
coefficient variation of steps indicate poor gait stability. RESULTS
The Shapiro–Wilkins test was conducted to test the
normality of the parameters. Descriptive analysis was
done for age, body mass index, education in years.
Within group analysis of single versus dual task was analyzed with paired t‑test. One‑way ANOVA was
conducted to reveal the difference between groups,
followed by post hoc test with Bonferroni correction.
The mean age of FTD group = 58.37 ± 8.38; AD
group = 66.7 ± 5.5; Control group = 59.5 ± 7.03, all
the subjects were male (8 in each group), the Hindi
Mental Status Examination score of FTD and AD group
were significantly lower than the controls [Table 1].
Within group comparison of single versus dual
Dynamic balance The OBI and API of the dynamic balance of FTD
group and control group significantly differed between
single versus dual task. However, AD group had
significant difference in  mediolateral (MLI) stability
index only [Table 2 and MLI score in Figure 1].
Limits of stability All the three group had significant difference in overall
LOS score between single vs. dual task however the
sub‑component of LOS revealed FTD patients had
problem balancing on forward lateral direction and control
group had problem in forward, left direction whereas
the AD group had significant difficulty in backward
direction [Table 2 and overall LOS score in Figure 2].
Gait analysis FTD, AD group, performed poorly in dual task gait
analysis while the control group showed no significant
worsening of gait. Ambulation index (AI) is a cumulative
score of overall gait performance which is found to be
low on dual task for both dementias [Figure 3]. In
addition, FTD group had significant reduction of step
cycle, step length especially on the right side [Table 3].
Between group comparisons
Dynamic balance ‑ Single task FTD group had a significant worsening of balance in
comparison with control group in all subcomponent
of dynamic balance, i.e., OBI, API, and MLI. The Table 1: Age, body mass index, HMSE score, education of
patients with FTD and AD
FTD (n=8) AD (n=8) Control (n=8) P (ANOVA)
Age (mean±SD)
BMI
Education in years
HMSE 58.37±8.38
23.26±2.86
9.50±5.21
16.25±7.3 66.7±5.57
20.8±1.63
11.63±5.20
16.88±5.91 59.5±7.03
23.75±3.83
11±3.46
30.8±0.34 NS
NS
NS
0.000 (<0.001) NS – Not significant; SD – Standard deviation; FTD – Frontotemporal
dementia; AD – Alzheimer disease; BMI – Body mass index; HMSE – Hindi
Mental Status Examination
178 Figure 1: Dynamic balance showing significant mediolateral
instability in Alzheimer diseases. FTD – Frontotemporal dementia;
AD – Alzheimer disease Indian Journal of Psychological Medicine | Volume 39 | Issue 2 | March-April 2017 [Downloaded free from http://www.ijpm.info on Friday, March 31, 2017, IP: 202.177.173.189]
Velayutham, et al.: Gait and balance in cortical dementia Table 2: Within group single task versus dual task‑balance measurement
Balance parameters
Dynamic balance
OBI
Single
Dual
API
Single
Dual
MLI
Single
Dual
LOS
Overall
Single
Dual
Forward
Single
Dual
Backward
Single
Dual
Right
Single
Dual
Left
Single
Dual
Forward left
Single
Dual
Time
Single
Dual FTD AD Control
Mean±SD Mean±SD P Mean±SD 3.563±0.947
4.013±1.172 0.053* 3.363±1.112
3.675±1.248 2.400±0.507
2.925±0.638 0.031* 2.763±0.723
3.300±1.002 0.053* 2.700±0.792
2.813±0.751 1.913±0.535
2.650±0.639 0.006* 2.400±0.761
2.100±0.680 14.75±20.673
8.88±16.797 0.058* P 2.088±0.771
2.488±1.124 0.037* 1.488±0.522
1.425±0.423 5.38±6.323
1.63±3.852 0.037* 24.25±12.116
16±8.685 0.002* 34±16.613
15.50±10.282 0.004* 8.63±10.460
10.50±20.029 3.88±7.220
0.00±0.000 12.25±11.622
6.50±11.551 5±5.657
1.00±2.646 19.50±31.482
5.75±10.620 8.25±16.395
0.63±1.188 27.50±24.101
15.50±11.637 24.75±34.652
9.88±16.686 7±10.268
7.75±21.920 23.13±12.438
12.13±5.592 3.25±4.773
0.00±0.000 25.13±14.287
15.13±8.692 284.25±47.376
301±0.000 185.25±62.962
217.38±69.156 19.38±3.645
9±20.396 0.052* 285.38±31.332
278.25±63.944 P 0.047* 16.88±15.914
16±10.797 0.017* 0.015* *Significant (P<0.05). LOS – Limits of stability; SD – Standard deviation; FTD – Frontotemporal dementia; AD – Alzheimer disease;
MLI – Mediolateral index; API – Anteroposterior index; OBI – Overall balance index Figure 2: Overall limits of stability performance between single vs
dual among frontotemporal dementia, AD and Controls. All the three
group performed poorly in dual task. FTD – Frontotemporal dementia;
AD – Alzheimer disease Alzheimer’s group had worsening of balance in OBI,
API only. There was no significant difference between
FTD and AD group on all parameters of dynamic Figure 3: Ambulation index score of frontotemporal dementia,
Alzheimer disease and controls. Both frontotemporal dementia and
Alzheimer disease had poor score in dual task. FTD – Frontotemporal
dementia; AD – Alzheimer disease balance. This denotes that both FTD and AD have a
deficit in dynamic balance than control group [Table 4].
Limits of stability ‑ Single task Alzheimer group had a significant deficit in overall LOS Indian Journal of Psychological Medicine | Volume 39 | Issue 2 | March-April 2017 179 [Downloaded free from http://www.ijpm.info on Friday, March 31, 2017, IP: 202.177.173.189]
Velayutham, et al.: Gait and balance in cortical dementia Table 3: Comparison of parameters in patients with FTD and AD during single and dual tasking
Gait parameters FTD Ambulation index (maximum=100)
Single
Dual
Step cycle
Single
Dual
Step length right
Single
Dual AD Control
Mean±SD Mean±SD P Mean±SD P 66.13±26.37
55.75±25.19 0.04* 63.63±18.68
56.88±17.93 0.00 (>0.1)* 78.28±27.61
85.63±6.14 NS 0.57±0.28
0.47±0.25 0.05* 0.54±0.22
0.46±0.18 NS 0.89±0.13
0.78±0.10 NS 0.32±0.17
0.37±0.22 0.02* 0.42±0.13
0.44±0.17 NS 0.45±0.17
0.42±0.11 NS P NS – Not significant; SD – Standard deviation Table 4: Between group comparison of balance‑single task
Single task Mean±SD
Control FTD
Dynamic balance
OBI
API
MLI
LOS
Overall
Forward
Backward right
Time P (ANOVA)
AD Post hoc comparison (P=0.05)*
FTD versus control
FTD versus AD
AD and control 3.56±0.94
2.76±0.72
2.40±0.76 2.40±0.50
1.91±0.53
1.48±0.52 3.36±1.11
2.70±0.79
2.08±0.77 0.037*
0.041*
0.046* 0.017*
0.023*
0.016* NS
NS
NS 0.054*
0.034*
0.099 14.75±20.67
8.63±10.46
7.25±0.30
285±31 24.25±12.11
34±16.61
22±14.50
185±62 5.38±6.32
3.88±7.22
4.63±6.73
284±47 0.049*
0.00 (<0.001)
0.008*
0.001* 0.198
0.000*
0.012*
0.324 NS
NS
NS
NS 0.015*
0.000*
0.004*
0.041* *Significant (P<0.05). NS – Not significant; MLI – Mediolateral index; API – Anteroposterior index; OBI – Overall balance index;
LOS – Limits of stability; SD – Standard deviation Table 5: Dual task balance analysis
Dual task
FTD
MLI
LOS
Backward
Right
FR
BR
Time 2.10±0.68
8.88±16.79
6.50±11.55
5.75±10.62
11.25±18.57
9.50±18.88
278±63.94 Mean±SD
Control
1.42±0.42
16±8.68
16±10.79
15.50±11.63
20.25±12.45
20±15.82
217±69.15 P (ANOVA)
AD
2.48±1.12
1.63±3.85
1±2.64
0.63±1.18
0.00±0.00
0.00±0.00
301±0.00 0.044*
0.055*
0.019*
0.012*
0.034*
0.035*
0.016* Post hoc comparison (P=0.05)
FTD versus control
FTD versus AD
AD versus control
NS
NS
0.058
0.044
NS
NS
0.036 NS
NS
NS
NS
NS
NS
NS 0.014*
0.017*
0.006*
0.004*
0.010*
0.010*
0.006* LOS – Limits of stability; FR – Forward right; BR – Backward right; MLI – Mediolateral index; SD – Standard deviation; FTD – Frontotemporal
dementia; AD – Alzheimer disease score in comparison with controls. FTD group had no
deficit in overall LOS score except few directions wise
deficit than controls. FTD group showed deficit in
forward, backward right direction (BR) than controls
whereas AD group had deficit in overall, forward (F),
backward (B), forward right (FR), forward left (FL),
and backward right (BR) direction. Both FTD and AD
groups consumed more time to complete the task than
the controls [Table 4 and Figure 4]. Limits of stability ‑ Dual task
Overall LOS, forward, backward, right, forward
right (FR), backward right (BR), was significantly
reduced, consumed more time to complete the task
in AD group compare to controls. FTD found to have
issues only in backward, right directions and consumed
more time complete the task than the controls
[Table 5 and Figure 5]. Dynamic balance ‑ Dual task
The OBI was significantly affected between FTD and
control group. Mediolateral stability index (MLI) was
significantly affected between AD and controls
[Table 5]. Gait analysis
The gait parameters such as distance walked, speed,
step cycle, CV of steps in the right, left leg, and AI were
affected in FTD and AD from controls in single, dual
task gait [Table 6]. 180 Indian Journal of Psychological Medicine | Volume 39 | Issue 2 | March-April 2017 [Downloaded free from http://www.ijpm.info on Friday, March 31, 2017, IP: 202.177.173.189]
Velayutham, et al.: Gait and balance in cortical dementia Table 6: Gait parameters in patients with FTD vs controls and AD vs controls
Gait parameters
Single task
Distance
Speed
Co efficient variation right
Dual task
Distance
Speed
Step cycle
AI
CV right (%)
CV left (%) FTD Mean±SD
Control AD P (ANOVA) FTD versus control* AD versus control* 43.13±27.21
0.35±0.22
87.13±48.51 87.50±30.88
0.73±0.26
30.50±19.94 49.75±17.73
0.41±0.14
61.63±9.50 0.005
0.005
0.005 0.003
0.002
0.001 0.008
0.008
0.056 36.75±25.22
0.30±0.20
0.47±0.25
55.75±25.19
70.25±26.08
76.38±28.99 80.63±25.60
0.67±0.21
0.78±0.10
85.63±6.14
32.38±17.21
34.25±21.55 41.25±16.14
0.33±0.13
0.46±0.18
56.88±17.93
71.75±17.73
71±19.09 0.001
0.001
0.004
0.005
0.001
0.003 0.001
0.001
0.004
0.004
0.001
0.002 0.002
0.002
0.003
0.005
0.001
0.005 *P<0.05. AI – Ambulation index; SD – Standard deviation; FTD – Frontotemporal dementia; AD – Alzheimer disease; CV – Co efficient
variation Figure 4: Between group single task analysis of limits of stability.
Alzheimer diseases performed worst in various direction. LOS – Limits
of stability; FR – Forward right; R – Right; L: Left; BL – Backward left;
FL – Forward left; F – Forward; B – Backward; BR – Backward right DISCUSSION
Even though AD and FTDs are predominantly
concerned with cognitive functions balance and gait
are significantly affected subclinically in both groups
compared to controls. Controls also had problems
during dual tasking in all parameters indicating
the role of divided attention in gait and balance
in even healthy aging. However, patients with
FTD had significant dynamic balance component
abnormalities evidenced by higher value in OBI
and API sparing MLI, patients with AD, had poor
scores during dual task score in MLI only, sparing
OBI and MLI.
LOS analysis, the individual direction wise analysis,
persons with FTD revealed poor score in Forward
left direction and AD had poor score in backward
direction. The overall LOS score did not show any
differentiation as the entire three group had poor score
in the dual task. Figure 5: Between group dual task analysis of limits of stability.
Alzheimer diseases performed worst in various direction (P = 0.05).
Lower the value indicates poorer the balance. LOS – Limits of stability;
FR – Forward right; BR – Backward right; MLI – Mediolateral index;
FTD – Frontotemporal dementia; AD – Alzheimer disease; R – Right;
L – Left;   FD – Forword; – BL – Backward left; FL – Forward left Single versus dual task gait performance
Patients with FTD showed a reduction of step cycle,
and step length and overall gait score, i.e., AI. The AD
subjects AI score too significantly reduced in dual task
though there was no specific gait parameters affected.
The between group
Both FTD and AD patients have balance and gait
difficulties than controls in single as well as dual task
but AD seems to be having deficit more on balance
especially LOS component of balance. CONCLUSION
This study reveals balance and gait problems in normal
elderly, as well as patients with AD and FTD during
dual tasking indicating the role of divided attention.
However, the abnormality is significantly more in
patients with FTD and AD. Patients with FTD and Indian Journal of Psychological Medicine | Volume 39 | Issue 2 | March-April 2017 181 [Downloaded free from http://www.ijpm.info on Friday, March 31, 2017, IP: 202.177.173.189]
Velayutham, et al.: Gait and balance in cortical dementia AD have abnormalities in overall AI, but patients with
FTD have significant abnormalities in stride length and
step cycle which is unaffected in AD. With reference to
balance, all parameters are uniformly affected in FTD,
but mediolateral balance is most affected in AD. Patients
with FTD have a tendency to tilt forward, but AD have
tendency to tilt backward. This unique information
indicates a differential pattern of balance and gait
impairment subclinically in cortical dementias. Uniform
but moderate involvement in FTD can be explained by
the role of frontal‑subcortical circuits as the cause of
impairment in FTD and the sensory WHERE pathway
involvement in patients with AD. These differences
might serve as a marker to differentiate these two
conditions in the early stages. Postural stability training
early in patients with AD and gait training in patients
with FTD might help in delaying future development
of falls in these patients. However, the study needs to
be repeated in a larger population.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest. REFERENCES
1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 182 Borson S, Raskind MA. Clinical features and pharmacologic
treatment of behavioral symptoms of Alzheimer’s disease.
Neurology 1997;48 5 Suppl 6:S17‑24.
Sudarsky L. Geriatrics: Gait disorders in the elderly. N Engl
J Med 1990;322:1441‑6.
Alexander NB, Mollo JM, Giordani B, Ashton‑Miller JA,
Schultz AB, Grunawalt JA, et al. Maintenance of balance,
gait patterns, and obstacle clearance in Alzheimer’s disease.
Neurology 1995;45:908‑14.
Allali G, Assal F, Kressig RW, Dubost V, Herrmann FR,
Beauchet O. Impact of impaired executive function on gait
stability. Dement Geriatr Cogn Disord 2008;26:364‑9.
Allali G, Dubois B, Assal F, Lallart E, de Souza LC, Bertoux M,
et al. Frontotemporal dementia: Pathology of gait? Mov
Disord 2010;25:731‑7.
Allan LM,...

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