Outcome measures for the assessment of balance and posture control in cerebellar ataxia

Abstract

Background: Discrepancies exist in the use of outcome measures for the assessment of balance and
postural control among people with cerebellar ataxia. There is a need to explore the spectrum of tools used
in order to determine their utility.
Objectives: The aims of this narrative review were to identify, categorize, and discuss outcome measures
used for the evaluation of balance and postural control in cerebellar assessment and intervention, and to
identify outcome measures which might relate to the localization of cerebellar lesion.
Major findings: Electronic search of the evaluation of cerebellar interventions and identification or illustration
of clinical features of problems relating to balance and postural control identified 45 outcome measures.
Using the international classification of functioning, the outcome measures were categorized as: health
condition-specific (n57), body structure and function level (n513), activity level (n525), and none at a
participatory level. Accessibility, time required to perform, and psychometric property testing determined
the utility of outcome measures. Frequency and amplitude of postural sway, and measures obtained from
force plate testing were used to localize the cerebellar lesion.
Conclusion: A wide range of outcome measures were used to assess balance and postural control deficits;
none of the clinical tools appeared to localize cerebellar lesion. Health condition-specific outcome
measures were used for cerebellar intervention trials and psychometric properties of outcome measures at
an activity level were not tested among pure cerebellar lesions. Further investigation is warranted to
streamline the utility and selection of outcome measures for clinical practice.

Full text

Narrative Review
Outcome measures for the assessment of
balance and posture control in cerebellar
ataxia
Stanley John Winser
1
, Leigh Hale
1
, Leica S. Claydon
1,2
, Cath Smith
1
1
Centre for Physiotherapy Research, University of Otago, New Zealand,
2
Department of Allied Health and
Medicine, Anglia Ruskin University, Chelmsford, UK
Background: Discrepancies exist in the use of outcome measures for the assessment of balance and
postural control among people with cerebellar ataxia. There is a need to explore the spectrum of tools used
in order to determine their utility.
Objectives: The aims of this narrative review were to identify, categorize, and discuss outcome measures
used for the evaluation of balance and postural control in cerebellar assessment and intervention, and to
identify outcome measures which might relate to the localization of cerebellar lesion.
Major findings: Electronic search of the evaluation of cerebellar interventions and identification or illustration
of clinical features of problems relating to balance and postural control identified 45 outcome measures.
Using the international classification of functioning, the outcome measures were categorized as: health
condition-specific (n57), body structure and function level (n513), activity level (n525), and none at a
participatory level. Accessibility, time required to perform, and psychometric property testing determined
the utility of outcome measures. Frequency and amplitude of postural sway, and measures obtained from
force plate testing were used to localize the cerebellar lesion.
Conclusion: A wide range of outcome measures were used to assess balance and postural control deficits;
none of the clinical tools appeared to localize cerebellar lesion. Health condition-specific outcome
measures were used for cerebellar intervention trials and psychometric properties of outcome measures at
an activity level were not tested among pure cerebellar lesions. Further investigation is warranted to
streamline the utility and selection of outcome measures for clinical practice.
Keywords: Assessment, Balance, Cerebellar ataxia, Outcome measures, Postural control
Introduction
Balance and postural control are two different yet
interconnected entities which work towards achieving
a state of equilibrium. In this context, we define
balance as an ability of an individual to maintain the
state of equilibrium during motion or dynamic
stability and postural control as an actively stabilized
orientation of the body and its segments in space and
in relation to each other to maintain static stability.
1
The cerebellum plays an important role in coordinat-
ing inputs from other neural systems to fine tune
postural control, balance, and locomotion.
2
Lesions
to the cerebellum lead to cerebellar ataxia, a
heterogeneous group of conditions which include
genetic and non-genetic forms.
3
Ataxias are char-
acterized clinically by deficits in co-ordinated oculo-
motor, speech, limb, balance, and gait function.
4
Lesions to the cerebellum can negatively influence
balance and postural control,
5
exhibited as abnormal
postural sway, impaired postural responses,
6
impaired
anticipatory adjustments,
7
and ataxic gait
8
resulting in
poor balance and an increased incidence of falls.
9
These movement deficits are observable; however,
there are no guidelines to direct selection of outcome
measures for the quantification and grading of
problems relating to balance and postural control in
individuals with cerebellar ataxia.
It is unclear how well current outcome measures
perform in the evaluation of interventions for a
cerebellar ataxia population. Furthermore, a wide
range of outcome measures are used in the assessment
of balance and postural control regardless of the area
of cerebellum involved despite evidence that the
clinical presentation of balance and postural control
in people with cerebellar lesions may vary with the
location of insult to the cerebellum.
2
Therefore, the
aims of this narrative review were to identify,
categorize, and discuss outcome measures used in
Correspondence to: Stanley John Winser, Centre for Physiotherapy
Research, University of Otago, New Zealand. Email: stanley.winser@
otago.ac.nz
ßW. S. Maney & Son Ltd 2013
DOI 10.1179/1743288X13Y.0000000065 Physical Therapy Reviews 2013 VOL.18 NO.2 117

the evaluation of balance and postural control in
cerebellar assessment and intervention, and to
identify outcome measures of balance and postural
control that might relate to localization of cerebellar
lesions.
Method
An electronic search of the following databases
identified pertinent literature: Google Scholar, Index
New Zealand, Ovid Medline, ProQuest Central,
ScienceDirect, Scopus, and Web of Knowledge. The
search terms used were ‘posture’ AND ‘cerebellar
ataxia’ AND ‘postural control’ AND ‘balance’ AND
‘imbalance’ AND ‘posturography’. Articles related to
evaluation of clinical interventions for cerebellar
signs, identification or illustration of clinical presenta-
tion of problems with balance and postural control
relating to cerebellar lesions, of any cause were selected
for review (see Fig. 1). Articles were excluded if: data
were inadequate (the abstract was only available for
electronic access), trials involved animals, studies on
cerebellar lesions did not involve postural control and
balance, or articles were published in languages other
than English. One author (SW) searched the database
and selected the articles.
The international classification of functioning,
disability and health
10
guided classification of the
outcomes reported in the selected articles into one of
the following four groups: health condition-specific
outcome measures, outcome measures of body
Figure 1 The flow of study and the number of outcome measures identified.
Winser et al. Balance and postural control outcome measures among cerebellar ataxia
118 Physical Therapy Reviews 2013 VOL.18 NO.2

structures and functions, outcome measures of activ-
ity, and outcome measures of participation. The
following information was extracted from each
identified outcome measure: (1) domain: subcompo-
nents of the tool included and components of balance
or postural control assessed by the tool; (2) scoring; (3)
reported psychometric properties including inter-rater
and/or intra-rater reliability, test–re-test reliability,
internal consistency, and validity; and (4) time taken to
complete the test.
Results
The search identified 131 full text articles of which 76
articles met the inclusion criteria. Fifty-five articles
were excluded; the main reasons for exclusion were
inadequate data (n512), trials involving animals
(n516), studies on cerebellar lesions which do not
involve postural control and balance (n521), and
articles published in languages other than English
(n56). In the 76 articles reviewed, 45 different
outcome measures were identified, 7 were health
condition-specific, 13 were related to body structure
and function, 25 were related to activity, and no
outcome measures were identified at a participatory
level. Each category was tabulated separately and the
identified outcome measures were listed according to
the frequency of utility as shown in Tables 1–3.
Health condition-specific outcome measures
Seven health condition-specific outcome measures
were identified from nine studies as shown in Table 1.
The dimensions tested included balance, gait, limb
kinetic function, and speech; overall these dimensions
were used to grade the severity of ataxia. The
international cooperative ataxia rating scale
(ICARS)
11
graded ataxia based on four domains:
posture and gait, kinetic function, speech, and
oculomotor disorder. The posture and gait subcom-
ponent used seven task-oriented tested items specific
to balance and gait. The coordination ability and
tremor system (CATSYS) 2000,
12
a portable device
assessing tremor, reaction time, hand coordination,
and postural sway used the force plate to study
postural control.
13
The ataxia functional composite
scale (AFCS),
14
a scale for grading ataxia used a
combination of visual acuity, hand dexterity, and
timed walk test. The timed 25-foot walk (T25W) test
was used for the assessment of balance and gait.
Maximum scores of the outcome measures ranged
from 30 to 100. The AFCS was calculated using the
sum of Z score of the three tests (low contrast visual
acuity, the 9-hole peg test, and the timed 25-foot
walk), Z score being an indication of the number of
standard deviations that an element is from the mean.
Inter-rater reliability, intra-rater reliability, and
internal consistency were studied for most outcome
measures. Time taken to complete the tests varied
from over 30 minutes for the ICARS or not
reported
15
or less than 15 minutes for the scale for
the assessment and rating of ataxia (SARA),
16
an
ataxia grading scale having eight subcomponents.
The subcomponents gait, stance, and sitting of the
SARA appear to assess balance among the corre-
sponding activities.
17
Five of the seven outcome
measures at the health condition-specific level rated
severity of ataxia.
11,14–16,18
The Fregly–Graybiel
ataxia battery,
19
a scale used to quantify gait and
balance assessed using a combination of Sharpened
Romberg, walk in line, and stand on one foot tests.
The CATSYS 2000 quantified tremor, reaction time,
hand coordination, and postural sway using a
computer-based assessment among people with
movement disorders including cerebellar ataxia. The
outcome measures assessing the severity of ataxia
had subcomponents to assess balance and postural
control.
The grading of balance differed from each scale, in
that the brief ataxia rating scale (BARS) and AFCS
graded balance based on the score obtained while
walking. The ICARS, SARA, and Friedreich’s ataxia
scale (FARS) had distinct balance-related compo-
nents which included sitting balance, standing bal-
ance, body sway, and walking capacity to grade
balance and posture. The ICARS had the most
comprehensive assessment for balance having seven
items specific to balance. The FARS grades ataxia
using the domains functional staging of ataxia,
activities of daily living, and neurological examina-
tion. The neurological examination is further classi-
fied to assess independent functions among which the
upright stability component has items relevant to
balance assessment. One of the items of the upright
stability component utilizes the T25W test to assess
the gait.
18
The ICARS is frequently used in pharmacological
studies,
20
and has 19 items in total to assess posture
and gait disturbances, kinetic function, speech
disorders, and oculomotor disorders.
21,22
This test
takes over 30 minutes to complete, and thus a shorter
version was developed, the BARS. The BARS has
five items (gait, knee-tibia test, finger-to-nose test,
dysarthria, and oculomotor abnormalities) resulting
in a maximum score of 30 and all the items are a part
of the modified international cooperative ataxia
rating scale.
15
One study in this review reported the
use of ICARC, FARS, SARA, and AFCS in
evaluating the progress of Fredrick’s ataxia.
18
Although, as this review reports, many tools have
been developed, identifying the most suitable measure
for evaluation of balance and postural control as well
as grading of ataxia remains inconclusive. Most of
the health condition-specific outcome measures were
used as tools for the assessment and grading of
Winser et al. Balance and postural control outcome measures among cerebellar ataxia
Physical Therapy Reviews 2013 VOL.18 NO.2 119

Table 1 Health condition-specific outcome measures
Outcome measures Domain Scoring
Psychometric properties
Time taken
Inter-rater/intra-rater
reliability Test–re-test reliability Internal consistency Validity
The international
cooperative ataxia
rating scale (ICARC)
Grading for ataxia.
Balance assessed
using posture and
gait (PG)
subcomponent
Total: 100 High inter-rater
reliability (ICC50.95)
High test–re-test
reliability (ICC50.97)
Adequate internal
consistency
(Cronbach’s a50.94)
Good internal
structural validity
Over 30 minutes
PG: 34
Min.: 0 Max.: 100
Scale for the
assessment and rating
of ataxia (SARA)
Grading for ataxia.
Subcomponents
gait, stance, and
sitting assess balance
among the
corresponding
activities
Total: 40 High inter-rater
reliability (ICCs5
0.90–0.96)
High test–re-test
reliability (ICCs5
0.90–0.96)
High internal
consistency
(Cronbach’s a50.94)
Good internal
structural validity
Less than
15 minutesGait: 8
Stance: 6
Sit: 4
Min.: 0 Max.: 40
Coordination ability
and tremor system
(CATSYS 2000)
Quantifies tremor,
reaction time, hand
coordination, and
postural sway. A force
plate is used to assess
postural sways.
Not reported. Not reported Not reported Not reported Normative data
across different
age groups of
normal individual
determined
15 minutes
The ataxia functional
composite scale
(AFCS)
Functional performance
measure assessing
vision, upper limb
function, and gait.
The T25W test is used
to assess gait and
mobility function.
Calculated as a sum
of Z scores of each
subtest and total
divided by 3.
Not reported Good test–re-test
reliability established
(ICC not reported)
Not reported Strong correlation
with the ICARS
(Spearman’s rank
correlations:
20.90 to 20.95)
20 minutes
Brief ataxia rating
scale (BARS)
Grading ataxia using
five subcomponents.
Gait subcomponent
assesses mobility
and reflects on
balance function.
Total: 30 High inter-rater
reliability (ICC5
0.91)
Not reported High internal
consistency
(Cronbach’s a50.90)
Not reported Not reported
Walking capacity: 8
Min.: 0 Max.: 30
Fregly–Graybiel
ataxia battery
Quantifies gait and
balance. Uses sharpened
Rhomberg’s, stand on
one foot and walk in
line to comment on balance.
Not reported. Not reported Not reported Not reported Not reported Not reported
Friedreich’s ataxia
rating scale (FARS)
Ataxia rating scale with
functional stage of
ataxia, activities of
daily living, and
neurological examination.
Upright stability
component of the
neurological examination
assesses balance
Functional staging: 6.0 Excellent inter-
rater reliability
(ICC not reported)
among selective
items of the scale
Not reported Not reported Good correlation
of ICARS and
FARS scores
(r50.933; P,0.0001)
30 minutes
Activities of daily living: 36
Neurological
examination: 129
Upright score: 28
Note: T25W: twenty-five-foot walk test; ICC: intraclass correlation coefficient; P: level of significance; r: correlation coefficient; Min.: minimum; Max.: maximum.
Winser et al. Balance and postural control outcome measures among cerebellar ataxia
120 Physical Therapy Reviews 2013 VOL.18 NO.2

Table 2 Outcome measures on body structure and function
Outcome
measures Domain Scoring
Psychometric
properties
Time taken
Inter-rater/intra-
rater reliability
Test–re-test
reliability
Internal
consistency Validity
Force platform Assess postural
control and
balance by
quantifying the
movement of
centre of
pressure
Expressed as hertz
(oscillations per
second).
Not reported Not reported Not
reported
Not reported Testing time is
negligible.
(preparation/
calibration/results
processing are
time-consuming).
Surface EMG Quantifies timing
of muscle
contraction in
relation to balance
and postural
control
The timing and
strength of muscular
contraction are
expressed as
milliseconds and
milliamperes
respectively.
Not reported Not reported. Not
reported
Not reported Testing time
negligible.
(preparation/
calibration/
results
processing
are time-
consuming).
Sensory
organization
test (SOT)
Measure of
postural control
assessing
sensory interaction
Postural sway
measured by force
platform and
time sustained in
each of the 6
conditions
measured.
Not reported Fair to good
test–re-test
reliability (ICCs
50.26 in
condition 3,
and 0.68 and
0.64 in
conditions
5 and 6).
Not
reported
Acceptable
predictive
validity among
mild stroke.
20 seconds
per level of
the test (six
levels).
Whole body
kinematics
Posture control and
balance assessed
as movements
happening at
different body
segments that
is expressed in
degrees
Measure of total
body segments
displacement of
COM in different
planes.
Not reported Not reported Not
reported
Not reported Testing time
negligible.
(preparation/
calibration/
results
processing
are time-
consuming).
Clinical test
for sensory
integrity and
balance
(CTSIB)
Test of balance and
sensory integration
Time sustained in
each of the six
conditions.
Excellent
interrater
reliability
(r50.99)
among
neurologically
asymptomatic
adults
Excellent inter-
rater reliability
(r50.99) among
neurologically
asymptomatic
adults
Not reported Discriminant
validity: significant
difference
between n
ormal and people
with vestibular
dysfunction.
20 minutes
Winser et al. Balance and postural control outcome measures among cerebellar ataxia
Physical Therapy Reviews 2013 VOL.18 NO.2 121

Outcome
measures Domain Scoring
Psychometric
properties
Time taken
Inter-rater/intra-
rater reliability
Test–re-test
reliability
Internal
consistency Validity
Minimum time:
0 second
Maximum time:
30 second in
each condition
Potentiometer Assess ROM at
ankle joint during
static stability and
perturbations
Measured as
degrees of
movement at
ankle, used
always along
with a force
plate.
Not reported Not reported Not reported Not reported Negligible.
(preparation/
calibration/
results
processing
are time-
consuming).
Accelerometer Works in
conjunction with
a force platform
to assess
postural control,
measures
trunk sway in
antero posterior
and lateral
directions
Postural sway
expressed
in degrees.
Not reported Not reported Not reported Not reported Negligible.
(preparation/
calibration/results
processing are
time-consuming).
The balance
evaluation-
systems test
(BESTest)
Assess the cause
for balance
instability which
includes
biomechanical,
stability limits,
postural responses,
sensory
orientation, and
dynamic balance
The test has 27
items to be tested
Excellent
inter-rater
reliability
(ICC50.96)
Excellent test–re-test
reliability (ICC50.091)
among subjects with PD.
Not reported Moderate
concurrent
validity with the
ABC scale
(r50.636).
Tested among
people with
balance
problems of
different causes.
20–30 minutes
Biomechanical
instability: 15
Stability limits: 21
Anticipatory: 18
Reactive: 18
Sensory
orientation: 15
Gait stability: 21
Min.: 0 Max.: 108
Photographic
anthropometry
and light track
registration
Balance
assessment
through static
photography. Static
pictures of posture
taken following a
1-minute hold.
Static pictures
of different
postures
compared before
and after trial.
Not reported Not reported Not reported Not reported 1 minute for
every posture
Table 2 Continued
Winser et al. Balance and postural control outcome measures among cerebellar ataxia
122 Physical Therapy Reviews 2013 VOL.18 NO.2

Outcome
measures Domain Scoring
Psychometric
properties
Time taken
Inter-rater/intra-
rater reliability
Test–re-test
reliability
Internal
consistency Validity
The SwayStar
system
Measure of
postural control.
Postural sway
and tremors
measured using
transducer
fixed to the waist.
Postural sway
expressed in
degrees.
Not reported Not reported Not reported Not reported Recording time
negligible.
(preparation/
calibration/results
processing are
time-consuming).
Anima plantar
pressure
measuring
system (ANIMA)
Measure of gait
parameters.
Measures stride,
gait cycle,
step length, and
step width,
gait velocity and
cadence.
The results of the
variable are
expressed as time,
distance, speed, or
cycles per second.
Not reported Not reported Not reported Not reported Negligible.
(preparation/
calibration/
results
processing
are time-
consuming).
Sharpened
Rhomberg test
Static balance,
measuring
one’s ability to
stand with
eyes closed
Timed test, ability
to maintain stance
for 60 seconds is
calculated
Not reported Not reported Not reported Not reported 1 minute
Min.: 0 Max.: 60
The number
of falls, range
of COP excursion,
and COP path
length
Dynamic balance
measured
with the number of
falls during
a series of balance
activities and
postural control
assessed using
a force plate
Recording number
of falls before and
after treatment
session and COP
assessment
similar to force
plate measurements.
Not reported Not reported Not reported Not reported 20 seconds
each activity
(12 activities)
Note: EMG: electro myography; ROM: range of motion; COP: centre of pressure; COM: centre of mass; ICC: intraclass correlation coefficient; r: correlation coefficient; P: level of significance; Min.: minimum;
Max.: maximum.
Table 2 Continued
Winser et al. Balance and postural control outcome measures among cerebellar ataxia
Physical Therapy Reviews 2013 VOL.18 NO.2 123

Table 3 Outcome measures on activity
Outcome
measures Domain Scoring
Psychometric
properties
Time taken
Inter-rater/
intra-rater
reliability
Test–re-test
reliability
Internal
consistency Validity
Berg balance
scale (BBS)
Dynamic balance
assessed by
performing 14
commonly used
functional tasks.
Each task scored
between 0 and
4. Scores less
than 40 indicative
of high risk of fall.
Excellent inter-
rater (ICC50.99)
Excellent test–
re-test reliability
(ICC50.98),
tested among
a variety of
neurological
disorders and
older adults
Not reported Excellent criterion
and construct
validity
15–20 minutes
Min.: 0 Max.: 56
The timed up
and go test (TUG)
Measure of
balance, functional
mobility, and gait
Timed test.
Older adults
requiring more
than 13.5 seconds
to complete the
task are considered
at the risk of fall.
Excellent inter-
rater reliability
(ICC50.95)
Excellent test–
re-test (ICC50.96)
Not reported Excellent
criterion and
adequate
construct
validity tested
among stroke,
older adults,
SCI, and PD.
Less than
5 minutes
Activities-specific
balance confidence
scale (ABC)
Measure of
balance and
functional mobility.
Self-perceived level
of confidence
during 16 activities.
The confidence of
performing each
activity is self-rated
from 0 to 100%
confidence.
Not reported Excellent test–
re-test reliability
(ICC50.94)
Excellent
internal
consistency
(Cronbach’s
a50.95)
Adequate
concurrent
validity when
correlated with
the BBS. Tested
among stroke, PD,
and older adults.
10–20 minutes
Dizziness handicap
inventory (DHI)
Measure of
perceived level
of handicap due
to dizziness.
Total score 100.
Each question is
scored 0 for ‘No’,
2 for ‘Sometimes’,
and 4 for ‘Yes’.
Not reported Good test–re-
test reliability
(0.97)
Good internal
consistency
(0.91) and
among patient
with dizziness
of vestibular
origin.
Acceptable
concurrent
validity among
MS.
Not reported
Min.: 0 Max.: 100
Dynamic gait
index (DGI)
Measure of
mobility and
dynamic balance.
Total: 24. Adequate to
excellent inter-
rater reliability
(ICC50.98) and
intra-rater reliability
(ICC50.98)
Excellent test–
re-test reliability
(ICC§0.94)
among people
with stroke
Not reported Excellent
criterion and
construct
validity among
stroke PD and
older adults.
Less than
10 minutes8 tasks related to
walking assessed.
Scores above 21
indicate minimal
or no risk of fall.
Min.: 0 Max.: 24
Winser et al. Balance and postural control outcome measures among cerebellar ataxia
124 Physical Therapy Reviews 2013 VOL.18 NO.2

Outcome
measures Domain Scoring
Psychometric
properties
Time taken
Inter-rater/
intra-rater
reliability
Test–re-test
reliability
Internal
consistency Validity
Single-limb stance
time (SLST) of the
dominant leg
Measure of
postural control.
Timed test Moderate to
good intersession
reliability (ICC:
0.56–0.99) among
children with CP
Good test–re-
test reliability
in children in
assessing balance
Not reported Not reported Less than
1 minute
Limits of stability
(LOS)
Measure of
dynamic balance.
A feature of the
‘balance master’.
Measures movement
velocity, maximal
excursion, and
directional control
along eight
different directions.
Not reported Good test–re-
test reliability
(ICC50.82)
tested among
older adults
Not reported Acceptable
predictive
validity among
older adults
5–10 minutes
Five times sit-to-
stand (FTSTS) test
Measure of
dynamic balance
and lower extremity
strength.
Timed test Not reported High degree of
test–re-test
reliability (r50.882).
Not reported Valid measure
of balance
and lower-
extremity
strength among
older adults
(statistics not
reported).
Less than
1 minute.
Standing balance
assessment
according to
Bohannon
Measure of
postural control
and balance.
Assess the ability
to maintain upright
standing with
increasing level
of challenge.
Total: 4 Not reported Not reported Not reported Not reported Less than
5 minutes5 point ordinal
scale, scores
ranging between
0 (inability to stand)
to 4 (normal standing).
Min.: 0 Max.: 4
Mokkens functional
independence
assessment
Measure of
functional
independence.
Total: 15. Not reported Not reported Not reported Not reported 10 minutes
5 tasks assessed
using a 4 point
ordinal scale.
Higher the score
obtained, better
the balance.
Min.: 0 Max.: 15
Self-reported fall
history
Measure of
dynamic balance,
involves self-
reporting of falls.
Number of times
the participant fell
over a period of time.
Not reported Not reported Not reported Not reported Negligible
Table 3 Continued
Winser et al. Balance and postural control outcome measures among cerebellar ataxia
Physical Therapy Reviews 2013 VOL.18 NO.2 125

Outcome
measures Domain Scoring
Psychometric
properties
Time taken
Inter-rater/
intra-rater
reliability
Test–re-test
reliability
Internal
consistency Validity
Functional
independence
measure (FIM)
Measure of
functional
independence.
Total518 items
Motor tasks513
Not reported Excellent test–
re-test reliability
(ICC50.90)
Excellent internal
consistency:
(Cronbach’s
a50.93) among
older adults
Excellent
concurrent
validity tested
among stroke
30–45 minutes
Cognitive tasks55.
Each task scored
out of 7.
Min.: 18 Max.: 126
Time to complete
a balance task
Measure of
dynamic balance.
Timed test, requiring
the subject to touch
the top of a step
with each foot four
times.
Not reported Not reported Not reported Not reported Less than
1 minute
Paediatric evaluation
of disability inventory
(PEDI)
Measure of
functional
capabilities,
performance
and changes in
functional skills
Total5237 items. High inter and
intra-rater
reliability
(ICC: 0.95–0.99)
Not reported High internal
consistency
(Cronbach’s
a: 0.90–0.99)
High concurrent
validity among
children with
disability aged
6 months to 7
years.
45–60 minutes
Functional skills5
197 (scored between
0 and 1)
Caregiver assistance:
20 (scored between
0 and 5)
Modification520
(scored as type
of modification).
Tinetti performance
oriented mobility
assessment (POMA)
Measure of gait
and balance.
Total 516 items Good inter-rater
reliability (ICC:
0.91–0.93)
Good test–re-
test (ICC: 0.82–
0.86)
Not reported Good concurrent
and discriminant
validity among
older adults
10–15 minutes
Gait57 items
Balance59 items
Most of the items
scored on a three
point ordinal scale.
Min.: 0 Max.: 28
Functional systems
scale (FSS) and the
expanded disability
status scale (EDSS)
Measure of
functional status
and disease
progression in MS.
FSS assesses eight
functional systems
and EDSS grades
the stage of illness
due to MS.
High inter- and
intra-rater
reliability (ICC
not reported)
Not reported Not reported Good face
validity as a
measure of
combined body
structure and
function, and
activity level
assessment
among MS.
Not reported
Min.: 0.0 Max.: 10.0
Table 3 Continued
Winser et al. Balance and postural control outcome measures among cerebellar ataxia
126 Physical Therapy Reviews 2013 VOL.18 NO.2

Outcome
measures Domain Scoring
Psychometric
properties
Time taken
Inter-rater/
intra-rater
reliability
Test–re-test
reliability
Internal
consistency Validity
Functional reach (FR) Measure of
dynamic balance
and motor
performance.
Results obtained as
distance reached
in metres.
Scores ,6 inches
are indicative of
high risk for falls.
Excellent intra-
rater reliability
(ICC50.92) and
inter-rater
reliability (ICC5
0.98).
Excellent test–
re-test (ICC5
0.92)
Not reported Not reported 5 minutes
Clinical tests of
standing balance
Measure of
static balance
in standing and
postural control.
Timed test measuring
ability to sustain
each position up
to 30 seconds.
Not reported Not reported Not reported Not reported 5 minutes
Subjective
observatory
assessment of
standing and gait
Assess standing
balance motor
performance
and gait.
Subjective
description of
gait parameters
and standing.
Not reported Not reported Not reported Not reported Not reported
25-foot timed walk test Assess speed,
motor performance
during gait
and balance.
Timed test. Not reported Not reported Not reported Not reported Less than
5 minutes
Hauser
ambulation
index
Grading of
walking ability
among people
with MS.
Total: 10 stages. Not reported Not reported Not reported Not reported. Not reported.
0 indicated
‘asymptomatic’
and 9 ‘bound
to wheelchair’.
Timed
unsupported
stance
Measure of
standing
balance and
motor
performance
during standing.
Five point ordinal
scale ranging
between 0 (inability
to perform) and 4
(able to stand
unsupported for
2 minutes).
Not reported Not reported Not reported Not reported 2 minutes
Postural
assessment
scale for
stroke
patients
(PASS)
Measure of
postural control,
a scale specific
to people with
stroke.
Total512 items High inter-rater
and intra-rater
reliability (ICC
not reported)
Not reported High internal
consistency
(Cronbach’s
a50.95)
Excellent
predictive
validity and
good construct
validity in
assessing
postural control
among stroke
Not reported
Static55 items
Dynamic57 items.
Each item scored
from 0 to 3.
Min.: 0 Max.: 36
Table 3 Continued
Winser et al. Balance and postural control outcome measures among cerebellar ataxia
Physical Therapy Reviews 2013 VOL.18 NO.2 127

cerebellar lesion. None of these outcome measures
related to the localization of cerebellar lesion.
Outcome measures on body structure and
function
Thirteen outcome measures which assessed body
structure and function were identified from 32 articles
as shown in Table 2. The dimensions tested were
static and dynamic balance. The balance and postural
control assessment included quantification of centre
of pressure (COP), muscle contraction variables,
sensory interaction, joint range of motion, stability
limits, and gait variables. The scoring scheme,
execution, and interpretation varied between these
outcome measures; however, results of most of the
identified outcome measures of this category were
computer generated.
The psychometric properties of most of these
outcome measures were not reported. The sensory
organization test (SOT), a measure of dynamic
balance that assesses sensory interaction using force
plate and visual surround had fair to good test–re-test
reliability [intraclass correlation coefficient (ICC)
ranged between 0.26 in condition 3 to 0.68 and 0.64
in conditions 5 and 6].
23
Clinical test for sensory
integrity and balance (CTSIB)
24
and the balance
evaluation system test (BESTest)
25
had excellent
inter-rater reliability (r50.99 and ICC50.91 respec-
tively) . The CTSIB is a clinic-based assessment for
sensory interaction measuring one’s ability to effec-
tively use vision, vestibular, and somatosensory
inputs in maintaining balance. The BESTest
addresses the cause for balance instability at an
impairment level by assessing the following domains:
biomechanical, stability limits, postural responses,
sensory orientation, and dynamic balance.
26
All
laboratory-based assessments in this category took
minimal time to complete; however, the interpreta-
tion of the data requires careful preparation and
calibration and the results are time-consuming to
process and interpret. The BESTest was the most
time-consuming, taking 20–30 minutes to complete.
Outcome measures at the body structure and
function level were used to try and identify under-
lying impairments associated with imbalance and
poor postural control. Of the 13 outcome measures,
nine were performed in a laboratory. Twenty-one
articles used a force plate;
7,21,27–45
which is a
laboratory-based test comprising a plate on which
the individual stands that has four piezoelectric
transducers attached to four corners that measure
pressure and are operated via a computer. The
individual’s postural sway is a reflection of movement
of their COP on the force plate. The clinically based
tests (CTSIB,
46
BESTest,
25,26
and the sharpened
Rhomberg’s
47
) had reasonable clinical utility as they
do not require sophisticated equipment, and are
Table 3 Continued
Outcome
measures Domain Scoring
Psychometric
properties
Time taken
Inter-rater/
intra-rater
reliability
Test–re-test
reliability
Internal
consistency Validity
Equilibrium
coordination
test
Measure of
dynamic balance
and Coordination.
Calculate number
of steps taken out
of 10 cm wide
base of support
during tandem walking.
Not reported Not reported Not reported Not reported Less than 1 minute
Note: SCI: spinal cord injury; MS: multiple sclerosis; CP: cerebral palsy; PD: Parkinson’s disease; ICC: intraclass correlation coefficient; r: correlation coefficient; P: level of significance; Min.: minimum; Max.:
maximum.
Winser et al. Balance and postural control outcome measures among cerebellar ataxia
128 Physical Therapy Reviews 2013 VOL.18 NO.2

quick to execute and easy to perform. The sharpened
Romberg’s test assesses the static balance, requiring
the participant to perform tandem standing with eyes
closed and maintain the posture for 60 seconds.
47
The SOT was used in five studies,
42,48–51
three of
which were clinical intervention trials. Results of this
test interpret the contribution of vision, vestibular and
somatosensory inputs towards balance. However, like
the other laboratory tests, this outcome measure
requires sophisticated equipment.
One of the studies used photographic anthropo-
metry; however, this method of testing the progress of
balance over a period of time, has been criticized for
its subjectivity as it may not measure subtle changes
in balance over a period of time and for having no
psychometric properties tested.
52
Other measures used
to assess postural control at the body and structure
level were electromyography (EMG)
7,34–36,41,43,53
and
whole body kinematics.
37,53,54
Electromyography
involved recording variables such as latency, action
potential, duration, and symmetry of muscular con-
traction. Commonly, the EMG was coupled with the
force plate and the readings of the EMG were studied
in relation to the postural sway. Tibialis anterior,
gastrocnemius, soleus, quadriceps, hamstrings, para-
spinal, and abdominal muscles were commonly
measured with EMG when studying postural control.
Whole body kinematics normally involved three-
dimensional tracking system using infrared emitting
diodes. The diodes were placed symmetrically over
different body segments throughout the body.
Movements happening at these body segments were
captured using cameras during erect stance as well as
during perturbation in different directions. One study
combined EMG and whole body kinematics.
53
The force platform was used in conjunction with
the potentiometer,
30,31
accelerometer,
30,55
and num-
ber of falls during a series of activities
56
to measure
the COP. The potentiometer measured the ankle
range of motion during quiet stance, accelerometer
measured truck sway along antero-posterior, and
lateral directions and the number of falls assessment
required the participant to stand over the force
platform and perform a series of activities during
which the postural sway was tracked using COP. The
Swaystar system assessed the postural sway similar to
the accelerometer; however, a force platform is not
required for this device. Sway measuring transducer
was fixed to the waist. Movement of the truck
was measured bi-directional, antero-posterior, and
medio-lateral.
57
The anima plantar pressure measur-
ing system appeared to be a gait assessment tool
measuring the variables stride, gait cycle, step length,
and step width, gait velocity, and cadence.
58
One article was identified that used the pattern and
amplitude of postural sway, measured using force
plate to localize the cerebellar lesion.
31
People with
isolated lesions of the cerebellar functional zones had
distinct pattern of postural sway, for example lesions
of spinocerebellum result in an increased sway in an
antero-posterior direction whereas those of vestibu-
locerebellum involves a multi-directional sway. None
of the other identified outcome measures were able to
identify the site of lesion. The equipment used in the
laboratory-based trials has poor clinical utility as
they are costly, require a trained individual to
perform the assessment, and require the study
participants to come to a laboratory for testing.
Outcome measures on activity
Thirty-five articles reported using 25 outcome mea-
sures at an activity level. The outcome measures of
this category tested dynamic balance and functional
mobility. The domains used to test balance included
functional tasks, walking ability, self-perceived level
of confidence, lower limb strength, and self-reporting
on falls. The scoring scheme varied from cumulative
score of multiple items as in the Berg balance scale
(BBS), timed scores,
47
subjective self-reporting,
59
comprehensive inventory,
60
and grading of disease,
as in the functional system scale (FSS) and the
expanded disability status scale (EDSS).
61
The BBS
wasusedintenstudies
46,49–51,62–67
andthetimedupand
go (TUG) test was used in eight studies.
47,48,63,64,68–71
The BBS is a measure of dynamic balance assessing
14 commonly used functional tasks, and score
less than 40 is indicative of increased risk if fall.
However, the BBS needs to be used in conjunction
with other measures as a complete balance assess-
ment.
72
The TUG is a timed test for assessing
dynamic balance and functional mobility, and scores
above 13.5 seconds to complete the task are indicative
of increased risk of fall.
73
Both the BBS and TUG’s
psychometric properties have been extensively tested.
Both measures have established validity and reliability
in assessing balance among multiple groups of
populations, including those with cerebellar lesions.
64
Othertimedtestsidentifiedinthisreviewwerethe
single limb stance time (SLST) of the dominant lower
extremity,
48,59
the five times sit-to-stand test,
68
time to
complete a balance task,
69
clinical tests of standing
balance,
74
25-foot timed walk test,
71
and timed unsup-
ported stance.
65
The timed tests required the participant
to perform one or more functional activities and the test
was interpreted as the time taken to complete the task.
The subjective observational assessment of standing and
gait reported standing balance as a subjective description
of walking and stance with differing level of challenges.
75
The psychometric properties of these tests have not yet
been determined.
Balance assessment requiring self-reporting included
activities-specific balance confidence scale,
49,64,67,68
Winser et al. Balance and postural control outcome measures among cerebellar ataxia
Physical Therapy Reviews 2013 VOL.18 NO.2 129

dizziness handicap inventory,
64,67,68
self-reported fall
history,
59
and paediatric evaluation of disability
inventory (PEDI).
60
Measures of functional indepen-
dence used as an outcome of balance were functional
independence measure
76
and Mokkens functional
independence assessment.
77
Two outcome measures
were based on staging of balance and gait abilities, and
these were the EDSS
61,78
and Hauser ambulation
index.
64
There were three outcome measures that were
condition-specific, the FSS, the EDSS,
61,78
a scale for
assessing disability and symptom severity in multiple
sclerosis, and postural assessment scale for stroke
patients, a measure for trunk stability among people
with stroke.
79
Some of the other outcome measures
that were used as a balance assessment tool included
the dynamic gait index,
49,64,66–68
ameasureof
mobility and dynamic balance scored on a four-point
ordinal scale, the standing balance assessment
according to Bohannon,
77
the Tinetti performance-
oriented mobility assessment,
46
and the functional
reach (FR).
70,74
The time required to administer the
activity level outcome measures identified varied;
some outcome measures like the standing balance
assessment
74
and equilibrium coordination test
78
take
less than 5 minutes whereas the PEDI
60
and BBS
were reported to take over 30 minutes. The time
required to complete the test is an important factor in
determining clinical utility.
No studies at the activity level used a health
condition-specific outcome measure specific to cere-
bellar ataxia and most of the studies categorized
under this group were clinical trials studying treat-
ment effects. Of the identified 35 articles, four were
related to cerebellar assessment and the remaining
to cerebellar intervention. None of these outcomes
measures were used to localize the cerebellar lesion.
Discussion
This narrative review involved an electronic search of
articles related to balance and postural control in
people with cerebellar ataxia to identify, categorize,
and discuss the outcome measures used in cerebellar
assessment and intervention, and to identify the
outcome measures that relate to the localization of
cerebellar lesion.
In our review, we identified 45 outcome measures
that evaluated balance and postural control of
individuals with cerebellar lesions. Using the inter-
national classification of functioning, disability and
health, these outcome measures were categorized as
follows: 7 health condition-specific, 13 at a body
structure and function level, 25 at an activity level,
and none were identified at a participatory level.
Apart from the ICARS,
11
the health condition-
specific outcome measures were not commonly used
in clinical trials. None of these trials utilized these
tools for the localization of the cerebellar lesion site.
Most of the articles listed under this category were
studies which reported on scale development and
psychometric testing. Participants used in the psycho-
metric testing of the outcome measures identified had
spinocerebellar ataxia and Friedreich ataxia.
The ICARS has been widely used in the validation
of the other health condition-specific outcome
measures. Ilg et al. studied the influence of cerebellar
lesion on gait
80
establishing good correlation between
the gait parameters using kinematic analysis and limb
kinetic function using the ICARS, and the latter may
be considered the gold standard in determining
severity of ataxia. The ICARC is comprehensive,
especially in the assessment and grading of ataxia,
has excellent inter-rater reliabillty (ICC50.95) and
test–re-test reliability (ICC50.97), and excellent
internal consistency indicated by Cronbach’s aof
0.94, and has been used to differentiate between
patients with static and progressing ataxia.
21
There is
no cost to purchase the ICARS. However, the time
required to complete the ICARS (over 30 minutes)
and the need of physician or a trained technician
81
to
complete the assessment reduce the tool’s utility. The
BARS
15
a shorter version of the ICARC, which
includes only five items, and has excellent inter-rater
reliability (ICC50.93) and internal consistency
(ICC50.96) may have better clinical utility. The
other health condition-specific outcome measures
identified in this review have not had extensive
psychometric testing or they require sophisticated
equipment (for example the CATSYS)
12
which may
explain their limited use in clinical trials.
Most of the outcome measures assessing at the
body structure and function level were used to assess
cerebellar function and those at the activity level were
used for clinical intervention trials. However, some
measures, for example the SOT and the use of a force
plate and EMG have been utilized both in assessment
of cerebellar function and in clinical trials. Outcome
measures at body structure and function level are
used to objectively identify changes in sensory
interaction, motor behaviour, individual muscle
response, postural sway variables (amplitude, fre-
quency, and intersegment response), and biomecha-
nical causes for imbalance. However, to our
knowledge, in spite of their frequent use, their
psychometric properties, with the exception of the
SOT, have not been reported. These outcome
measures are frequently used in laboratory-based
studies but their sophistication and expense reduce
their clinical utility.
The clinic-based studies mostly used activity level
balance assessments, such as the BBS, the TUG, the
25-foot timed walk test, and the FR, all of which have
Winser et al. Balance and postural control outcome measures among cerebellar ataxia
130 Physical Therapy Reviews 2013 VOL.18 NO.2

moderately good psychometric properties and a high
degree of clinical utility. They are easy to administer,
require minimal time or special training to adminis-
ter, and do not require special equipment other than a
simple measuring scale, a stop watch, a chair, and
space to perform them in. However, it does not
appear that the outcome measures categorized under
the activity group have been tested for their psycho-
metric properties in people with pure cerebellar
lesions. Instead, they have been mostly tested with
multiple sclerosis and central vestibular dysfunctions,
conditions considered as having a mixed lesion
involving multiple regions of the brain including that
of the cerebellum. For the most part, these outcome
measures have been validated in people with stroke,
Parkinson’s disease, and older adults. Further
research is warranted to study the psychometric
properties of these scales for people with pure
cerebellar lesions. Some measurement tools, like
standing erect or walking,
75
self-reported falls,
59
timed unsupported stance,
65
and time to complete
balance tasks
69
assessing at the activity level identi-
fied in this review were not comprehensive in
assessing balance, in that the results obtained could
be inconsistent, not specific to balance and involved
self-reporting from the patient. These outcomes did
not have reported psychometric properties which
may reduce their utility for future research. Thus,
from a clinical utility perspective, we identified, time
required to perform the test, psychometric property
testing of the tool, and accessibility including cost,
ability to perform at bed side, and training required
to perform the test determines a measure’s utility.
No clinical outcome measure identified the locali-
zation of the cerebellar lesion. Pattern of sway could
be considered to differentiate localization of lesion;
however, this may require laboratory-based equip-
ment. Mauritz demonstrated that studying the
pattern of postural sway and sway amplitude using
a platform was able to distinguish lesions of different
functional zones of cerebellum.
31
Mauritz’s findings
suggested that people with spinocerebellar lesion may
have postural tremor in an antero-posterior direction
with a specific frequency of 3 Hz, lesions of
cerebrocerebellum show limited postural instability
without directional preference, and lesions of the
vestibulocerebellum may be exhibited as severely
affected multi-directional postural sways. The ampli-
tude of postural sway along different directions in
relation to the line of gravity ranged between 4 and
12 mm. However, assessment using a force platform
requires a sophisticated lab compromising its feasi-
bility in clinical practice. However, designing a
clinical assessment tool that is cerebellar site-specific
looks impractical, as it may be hard for clinical tools
to pick up subtle differences (ranging in a few
millimetres) using a force platform. At this stage, it
is accepted that identifying functional zones of
cerebellum would be a role of sophisticated diagnos-
tic imaging techniques.
This review was limited in that the search and
selection of articles were performed by one examiner.
However, the analysis and results interpretation
involved all authors. To the knowledge of the
authors, this is the first review of outcome measures
to assess balance and postural control among people
with cerebellar ataxia.
Conclusion
This narrative review identified 45 clinical and
laboratory-based outcome measures that have been
used to assess balance and postural control deficits
due to cerebellar dysfunction; only one study, using a
force plate, an outcome measure assessing at the body
structure and function level reported being able to
localize the cerebellar lesion. None of the clinic-based
tools were specific to the localization of the cerebellar
lesion. The health condition-specific and body
structure and function level outcome measures were
commonly used for cerebellar assessments. Outcome
measures at activity level were used to evaluate
cerebellar treatment effects. The ICARC or BARS
may be recommended as a health condition-specific
measure that is used to grade the severity of ataxia. A
force platform may be used to localize the lesion site
of ataxia with direction of postural sway being the
most important factor. Common activity-based
measures, although used frequently to evaluate
treatment effects and which are quick and easy to
perform (the TUG, BBS, FR, and 25-foot timed walk
test) do not appear to have had psychometric
property testing in a cerebellar population.
The findings of this review highlight the need for
testing the psychometric properties of balance and
postural control assessment tools and arriving at a
consensus on choosing an outcome measure for the
assessment of balance and postural control among
people with cerebellar ataxia.
Clinical implication
Currently there are a wide range of outcome
measures available for the assessment of balance
and postural control due to cerebellar deficits.
Careful consideration of factors such as psychometric
properties, time taken, accessibility, and specific
domain to be tested on balance needs to be
determined before making a decision on choosing
these outcome measures. It appears that the ICARS
and BARS may be considered as ataxia grading
scales. However, assessment of balance and postural
control using these ataxia grading scales and the
other identified outcome measures assessing at
Winser et al. Balance and postural control outcome measures among cerebellar ataxia
Physical Therapy Reviews 2013 VOL.18 NO.2 131

function level need further psychometric property
testing among people with cerebellar ataxia.
References
1 Pollock AS, Durward BR, Rowe PJ, Paul JP. What is balance?
Clin Rehabil. 2000;14(4):402–6.
2 Morton SM, Bastian AJ. Cerebellar control of balance and
locomotion. Neuroscientist (Baltimore, Md). 2004;10(3):247–
59.
3 Klockgether T. Sporadic ataxia with adult onset: classification
and diagnostic criteria. Lancet Neurol. 2010;9(1):94.
4 Manto M-U. The wide spectrum of spinocerebellar ataxias
(SCAs). Cerebellum (London, England). 2005;4(1):2–6.
5 Mariotti C, Fancellu R. An overview of the patient with ataxia.
J Neurol. 2005;252(5):511–8.
6 Massion J. Postural control system. Curr Opin Neurobiol.
1994;4(6):877.
7 Diener HC, Dichgans J, Guschlbauer B, Bacher M, Rapp H,
Klockgether T. The coordination of posture and voluntary
movement in patients with cerebellar dysfunction. Mov Disord.
1992;7(1):14–22.
8 Thach TW, Bastian AJ. Brain mechanisms for the integration
of posture and movement role of the cerebellum in the control
and adaptation of gait in health and disease. Prog Brain Res.
2004;143:353–66.
9 van de Warrenburg BP, Steijns JA, Munneke M, Kremer BP,
Bloem BR. Falls in degenerative cerebellar ataxias. Mov
Disord. 2005;20(4):497–500.
10 Organization WH, editor. International classification of func-
tioning, disability and health. Geneva: World Health
Organization; 2001.
11 Cano SJ, Hobart JC, Hart PE, Korlipara LV, Schapira AH,
Cooper JM. International cooperative ataxia rating scale
(ICARS): appropriate for studies of Friedreich’s ataxia? Mov
Disord. 2005;20(12):1585–91.
12 Lamoureux D, Beuter A. Standardization of a neuromotor test
battery: the CATSYS system. Neurotoxicology (Park Forest
South). 2000;21(5):725–35.
13 Saute JA, Donis KC, Serrano-Munuera C, Genis D, Ramirez
LT, Mazzetti P, et al. Ataxia rating scales-psychometric
profiles, natural history and their application in clinical trials.
Cerebellum. 2012;11(2):488–504.
14 Assadi M, Leone P, Veloski JJ, Schwartzman RJ, Janson CG,
Campellone JV. Validating an ataxia functional composite scale
in spinocerebellar ataxia. J Neurol Sci. 2008;268(1–2):136.
15 Schmahmann JD, Gardner R, MacMore J, Vangel MG.
Development of a brief ataxia rating scale (BARS) based on a
modified form of the ICARS. Mov Disord. 2009;24(12):1820–8.
16 Schmitz-Hu¨bsch T, du Montcel ST, Baliko L, Berciano J,
Boesch S, Depondt C, et al. Scale for the assessment and rating
of ataxia: development of a new clinical scale. Neurology.
2006;66(11):1717–20.
17 Ilg W, Synofzik M, Brotz D, Burkard S, Giese MA, Schols L.
Intensive coordinative training improves motor performance in
degenerative cerebellar disease. Neurology. 2009;73(22):1823–
30.
18 Delatycki MB. Evaluating the progression of Friedreich ataxia
and its treatment. J Neurol. 2009;256(s1):36–41.
19 Sullivan EV, Deshmukh A, Desmond JE, Lim KO,
Pfefferbaum A. Cerebellar volume decline in normal aging,
alcoholism, and Korsakoff’s syndrome: relation to ataxia.
Neuropsychology. 2000;14(3):341–52.
20 Trouillas P, Takayanagi T, Hallett M, Currier RD, Subramony
SH, Wessel K, et al. International cooperative ataxia rating
scale for pharmacological assessment of the cerebellar syn-
drome. J Neurol Sci. 1997;145(2):205.
21 Morton SM, Tseng YW, Zackowski KM, Bastian AJ.
Longitudinal tracking of gait and balance impairments in
cerebellar disease. Mov Disord. 2010;25(12):1944–52.
22 Schmitz-Hu
¨bsch T, Tezenas du Montcel S, Baliko L, Boesch S,
Bonato S, Fancellu R, et al. Reliability and validity of the
international cooperative ataxia rating scale: a study in 156
spinocerebellar ataxia patients. Mov Disord. 2006;21(5):699–
704.
23 Ford-Smith CD, Wyman JF, Elswick RK Jr, Fernandez T,
Newton RA. Test-retest reliability of the sensory organization
test in noninstitutionalized older adults. Arch Phys Med
Rehabil. 1995;76(1):77.
24 Cohen H, Blatchly CA, Gombash LL. A study of the clinical
test of sensory interaction and balance. Phys Ther.
1993;73(6):346.
25 Horak FB, Wrisley DM, Frank J. The balance evaluation
systems test (BESTest) to differentiate balance deficits. Phys
Ther. 2009;89(5):484–98.
26 McGregor L, Hale LA. Management of balance impairment,
guided by the balance evaluation-systems test, in a patient
following cerebellar infarct: a case report. NZ J Physiother.
2008;36(2):88.
27 Sullivan EV. Effect of vision, touch and stance on cerebellar
vermian-related sway and tremor: a quantitative physiological
and MRI study. Cerebral Cortex (New York, NY 1991).
2005;16(8):1077–86.
28 Baloh RW, Jacobson KM, Beykirch K, Honrubia V. Static and
dynamic posturography in patients with vestibular and
cerebellar lesions. Arch Neurol (Chicago). 1998;55(5):649–54.
29 Sriranjini SJ, Pal PK, Devidas KV, Ganpathy S. Improvement
of balance in progressive degenerative cerebellar ataxias after
therapy: a preliminary report. Neurol India. 2009;57(2):166.
30 Morgan MH. Ataxia — its causes, measurement, and manage-
ment. Int Rehabil Med. 1980;2(3):126–32.
31 Mauritz KH, Dichgans J, Hufschmidt A. Quantitative analysis
of stance in late cortical cerebellar atrophy of the anterior lobe
and other forms of cerebellar ataxia. Brain. 1979;102(3):461–82.
32 Morton SM, Bastian AJ. AJ. Relative contributions of balance
and voluntary leg-coordination deficits to cerebellar gait ataxia.
J Neurophysiol. 2002;89(4):1844–56.
33 Ioffe ME, Ustinova KI, Chernikova LA, Kulikov MA.
Supervised learning of postural tasks in patients with post-
stroke hemiparesis, Parkinson’s disease or cerebellar ataxia.
Exp Brain Res. 2006;168(3):384–94.
34 Horak FB, Diener HC. Cerebellar control of postural scaling
and central set in stance. J Neurophysiol. 1994;72(2):479.
35 Timmann D, Horak FB. Perturbed step initiation in cerebellar
subjects 1. Modifications of postural responses. Exp Brain Res.
1998;119(1):73–84.
36 Mummel P, Timmann D, Krause UW, Boering D, Thilmann
AF, Diener HC, et al. Postural responses to changing task
conditions in patients with cerebellar lesions. J Neurol
Neurosurg Psychiatry. 1998;65(5):734–42.
37 Bloem BR, Hegeman J, Bakker M, Oude Nijhuis LB, Van Meel
M, Allum JHJ. The influence of knee rigidity on balance
corrections: a comparison with responses of cerebellar ataxia
patients. Exp Brain Res. 2008;187(2):181–91.
38 Diener HC, Dichgans J, Bacher M, Gompf B. Quantification of
postural sway in normals and patients with cerebellar diseases.
Electroencephalogr Clin Neurophysiol. 1984;57(2):134.
39 Schwabe A, Drepper J, Maschke M, Diener HC, Timmann D.
The role of the human cerebellum in short-and long-term
habituation of postural responses. Gait Posture. 2004;19(1):16.
40 Riach CL, Hayes KC, Lucy SD. Changes in centre of pressure
of ground reaction forces prior to rapid arm movement in
normal subjects and patients with cerebellar ataxia. Clin
Biomech (Bristol). 1992;7(4):208–14.
41 Tokuda T, Tako K, Hayashi R, Yanagisawa N. Disturbed
modulation of the stretch reflex gain during standing in
cerebellar ataxia. Electroencephalogr Clin Neurophysiol.
1991;81(6):421.
42 Gatev P, Thomas S, Lou JS, Lim M, Hallett M. Effects of
diminished and conflicting sensory information on balance in
patients with cerebellar deficits. Mov Disord. 1996;11(6):654–
64.
43 Asaka T, Wang Y. Feedforward postural muscle modes and
multi-mode coordination in mild cerebellar ataxia. Exp Brain
Res. 2011;210(1):153–63.
44 Ku¨ng UM, Horlings CG, Honegger F, Kremer HP, Bloem BR,
van De Warrenburg BP. Postural instability in cerebellar
ataxia: correlations of knee, arm and trunk movements to
center of mass velocity. Neuroscience. 2009;159(1):390.
45 Liao K, Walker MF, Joshi AC, Reschke M, Strupp M, Wagner
J, et al. The linear vestibulo-ocular reflex, locomotion and falls
in neurological disorders. Restor Neurol Neurosci. 2010;28(1):
91.
46 Silkwood-Sherer D, Warmbier H. Effects of hippotherapy on
postural stability, in persons with multiple sclerosis: a pilot
study. J Neurol Phys Ther. 2007;31(2):77.
47 Gibson-Horn CC. Balance-based torso-weighting in a patient
with ataxia and multiple sclerosis: a case report. J Neurol Phys
Ther. 2008;32(3):139.
10*
13*
21*
30*
31*
Winser et al. Balance and postural control outcome measures among cerebellar ataxia
132 Physical Therapy Reviews 2013 VOL.18 NO.2

48 Schuhfried O, Mittermaier C, Jovanovic T, Pieber K,
Paternostro-Sluga T. Effects of whole-body vibration in
patients with multiple sclerosis: a pilot study. Clin Rehabil.
2005;19(8):834–42.
49 Landers M, Adams M, Acosta K, Fox A. Challenge-oriented
gait and balance training in sporadic olivopontocerebellar
atrophy: a case study. J Neurol Phys Ther. 2009;33(3):160.
50 Fjeldstad C, Pardo G, Frederiksen C, Bemben D, Bemben M.
Assessment of postural balance in multiple sclerosis. Int J MS
Care. 2009;11:1–5.
51 Jackson K, Mulcare JA, Donahoe-Fillmore B, Fritz HI,
Rodgers MM. Home balance training intervention for people
with multiple sclerosis. Int J MS Care. 2007(9):7.
52 Dordel HJ. Intensive mobility training as a means of late
rehabilitation after brain injury. Adapt Phys Act Q.
1989;6(2):176–87.
53 Bakker M, Allum JH, Visser JE, Gru¨neberg C, van de
Warrenburg BP, Kremer BH, et al. Postural responses to
multidirectional stance perturbations in cerebellar ataxia. Exp
Neurol. 2006;202(1):21.
54 Hudson CC, Krebs DE. Frontal plane dynamic stability and
coordination in subjects with cerebellar degeneration. Exp
Brain Res. 2000;132(1):103–13.
55 Sanes JN, LeWitt PA, Mauritz KH. Visual and mechanical
control of postural and kinetic tremor in cerebellar system
disorders. J Neurol Neurosurg Psychiatry. 1988;51(7):934–
43.
56 Betker AL, Szturm T, Moussavi ZK, Nett C. Video game-based
exercises for balance rehabilitation: a single-subject design.
Arch Phys Med Rehabil. 2006;87(8):1141.
57 Van de Warrenburg BPC, Bakker M, Kremer BPH, Bloem BR,
Allum JHJ. Trunk sway in patients with spinocerebellar ataxia.
Mov Disord. 2005;20(8):1006–13.
58 Ienaga Y, Mitoma H, Kubota K, Morita S, Mizusawa H.
Dynamic imbalance in gait ataxia. Characteristics of plantar
pressure measurements. J Neurol Sci. 2006;246(1–2):53.
59 Harris-Love MO, Siegel KL, Paul SM, Benson K.
Rehabilitation management of Friedreich ataxia: lower extre-
mity force-control variability and gait performance.
Neurorehabil Neural Repair. 2004;18(2):117–24.
60 Nicholson JH, Morton RE, Attfield S, Rennie D. Assessment of
upper-limb function and movement in children with cerebral palsy
wearing lycra garments. Dev Med Child Neurol. 2001;43(6):384–91.
61 Jones L, Lewis Y, Harrison J, Wiles CM. The effectiveness of
occupational therapy and physiotherapy in multiple sclerosis
patients with ataxia of the upper limb and trunk. Clin Rehabil.
1996;10(4):277–82.
62 Smedal T, Lygren H, Myhr KM, Moe-Nilssen R, Gjelsvik B,
Gjelsvik O, et al. Balance and gait improved in patients with
MS after physiotherapy based on the Bobath concept.
Physiother Res Int. 2006;11(2):104–16.
63 Hammer A, Nilsaga˚ rd Y, Forsberg A, Pepa H, Skargren E,
Oberg B. Evaluation of therapeutic riding (Sweden)/hippother-
apy (United States). A single-subject experimental design study
replicated in eleven patients with multiple sclerosis. Physiother
Theory Pract. 2005;21(1):51–77.
64 Cattaneo D, Regola A, Meotti M. Validity of six balance
disorders scales in persons with multiple sclerosis. Disabil
Rehabil. 2006;28(12):789–95.
65 Freund JE, Stetts DM. Use of trunk stabilization and
locomotor training in an adult with cerebellar ataxia: a single
system design. Physiother Theory Pract. 2010;26(7):447–58.
66 Cattaneo D, Jonsdottir J, Zocchi M, Regola A. Effects of
balance exercises on people with multiple sclerosis: a pilot
study. Clin Rehabil. 2007;21(9):771–81.
67 Cattaneo D, Jonsdottir J, Repetti S. Reliability of four scales on
balance disorders in persons with multiple sclerosis. Disabil
Rehabil. 2007;29(24):1920–5.
68 Brown KE, Whitney SL, Marchetti GF, Wrisley DM, Furman
JM. Physical therapy for central vestibular dysfunction. Arch
Phys Med Rehabil. 2006;87(1):76.
69 Vaz DV, Schettino Rde C, Rolla de Castro TR, Teixeira VR,
Cavalcanti Furtado SR, de Mello Figueiredo E. Treadmill
training for ataxic patients: a single-subject experimental
design. Clin Rehabil. 2007;22(3):234–41.
70 Brown TH, Mount J, Rouland BL, Kautz KA, Barnes RM,
Kim J. Body weight-supported treadmill training versus
conventional gait training for people with chronic traumatic
brain injury. J Head Trauma Rehabil. 2005;20(5):402.
71 Widener GL, Allen DD, Gibson-Horn C. Balance-based torso-
weighting may enhance balance in persons with multiple
sclerosis: preliminary evidence. Arch Phys Med Rehabil.
2009;90(4):602.
72 Neuls PD, Clark TL, Van Heuklon NC, Proctor JE, Kilker BJ,
Bieber ME, et al. Usefulness of the berg balance scale to predict
falls in the elderly. J Geriatr Phys Ther. 2011;34(1):3.
73 Shumway-Cook A, Brauer S, Woollacott M. Predicting the
probability for falls in community-dwelling older adults using
the timed up & go test. Phys Ther. 2000;80(9):896.
74 Frzovic D, Morris ME, Vowels L. Clinical tests of standing
balance: Performance of persons with multiple sclerosis. Arch
Phys Med Rehabil. 2000;81(2):215–21.
75 Vinci P. Gait rehabilitation in a patient affected with Charcot-
Marie-Tooth disease associated with pyramidal and cerebellar
features and blindness. Arch Phys Med Rehabil.
2003;84(5):762–5.
76 Perlmutter E, Gregory PC. Rehabilitation treatment options
for a patient with paraneoplastic cerebellar degeneration. Am J
Phys Med Rehabil. 2003;82(2):158.
77 Karakaya M, Ko¨se N, Otman S, Ozgen T. Investigation and
comparison of the effects of rehabilitation on balance and
coordination problems in patients with posterior fossa and
cerebellopontine angle tumours. J Neurosurg Sci. 2000;44(4):
220–5.
78 Armutlu K, Karabudak R, Nurlu G. Physiotherapy approaches
in the treatment of ataxic multiple sclerosis: a pilot study.
Neurorehabil Neural Repair. 2001;15(3):203–11.
79 Stojakovich M, Stevens JA. Beneficial effects of postural
intervention on prehensile action for an individual with ataxia
resulting from brainstem stroke. NeuroRehabilitation
(Reading, Mass). 2005;20(2):85.
80 Ilg W, Golla H, Thier P, Giese MA. Specific influences of
cerebellar dysfunctions on gait. Brain. 2007;130(3):786–98.
81 Herndon RM. Scales for assessment of ataxia. In: Herndon
RM, editor. Handbook of neuroloic rating scales: library of
congress cataloging in publication data. New York: Demos
Medical; 2006. p. 347–61.
64*
66*
67*
68*
78*
Winser et al. Balance and postural control outcome measures among cerebellar ataxia
Physical Therapy Reviews 2013 VOL.18 NO.2 133