Balance in Relation to Walking Deterioration in

Adults With Spastic Bilateral Cerebral Palsy

Arve Opheim, Reidun Jahnsen, Elisabeth Olsson and
Johan Kvalvik Stanghelle
PHYS THER. 2012; 92:279-288.
Originally published online October 27, 2011
doi: 10.2522/ptj.20100432

The online version of this article, along with updated information and services, can be
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Research Report

Balance in Relation to Walking

Deterioration in Adults With Spastic
Bilateral Cerebral Palsy
Arve Opheim, Reidun Jahnsen, Elisabeth Olsson, Johan Kvalvik Stanghelle

Background. Balance function is central in walking, and impaired balance function may be related to walking deterioration in adults with spastic bilateral cerebral
palsy (CP).

Objectives. The purposes of this study were: (1) to compare balance confidence,
fear of falling, and balance ability in adults with spastic bilateral CP, with and without
self-reported walking deterioration; (2) to characterize balance confidence, fear of
falling, and balance ability across all participants; and (3) to examine the relationship
between balance confidence and balance ability across all participants.

Design. A case-control design was used.

Methods. Sixteen adults from a 7-year follow-up study who had spastic bilateral
CP and were under 40 years of age in the 2006 survey participated. Eight participants
reported walking deterioration (cases), and 8 participants did not report walking
deterioration (controls). Outcome variables were: the Activities-specific Balance
Confidence (ABC) Scale, the Falls Efficacy ScaleInternational (FES-I), and the Balance
Evaluation Systems Test (BESTest).

Results. No differences in any of the outcome variables were found between the
cases and the controls. Across all participants, the ABC Scale and FES-I scores were
62% and 24 points, respectively. Reduced ABC Scale scores and increased FES-I scores
were found when using escalators, walking in crowds, and walking on slippery
surfaces. The BESTest subscale scores were 60% to 79% of the maximum score, but
only 31% and 42% of the maximum score in postural responses and anticipatory
adjustments, respectively. Balance confidence correlated positively with postural
responses, sensory orientation, stability in gait, and BESTest total score.

A. Opheim, PT, MSc, Karolinska

Institutet, Stockholm, Sweden,
and Sunnaas Rehabilitation Hospital, 1450 Nesoddtangen, Norway. Address all correspondence
to Mr Opheim at: arvei.opheim@
sunnaas.no.
R. Jahnsen, PT, PhD, Sunnaas
Rehabilitation
Hospital,
and
Department of Clinical Neurosciences in Children, Oslo University Hospital, Rikshospitalet, Oslo,
Norway.
E. Olsson, PT, PhD, Karolinska
Institutet.
J.K. Stanghelle, PhD, MD, Sunnaas
Rehabilitation Hospital, and Faculty of Medicine, University of
Oslo, Oslo, Norway.
[Opheim A, Jahnsen R, Olsson E,
Stanghelle JK. Balance in relation
to walking deterioration in adults
with spastic bilateral cerebral palsy.
Phys Ther. 2012;92:279 288.]
2012 American Physical Therapy
Association
Published Ahead of Print:
October 27, 2011
Accepted: September 5, 2011
Submitted: December 22, 2010

Limitations. The lack of reliability and validity tests for the outcome variables in
this study population and the small number of participants were limitations of the
study.

Conclusions. Self-reported walking deterioration in this group could not be

explained by differences in balance confidence, fear of falling, or balance ability.
Across all participants, most balance problems seemed related to reduced postural
responses and anticipatory adjustments.
Post a Rapid Response to
this article at:
ptjournal.apta.org
February 2012

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Balance in Adults With Spastic Bilateral Cerebral Palsy

igh levels of fatigue, pain, and

deterioration of walking have
been reported in adults with
cerebral palsy (CP).17 In our 7-year
follow-up study of people with spastic unilateral and bilateral CP in
2006,7 a substantial increase in the
proportion of people reporting walking deterioration was seen in the
ages of 35 to 40 years in people with
spastic bilateral CP. Those reporting
walking deterioration also reported
significantly higher levels of both
musculoskeletal pain and physical
fatigue. Seventy-eight of the 149 people with spastic CP reported deterioration in walking in adult age, and
51 of the 78 reported that this deterioration was characterized by
reduced balance.7 These findings led
us to focus on balance as an important factor for early walking deterioration in people with spastic CP.
Postural stability, also referred to as
balance, is the ability to control the
center of mass in relationship to the
base of support.8 In order to maintain balance during a certain task,
complex processes take place
involving vestibular, somatosensory,
visual, cognitive, and musculoskeletal systems, controlling the relationships among the different body segments and between the body and the
environment.9,10 Balance has been
described as one of the prerequisites
for walking11 and was found to be
impaired in children with CP.12,13
Burtner et al14 found that children
with spastic bilateral CP had a
proximal-to-distal muscle activation
pattern, more co-contraction, and
slower muscle activation compared
with children with typical development. To the best of our knowledge,
studies of balance in adults with CP
have not been carried out.
In order to gather more information
about balance in adults with spastic
bilateral CP, we invited 3 adults to
share their experiences in a group
discussion. They revealed that walk280

Physical Therapy

ing on uneven or slippery ground,

walking in crowds, using escalators
and public transportation, and walking down stairs were difficult situations that challenged their balance
reactions. They often felt too slow
and unable to prevent a fall.
Impaired vision and reduced lighting
conditions presented additional
problems. These difficulties often
led to compensatory strategies such
as holding on to railings or other
objects. Some participants in the
group discussion regarded themselves as expert fallers (ie, they
often fell but had not had serious
injuries and were not afraid of falling). Others reported that they were
afraid of falling.
These described difficulties may lead
to an increased risk of falling, injuries, and a gradual reduction in walking frequency and distance, thus
contributing to walking deterioration. This deterioration might reduce
activity participation in the community at a far earlier age than would be
expected due to normal aging. However, studies of balance ability and its
relationship to walking deterioration
in adults with spastic bilateral CP are
lacking.
Our previous 7-year follow-up study7
indicated an association between
impaired balance and walking deterioration, as 51 of 78 people
regarded the deterioration as a result
of reduced balance. Of those with
unchanged or improved walking
(n71), 26 regarded their walking
ability to be a result of improved
balance.7 Walking deterioration was
more common in individuals with
spastic bilateral CP.7 Given these
results, the lack of research in the
area, and the information from the
group discussion, the first purpose
of this study was to compare balance
confidence, fear of falling, and balance ability in adults with spastic
bilateral CP, with and without selfreported walking deterioration. The

second purpose was to describe balance confidence, fear of falling, and

balance ability across all participants.
The third purpose was to examine
the relationship between balance
confidence and balance ability across
all participants.

Method
Design
A case-control design was chosen to
compare people who reported walking deterioration (cases) with people
who did not (controls).
Setting
The testing took place during the
fall of 2009 in the Motion Analysis
Laboratory at Sunnaas Rehabilitation
Hospital, Norway, and was conducted by trained and experienced
multidisciplinary personnel.
Participants
The participants were recruited
from a 7-year follow-up study of 149
adults with spastic unilateral and
bilateral CP in 2006.7 In a mailed
letter, we invited all people with
spastic bilateral CP who reported
Gross Motor Function Classification
System (GMFCS) levels I through
III15 and were under 40 years of age
in the 2006 survey to participate.
Individuals who were unable to walk
at least 10 m without walking aids
were excluded. A flow chart of the
inclusion process is presented in Figure 1. Sixteen adults (5 men, 11
women) with documented spastic
bilateral CP, GMFCS levels II (n15)
and III (n1), agreed to participate
(Tab. 1).
Procedure
The Activities-specific Balance Confidence (ABC) Scale was administered
in a telephone interview by a physical therapist 2 to 3 weeks before the
semistructured interview and the
tests of balance ability in the laboratory. This physical therapist did not
take part in the other assessments. In
the semistructured interview, carried

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Balance in Adults With Spastic Bilateral Cerebral Palsy

out by the principal investigator
(A.O.), the changes in walking
function over the years (since the
end of adolescence) were reassessed and categorized as improved,
unchanged, or deteriorated. Each
participants Falls Efficacy Scale
International (FES-I) and Functional
Mobility Scale (FMS) scores, GMFCS
level, and history of falls also were
obtained during this interview. All
assessments were carried out in the
same order: first the semistructured
interview, then tests of muscle tone
and muscle strength, followed by the
tests of balance ability. The principal
investigator led and administered all
balance tests, assisted by at least one
other person (physical therapist or
biomechanist) who observed and
registered the performance of the
tests of balance ability and aided in
participants safety. The principal
investigator was blinded to the ABC
Scale scores until after the tests of
balance ability. When there were
doubts about the scorings on the
tests of balance ability, these doubts
were discussed, and the principal
investigator had the final word.
Descriptive Variables
The GMFCS15 was used to assess
gross motor function. The GMFCS
categorizes gross motor function
into 5 levels, with level I being the
highest and level V being the lowest
functional level. The need for railings when descending stairs was
used to distinguish between levels I
and II. The GMFCS has been found to
be valid and reliable in adults with
CP.16,17
The FMS18 was used to describe the
level of independent walking on a
scale of 1 to 6 points (1wheelchair
user, 6fully independent on all surfaces) over 5, 50, and 500 m, respectively. The FMS has been found to be
both reliable and valid in children
with CP.18

February 2012

Figure 1.
Flow chart of the inclusion of participants for the present study. CPcerebral palsy,
GMFCSGross Motor Function Classification Scale.

Muscle tone in the triceps surae, rectus femoris, hamstring, and adductor
muscle groups was assessed bilaterally using the 6-level modified Ashworth scale (MAS) (0 5),19 which
assesses resistance to rapid, passive
movements. Higher scores indicate
higher muscle tone. The median
MAS score for these muscle groups
was calculated. Bohannon and
Smith19 found an agreement of 87%
between 2 raters who used the MAS
to assess muscle tone in the elbow
flexors, but the reliability of the MAS
was found to variable in later studies.20 The validity of the MAS in the
assessment of muscle spasticity has
been questioned,20,21 but it is still the
most common clinical scale for
assessing muscle tone by grading the
resistance to passive movements,22

acknowledging that this assessment

also includes mechanical compliance in muscle and joints.23
Muscle strength in the hip flexors,
extensors and abductors, knee flexors and extensors, and ankle plantar
flexors and dorsiflexors, bilaterally,
was assessed using the 0 5 grade
manual muscle test scale.24 Higher
scores indicate stronger muscles.
The median muscle strength score
for these muscles was calculated.
Manual muscle test scores have been
found to correlate (r.768, P.001)
with the results of dynamometer
testing.25
Outcome Variables
Balance confidence and fear of falling were assessed with the ABC

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Balance in Adults With Spastic Bilateral Cerebral Palsy

Table 1.
Characteristics of the Participants in the Study (N16)a
Variable

All

Cases (n8)

Controls (n8)

Female/male, n

11/5

5/3

6/2

Age (y), median (Q1Q3)

38 (3140)

39 (3142)

36 (3139)

Body mass index (kg/m2), median

(Q1Q3)

24.7 (23.131.4)

25.0 (23.537)

24.7 (22.727.1)

GMFCS level II/III, n

15/1

8/0

7/1

MAS,b median (Q1Q3)

2.0 (1.62.5)

2.0 (2.02.4)

2.0 (1.12.9)

Muscle strength,c median (Q1Q3)

4.0 (3.64.0)

4.0 (3.14.0)

4.0 (4.04.0)

12

38

20

Falls in the previous month, n

Falls in the previous year, n

5
510

1125

2650

51

Q1Q3first through third quartiles, GMFCSGross Motor Function Classification Scale.

Modified Ashworth scale (MAS) (0 5), median score of triceps surae, rectus femoris, hamstring, and hip adductor muscles. Higher scores indicate higher
muscle tone and greater resistance to rapid, passive movements. The original MAS scores were coded as: 00, 11, 12, 23, 34, and 45.
c
Manual muscle test (0 5), median score of hip flexors, extensors, and abductors, knee flexors and extensors, and ankle plantar flexors and dorsiflexors.
Higher scores indicate stronger muscles.
b

Scale and the Norwegian version of

the FES-I, respectively. Balance ability was tested with the Balance Evaluation Systems Test (BESTest) and
the Four-Square Step Test (FSST).
These scales and balance ability tests
were chosen because they cover several of the balance problems mentioned in the group discussion, such
as fear of falling, maintaining balance
while performing different activities,
balance reactions, and stepping over
obstacles.
The ABC Scale (with scores
expressed as a percentage) was used
to quantify, from 0 to 100 (0not at
all), the confidence a person had in
not losing balance while performing
16 activities in daily living.26 The
scale has been used extensively in
both balance and fall prevention
research in the elderly population
282

Physical Therapy

and has good psychometric properties.27 It was found to be valid and

reliable in people who were healthy
and frail elderly people, in people
with a history of falls, and in patients
with Parkinson disease.26,28,29
The Norwegian version of the FES-I
was used to grade fear of falling during different activities in daily living
on a 4-point scale (1not at all concerned, 4very concerned), giving a
total scoring range of 16 to 64
points.30 32 It is widely used internationally in the field of fall prevention
and has been found to be reliable
and valid for community-dwelling
elderly people and elderly patients
who were treated for fall-related
fractures.33,34
The BESTest was used to assess different subsystems related to bal-

ance.35 It contains 6 subscales covering these different subsystems: I

biomechanical constraints, IIstability limits/verticality, IIIanticipatory postural adjustments, IV
postural responses, Vsensory orientation, and VIstability in gait.
The BESTest consists of 27 items,
some of which are divided into 2 to
4 sub-items (eg, for left and right
sides), resulting in a total of 36 tasks.
All items are scored on a 4-category
ordinal scale from 0 (not able or
absent) to 3 (normal), and the scores
are summed for each subscale. The
sum of the 6 subscale scores is the
BESTest total score. The BESTest subscale and total scores are reported as
a percentage of the maximum score.
The FSST (in seconds) was used to
test the participants ability to step
over a low obstacle in all 4 directions

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Balance in Adults With Spastic Bilateral Cerebral Palsy

in a given sequence as fast as possible.36 The FSST was found to have
good test-retest reliability, it correlated well with other gait measures,37 and it was feasible and valid
for testing dynamic balance in
patients who were ambulatory after
stroke.38
Bias
Bias was controlled for by having the
principal investigator (A.O.) administer the FES-I and FMS, assess GMFCS
level, and lead all tests of balance
ability. At least 2 people were always
present during all balance tests. The
principal investigator was blinded to
the scores on the ABC Scale during
the tests of balance ability. He was
not blinded to whether the participants had reported deteriorated
walking. All participants gave written informed consent.
Data Analysis
We used SPSS version 15.0 statistical
software (SPSS Inc, Chicago, Illinois)
to analyze the data. Because of the
small number of participants and the
explorative nature of the study, nonparametric statistics were used
throughout the study. Descriptive
variables are presented with frequencies for history of falls and GMFCS
levels and with medians and interquartile ranges (Q1Q3) for muscle
strength and MAS. All outcome variables (ABC Scale, FES-I, BESTest, and
FSST) are presented with medians
and interquartile ranges (Q1Q3).39
For the case-control study, the
between-group differences in ABC
Scale, FES-I, BESTest (subscale and
total), and FSST scores were tested
with the Mann-Whitney U test.39 The
relationship between balance confidence and the BESTest subscale
scores, BESTest total scores, and
FSST scores was tested with scatter
plots and Spearman rho (rs) correlation coefficient. The 95% confidence
interval (CI) for the correlation coefficient was calculated with VassarStats.40 The correlation coeffiFebruary 2012

cient was interpreted according to

Domholt41: 1.00 0.90very high;
0.89 0.70high; 0.69 0.50moderate; 0.49 0.26low; and 0.25
0.00little, if any correlation.

Results
The descriptive variables of the participants are presented in Table 1.
Eight participants reported deteriorated walking over the years (cases),
and 8 participants reported either
improved (n2) or unchanged (n
6) walking (controls) (Tab. 1). The
FMS showed that 15 participants
were independent walkers on even
surfaces over 50 m, and 12 participants were independent walkers
over 500 m (data not shown). There
were frequent falls among the participants, but no serious injuries
were reported. There were no significant differences between the cases
and the controls for the descriptive
variables (Tab. 1). There were no
differences in ABC Scale and FES-I
scores between the participants who
reported deteriorated walking and
those who did not, nor were there
any differences in BESTest subscale
scores, BESTest total scores, or FSST
scores (Tab. 2).

The BESTest showed the lowest

scores (percentage of the maximum
score) for anticipatory postural
adjustments (subscale III), with a
median score of 42 (Q1Q339
54), and for postural responses (subscale IV), with as median score of
31 (Q1Q318 58). The median
scores for the other subscales ranged
from 60% to 79% of the maximum
score (Tab. 2). The BESTest total
score (percentage of the maximum
score) showed a median score of 60
(Q1Q355 68) (Tab. 2). The FSST
showed a skewed distribution, with
2 distinct outliers. The median time
to complete the stepping sequence
was 16 seconds (Q1Q31122)
(Tab. 2).
The relationship between balance
confidence and balance ability
showed a moderate positive correlation between the ABC Scale scores
and the BESTest subscale IV, V, and
VI scores and BESTest total scores
(Tab. 3). The tests of balance ability
were easily understood by the participants, there were no major practical
problems during the testing, and all
participants completed all tests.

Discussion
For the whole group, the scores on
the ABC Scale showed the lowest
confidence in balance during the
activities stepping on or off an escalator without holding the railings,
walking on an icy surface, and
stand on chair and reach (Fig. 2).
The overall ABC Scale score across
all activities was 62% (Q1Q337
70) confidence in not losing balance.
The FES-I showed the greatest fear of
falling during the activities walk on
a slippery surface and walk up or
down a slope, with median scores
of 3 (Q1Q32 4) and 2 (Q1
Q32 4), respectively. The median
FES-I summed score was 24 points
(Q1Q32134). For 12 of the 16
items, the participants reported no
or little fear of falling (Tab. 2).

There were no differences in balance

confidence, fear of falling, and balance ability in adults with spastic
bilateral CP, with and without selfreported walking deterioration. This
finding might reflect a more complex interaction between walking
deterioration and balance than originally hypothesized. The variability
in the outcome variables in both
groups was substantial. Different
social roles and exposure to different
contextual factors at work, in the
family, and during leisure time, as
well as personal factors, put different demands on both balance and
walking. A small change in balance
ability, therefore, might have a considerable impact on walking for
some people with high functional
demands and expectations, whereas

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Balance in Adults With Spastic Bilateral Cerebral Palsy

Table 2.
Comparison of Balance Confidence, Fear of Falling, and Clinical Balance Tests Between People Who Reported Deteriorated
Walking (n8) and Those Who Did Not (n8) in a Group of Adults With Spastic Bilateral Cerebral Palsy (N16)a
Measure
c

Deteriorated
Walking

Nondeteriorated
Walking

Pb

All

ABC Scale (%)

62 (3276)

58 (4670)

.713

62 (3770)

FES-Id (1664)

24 (2236)

26 (1934)

.804

24 (2134)

57 (4973)

60 (5567)

.798

60 (5372)

II

76 (7685)

84 (7186)

.645

79 (7286)

III

39 (3550)

44 (3960)

.328

42 (3954)

IV

28 (1863)

36 (1856)

.878

31 (1858)

64 (4578)

67 (5073)

.959

67 (5073)

BESTeste (%)

VI

67 (6071)

69 (6776)

.505

67 (6775)

Total

58 (5368)

60 (5771)

.505

60 (5568)

FSSTf (s)

19 (1528)

12 (1020)

.130

16 (1122)

All scores presented as median and interquartile range (Q1Q3).

b
Nonparametric Mann-Whitney U test.
c
ABC ScaleActivities-specific Balance Confidence Scale (0%100%). Higher score indicates higher confidence of not losing balance across 16 different
activities.
d
FES-IFalls Efficacy ScaleInternational. Higher score indicates greater fear of falling during 16 different activities.
e
BESTestBalance Evaluation Systems Test (0%100% of maximum score). Higher score indicate better balance. BESTest subscales: Ibiomechanical
constraints, IIstability limits/verticality, IIIanticipatory postural adjustments, IVpostural responses, Vsensory orientation, VIstability in gait.
f
FSSTFour-Square Step Test.

for people with smaller demands

these changes might go unnoticed.
The groups had similar median levels
and range of both muscle strength
and muscle tone, and as 12 of the 16
participants were independent walkers over more than 500 m, the sample size was too small to detect a
possible between-group difference.
If there are changes in balance ability
over time in adults with spastic bilateral CP, they might be the result of
slow processes involving both neural
and musculoskeletal structures, such
as slower proprioception, signal processing and execution, contractures,
and reduced muscle strength. These
processes might take a long time to
develop before they result in
reduced balance and later affect
walking. Therefore, a prospective,
longitudinal study of both walking
and balance ability would have been
the preferred design. However, as
little is known about the optimal
follow-up time, the most relevant
outcome variables, or the balance in
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this group, we decided to use a

cross-sectional study design in this
study.
The BESTest showed reductions in
all subsystems of balance, with
anticipatory adjustments and postural responses being the most
affected. Difficulties with anticipatory postural adjustments points
toward reduced ability to anticipate the effect of movements on
balance. When anticipating a posteriorly directed push, the anterior
muscles must be activated and the
body center of mass directed forward. These mechanisms are result
of experience and motor learning,8,42 but are known to be slow and
delayed in children with CP.8
The difficulties related to postural
responses are in accordance with
Gage et al,11 who described the equilibrium problem as one of the primary abnormalities of gait in children with CP. Reduced postural
responses in children with CP com-

pared with children developing typically also were found by Burtner

et al.12 The ability to take a rapid step
to regain balance is a crucial postural
response to avoid falls and is probably a primary problem in adults with
CP as well. Lajoie and Gallagher28
found significantly higher reaction
times in fallers than in nonfallers
in a group of elderly people.
In people with spastic CP, both
anticipatory adjustments and postural responses can be affected by
the brain lesion itself. Increased
antagonistic coactivation,14 perhaps
as a strategy to cope with reduced
postural control,42 a top-down muscle activation,43 a reduced ability to
modulate electromyography amplitude,44 and muscle weakness and
joint impairments also are likely to
be contributing factors. For overall
balance, the BESTest total score was
60% of the maximum score, and the
BESTest subscale scores ranged from
31% to 79% of the maximum score.
These scores were considerably

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Figure 2.
Box plot of the scores on the different items of the Activities-specific Balance Confidence (ABC) Scale of 16 adults with spastic bilateral
cerebral palsy. A score of 100 represents 100% confidence in not losing balance during an activity, thus higher scores represent
higher balance confidence. The boxes represent 50% of the observations (Q1Q3), the black line shows the median score, and the
error bars show the minimum and maximum values. The outliers are those that lie between 1.5 and 3 box lengths from the lower
or upper edge of the box.

lower than those in the study by

Lord et al,45 who found BESTest
scores of 80% to 90% of the maximum in elderly people who were
healthy.
The overall balance confidence was
62%, which is the same level as in
elderly people with a history of hip
fracture46 and lower than in
community-dwelling elderly people.47 Lajoie and Gallagher28 found
that a cutoff ABC Scale score of 67%
could predict fallers in the elderly
population with a sensitivity of 84%
February 2012

and nonfallers with a specificity of

88%. The high number of fallers in
the present study suggests an even
higher cutoff point in this group.
There were substantial differences in
ABC Scale scores for the different
activities. The ABC Scale scores were
lowest when using escalators and
walking on icy surfaces. In 7 of the
16 activities, the median scores
showed more than 80% confidence
and, consequently, did not reflect
the balance problems of the study
group. Not surprisingly, fear of falling showed a trend similar to that of

balance confidence. Delbaere et al33

found cutoff points for low (16 19),
moderate (20 27) and high (28 64)
concern in community-dwelling
elderly people. Fear of falling in the
present study was moderate, and
slightly lower than in a group of people with spinal cord injury48 and in a
group of women with osteoporosis.49 It was at about the same level as
in the validation study by Delbaere et
al33 and as in elderly people who
were treated for fall-related fractures.34 There was a high prevalence
of fallers in the present group, but no

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Balance in Adults With Spastic Bilateral Cerebral Palsy

Table 3.
Correlations Between Balance Confidence and Balance Ability in Adults With Spastic
Bilateral Cerebral Palsy (N16)a
Activities-specific Balance
Confidence Scale

Measure
BESTestb
I

.45, P.084

II

.24, P.36

III

.29, P.27

IV

.52 (95% CI.04, .81), P.04

.52 (95% CI.04, .81), P.038

VI

.57 (95% CI.10, .83), P.022

Total

.57 (95% CI.10, .83), P.022

Four-Square Step Test

.346, P.189

Correlation coefficients with 95% confidence intervals (CI) were obtained using Spearman rho (rs);
the CIs are given where significant correlations were found, P.05.
b
BESTestBalance Evaluation Systems Test. BESTest subscales: Ibiomechanical constraints, IIstability
limits/verticality, IIIanticipatory postural adjustments, IVpostural responses, Vsensory orientation,
VIstability in gait.

reports on fractures due to falls,

which might partly correspond to
expert fallers (ie, those who fall
often, but without injuries and fear
of falling). However, the risk of an
injurious fall, reduced balance confidence, and fear of falling, especially
in outdoor and community activities,
might substantially restrict both
social and community participation
for these relatively young people.
Fatigue also is a factor that might
have an impact on both balance and
falls, but this relationship was not
assessed in this study.
The relationship between balance
confidence and balance ability
showed a moderate positive correlation for the BESTest subscales of postural responses, sensory orientation,
and stability in gait and for the BESTest total score. The correlation
between postural responses and balance confidence suggests that a
reduced ability to react to external
perturbations with a rapid step has a
negative impact on balance confidence. The proximal-to-distal activation pattern found in children with
CP43 indicates a reduced ability to
use an ankle strategy for regaining
balance. Thus, a reduced ankle strat286

Physical Therapy

egy in addition to the reduced postural responses, creates a double

problem, as both the most adequate
balance adjustment strategy and the
ability to take rapid steps to regain
balance are reduced. The reduced
postural responses may be confirmed by the low score of balance
confidence when using escalators
and walking on slippery surfaces.
Sensory orientation, as evaluated in
the test, can be the result not only of
impaired sensory systems such as
vision, the vestibular system, and
proprioception, but also of an
impaired motor output (ie, task
execution). Both sensation and proprioception often are affected in
CP.50 The group discussion highlighted balance problems during
dim light conditions, when compensatory mechanisms (eg, vision
for reduced proprioception) are
no longer available. Stability in gait,
as tested in the BESTest, includes
walking under different conditions
that challenge the balance. Impaired
balance during walking may reduce
the balance confidence and, therefore, could explain the correlation
between stability in gait and balance
confidence. A positive correlation
between balance confidence and bal-

ance ability was found by Horak et

al35 (r.64) and by Sihvonen et al46
(r.74), and confirmed by the present study.
The positive correlation between
balance confidence and the scores
on BESTest subscales IV, V, and VI
and the BESTest total score suggests
that the participants had a realistic
perception of their own balance.
The fact that there were no correlations between balance confidence
and scores on BESTest subscales I, II,
and III may be due to the mixture of
different body functions and structures in these subscales, as well as
the small number of participants.
The FSST had little, if any, correlation with balance confidence, as
also shown by Whitney et al37 in people with vestibular dysfunctions.
The FSST includes tasks with different levels of difficulty, a variation
that may have different effects on
balance confidence and result in
increased FSST time. For instance,
the reduced ability to step backward
may have a different effect on the
balance confidence than a reduced
ability to take a step forward or
sideways.
These results confirmed the balance
problems described in the group discussion and highlight the specific balance problems in this group. These
problems were at the same level as
in the elderly population treated for
fall-related fractures, and thus they
can be in need of targeted interventions. No major practical problems
were encountered during the testing,
indicating the practical feasibility of
these tests in this population.
Future research should focus on
long-term changes in balance in a
prospective, longitudinal design
among people who have spastic CP
and on the relationship between
changes in balance ability and walking. Furthermore, there is a need for

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February 2012

Balance in Adults With Spastic Bilateral Cerebral Palsy

studies on the reliability and validity
of these balance tests in this group.

Southeastern Norway (Ref. ID: 1.2006.952

and 2009/119) and the Commissioner for
the Protection of Privacy in Research.

Study Limitations
The reliability and validity of the outcome variables for use with this
group were not previously tested.
The number of participants in this
study was relatively small; therefore,
this study should be regarded as
exploratory, and the results of the
between-group comparisons should
not be generalized to a larger group.
However, the study group was not a
convenience sample, but a specific
subgroup of people recruited from
our previous follow-up study.

This research, in part, was presented at the

4th Journee Regionale du Reseau Breizh IMC;
Rennes, France; February 1, 2011.

Conclusion
Self-reported walking deterioration
in this group of adults with spastic
bilateral CP could not be explained
by differences in balance confidence, fear of falling, or balance ability in this exploratory study. Across
the whole group, most balance problems seemed related to reduced postural responses and anticipatory
adjustments. Fear of falling was at
the same level as in elderly people
with fall-related fractures. Those
individuals with higher balance confidence scored better on several of
the tests of balance ability.
Mr Opheim, Dr Jahnsen, and Dr Olsson
provided concept/idea/research design. All
authors provided writing. Mr Opheim provided data collection. Mr Opheim and Dr
Olsson provided data analysis. Mr Opheim
and Dr Stanghelle provided project management. Dr Stranghelle provided fund procurement and facilities/equipment. Dr Olsson
and Dr Stanghelle provided institutional
liaisons. Dr Jahnsen, Dr Olsson, and Dr
Stanghelle provided consultation (including
review of manuscript before submission).
The authors thank all of the participants and
the personnel at the Motion Analysis Laboratory, Sunnaas Rehabilitation Hospital, for
their respective contributions to the study.
This article was published as part of Mr
Opheims PhD thesis at Karolinska Institutet,
Stockholm, Sweden.
Ethical approval for the study was obtained
from the Regional Ethics Committee in

February 2012

This study was financially supported by

the Research Council of the South-Eastern
Regional Health Authority in Norway.
DOI: 10.2522/ptj.20100432

References
1 Sandstrom K, Alinder J, Oberg B. Descriptions of functioning and health and relations to a gross motor classification in
adults with cerebral palsy. Disabil Rehabil. 2004;26:10231031.
2 Jahnsen R, Villien L, Stanghelle JK, Holm I.
Fatigue in adults with cerebral palsy in
Norway compared with the general population. Dev Med Child Neurol. 2003;45:
296 303.
3 Jahnsen R, Villien L, Egeland T, et al. Locomotion skills in adults with cerebral palsy.
Clin Rehabil. 2004;18:309 316.
4 Jahnsen R, Villien L, Aamodt G, et al. Musculoskeletal pain in adults with cerebral
palsy compared with the general population. J Rehabil Med. 2004;36:78 84.
5 Schwartz L, Engel JM, Jensen MP. Pain in
persons with cerebral palsy. Arch Phys
Med Rehabil. 1999;80:12431246.
6 Andersson C, Mattsson E. Adults with cerebral palsy: a survey describing problems,
needs, and resources, with special emphasis on locomotion. Dev Med Child Neurol.
2001;43:76 82.
7 Opheim A, Jahnsen R, Olsson E, Stanghelle
JK. Walking function, pain, and fatigue in
adults with cerebral palsy: a 7-year
follow-up study. Dev Med Child Neurol.
2009;51:381388.
8 Shumway-Cook A, Woollacott MH. Motor
Control: Translating Research Into Clinical Practice. 3rd ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2007:158.
9 Horak FB, Macpherson J.M. Postural orientation and equilibrium. In: Rowell LB,
Shepard JT, eds. Handbook of Physiology,
Section 12Exercise: Regulation and
Integration of Multiple Systems. New
York, NY: Oxford University Press; 1996:
255292.
10 Horak FB. Postural orientation and equilibrium: what do we need to know about
neural control of balance to prevent falls?
Age Ageing. 2006;35:ii7ii11.
11 Gage JR, Schwartz MH, Koop SE, Novacheck TF. The identification and Treatment of Gait Problems in Cerebral Palsy.
2nd ed. London, United Kingdom: Mac
Keith Press; 2009:107113.
12 Burtner PA, Woollacott MH, Craft GL, Roncesvalles MN. The capacity to adapt to
changing balance threats: a comparison of
children with cerebral palsy and typically
developing children. Dev Neurorehabil.
2007;10:249 260.

13 Rose J, Wolff DR, Jones VK, et al. Postural

balance in children with cerebral palsy.
Dev Med Child Neurol. 2002;44:58 63.
14 Burtner PA, Qualls C, Woollacott MH. Muscle activation characteristics of stance balance control in children with spastic cerebral palsy. Gait Posture. 1998;8:163174.
15 Palisano R, Rosenbaum P, Walter S, et al.
Development and reliability of a system to
classify gross motor function in children
with cerebral palsy. Dev Med Child Neurol. 1997;39:214 223.
16 Jahnsen R, Aamodt G, Rosenbaum P. Gross
Motor Function Classification System used
in adults with cerebral palsy: agreement of
self-reported versus professional rating.
Dev Med Child Neurol. 2006;48:734 738.
17 McCormick A, Brien M, Plourde J, et al.
Stability of the Gross Motor Function Classification System in adults with cerebral
palsy. Dev Med Child Neurol. 2007;49:
265269.
18 Graham HK, Harvey A, Rodda J, et al. The
Functional Mobility Scale (FMS). J Pediatr
Orthop. 2004;24:514 520.
19 Bohannon RW, Smith MB. Interrater reliability of a modified Ashworth scale of
muscle spasticity. Phys Ther. 1987;67:
206 207.
20 Bhimani RH, Anderson LC, Henly SJ, Stoddard SA. Clinical measurement of limb
spasticity in adults: state of the science.
J Neurosci Nurs. 2011;43:104 115.
21 Fleuren JFM, Voerman GE, Erren-Wolters
CV, et al. Stop using the Ashworth Scale
for the assessment of spasticity. J Neurol
Neurosurg Psychiatry. 2010;81:46 52.
22 Ahlborg L, Andersson C, Julin P. Wholebody vibration training compared with
resistance training: effect on spasticity,
muscle strength and motor performance
in adults with cerebral palsy. J Rehabil
Med. 2006;38:302308.
23 Patrick E, Ada L. The Tardieu Scale differentiates contracture from spasticity
whereas the Ashworth Scale is confounded by it. Clin Rehabil. 2006;20:173
182.
24 Hislop HJ, Montgomery J. Daniels and
Worthinghams Muscle Testing: Techniques of Manual Examination. 8th ed.
St Louis, MO: Saunders Elsevier; 2007.
25 Bohannon RW. Measuring knee extensor
muscle strength. Am J Phys Med Rehabil.
2001;80:1318.
26 Powell LE, Myers AM. The Activitiesspecific Balance Confidence (ABC) Scale. J
Gerontol A Biol Sci Med Sci. 1995;50:
M28 M34.
27 Myers AM, Fletcher PC, Myers AH, Sherk
W. Discriminative and evaluative properties of the Activities-specific Balance Confidence (ABC) scale. J Gerontol A Biol Sci
Med Sci. 1998:M287M294.
28 Lajoie Y, Gallagher SP. Predicting falls
within the elderly community: comparison of postural sway, reaction time, the
Berg Balance Scale and the Activitiesspecific Balance Confidence (ABC) scale
for comparing fallers and non-fallers. Arch
Gerontol Geriatr. 2004;38:1126.

Volume 92 Number 2
Downloaded from http://ptjournal.apta.org/ by guest on December 21, 2014

Physical Therapy f

287

Balance in Adults With Spastic Bilateral Cerebral Palsy

29 Mak MK, Pang MY. Balance confidence
and functional mobility are independently
associated with falls in people with Parkinsons disease. J Neurol. 2009;256:742
749.
30 Yardley L, Beyer N, Hauer K, et al. Development and initial validation of the Falls
Efficacy ScaleInternational (FES-I). Age
Ageing. 2005;34:614 619.
31 Helbostad JL, Taraldsen K, Granbo R, et al.
Validation of the Falls Efficacy ScaleInternational in fall-prone older persons. Age
Ageing. 2010;39:256 259.
32 Helbostad JL, Yardley L. Falls Efficacy
ScaleInternational Norwegian version.
Available
at:
www.profane.eu.org.
Accessed August 15, 2009.
33 Delbaere K, Close JC, Mikolaizak AS, et al.
The Falls Efficacy ScaleInternational (FESI): a comprehensive longitudinal validation study. Age Ageing. 2010:210 216.
34 Nordell E, Andreasson M, Gall K, Thorngren KG. Evaluating the Swedish version
of the Falls Efficacy ScaleInternational
(FES-I). Adv Physiother. 2009;11:81 87.
35 Horak FB, Wrisley DM, Frank J. The Balance Evaluation Systems Test (BESTest) to
differentiate balance deficits. Phys Ther.
2009;89:484 498.
36 Dite W, Temple VA. A clinical test of stepping and change of direction to identify
multiple falling older adults. Arch Phys
Med Rehabil. 2002;83:1566 1571.

288

Physical Therapy

37 Whitney SL, Marchetti GF, Morris LO,

Sparto PJ. The reliability and validity of the
Four-Square Step Test for people with balance deficits secondary to a vestibular disorder. Arch Phys Med Rehabil. 2007;88:
99 104.
38 Blennerhassett JM, Jayalath VM. The FourSquare Step Test is a feasible and valid
clinical test of dynamic standing balance
for use in ambulant people poststroke.
Arch Phys Med Rehabil. 2008;89:2156
2161.
39 Altman DG. Practical Statistics for Medical Research. London, United Kingdom:
Chapman & Hall/CRC; 1991.
40 VassarStats. Available at: http://faculty.
vassar.edu/lowry/VassarStats.html. Accessed June 8, 2011.
41 Domholt E. Rehabilitation Research. 3rd
ed. St Louis, MO: Elsevier Saunders; 2005:
358.
42 Carlberg EB, Hadders-Algra M. Postural
dysfunction in children with cerebral palsy: some implications for therapeutic guidance. Neural Plast. 2005;12:221228.
43 Nashner LM, Shumway-Cook A, Marin O.
Stance posture control in select groups of
children with cerebral palsy: deficits in
sensory organization and muscular coordination. Exp Brain Res. 1983;49:393 409.
44 Brogren E, Forssberg H, Hadders-Algra M.
Influence of two different sitting positions
on postural adjustments in children with
spastic diplegia. Dev Med Child Neurol.
2001;43:534 546.

45 Lord SE, Weatherall M, Rochester L. Community ambulation in older adults: which

internal characteristics are important?
Arch Phys Med Rehabil. 2010;91:378
383.
46 Sihvonen S, Kulmala J, Kallinen M, et al.
Postural balance and self-reported balance
confidence in older adults with a hip fracture history. Gerontology. 2009;55:630
636.
47 Wrisley DM, Kumar NA. Functional gait
assessment: concurrent, discriminative,
and predictive validity in communitydwelling older adults. Phys Ther. 2010;90:
761773.
48 Wirz M, Muller R, Bastiaenen C. Falls in
persons with spinal cord injury: validity
and reliability of the Berg Balance Scale.
Neurorehabil Neural Repair. 2009;24:
70 77.
49 Hubscher M, Vogt L, Schmidt K, et al. Perceived pain, fear of falling and physical
function in women with osteoporosis.
Gait Posture. 2010;32:383385.
50 Rosenbaum P, Paneth N, Leviton A, et al. A
report: the definition and classification of
cerebral palsy, April 2006. Dev Med Child
Neurol. 2007;49:8 14.

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February 2012

Balance in Relation to Walking Deterioration in

Adults With Spastic Bilateral Cerebral Palsy
Arve Opheim, Reidun Jahnsen, Elisabeth Olsson and
Johan Kvalvik Stanghelle
PHYS THER. 2012; 92:279-288.
Originally published online October 27, 2011
doi: 10.2522/ptj.20100432

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