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Gait and Posture 14 (2001) 19–27
The effect of exercise on gait and balance in patients with chronic
fatigue syndrome
Lorna M. Paul a,
*, Leslie Wood b
, William Maclaren c
a
Department of Physiotherapy, Podiatry and Radiography, Glasgow Caledonian Uni6ersity, City Campus, Cowcaddens Road, Glasgow,
Scotland G4 OBA, UK
b
School of Biological and Biomedical Sciences, Glasgow Caledonian Uni6ersity, City Campus, Cowcaddens Road, Glasgow, Scotland G4 OBA, UK
c
Department of Mathematics, Glasgow Caledonian Uni6ersity, City Campus, Cowcaddens Road, Glasgow, Scotland G4 OBA, UK
Received 14 July 2000; accepted 25 November 2000
Abstract
This study investigated anecdotal reports of gait and balance abnormalities in subjects with Chronic Fatigue Syndrome (CFS)
by examining the effects of a light exercise test on postural sway and various gait parameters. Tests were performed on 11 CFS
patients and 11 age- and sex-matched sedentary controls. Results demonstrated that postural sway was not significantly different
in both groups before or after the exercise test. There were, however, significant differences in gait parameters between the two
groups confirming anecdotal evidence, but these differences were not exacerbated by the exercise test. Heart rate responses
demonstrated that both groups were exercising at similar loads, although this was perceived to be higher by the CFS group.
© 2001 Elsevier Science B.V. All rights reserved.
Keywords: Chronic fatigue syndrome; Gait analysis; Balance assessment; Exercise
www.elsevier.com/locate/gaitpost
1. Introduction
Chronic Fatigue Syndrome (CFS) is now the recog-
nised term used to cover a number of previously re-
ported conditions which had been named to reflect
either the site of reported epidemics (e.g. Iceland Dis-
ease, Royal Free Disease), the causative agent (e.g.
Epstein–Barr Virus Disease) or the symptoms pro-
duced (e.g. post-infection fatigue syndrome, effort syn-
drome, myalgic encephalomyelitis). As infection often
appears to be the precipitating factor, patients com-
monly present with fever, sore throat, cervical adenopa-
thy, cough or abdominal symptoms. Other clinical
features associated with CFS are wide and varied and
may fluctuate over time [1–3]. As the name suggests,
fatigue is the primary and often the most debilitating
symptom and anecdotally is reported to be exacerbated
by mental and/or physical activity. The problem of
diverse clinical presentations, lack of an objective test
for diagnosis and a number of different terminologies
led to a working case definition for Chronic Fatigue
Syndrome being developed by the Centres for Disease
Control (CDC) in the United States of America [4].
This case definition was more recently reviewed and
updated [5]. The incidence of CFS in the population is
difficult to determine accurately and has been reported
to range from 0.86 to 2 per 1000 of the population [6,7].
There is, however, general agreement that females are
more commonly affected than males [1,3] and that the
condition most commonly affects those aged between
20 and 40 years [8].
Static and dynamic balance are essential elements for
the performance of activities of daily living (ADL).
Komaroff [2] estimated that between 30 and 50% of
patients with CFS suffered some degree of dysequi-
librium whilst Merry [9] suggested the incidence could
be as high as 70% of all cases. Although impairment of
balance appears to be a significant problem in patients
with CFS, only a small number of studies have investi-
gated this problem.
Furman [10] used dynamic posturography to assess
the vestibular function of three subjects with CFS and
* Corresponding author. Tel.: +44-141-3318136; fax: +44-141-
3318130.
E-mail address: l.paul@gcal.ac.uk (L.M. Paul).
0966-6362/01/$ - see front matter © 2001 Elsevier Science B.V. All rights reserved.
PII: S0966-6362(00)00105-3
L.M. Paul et al. / Gait and Posture 14 (2001) 19–2720
reported that all three had abnormal test results, one
suggestive of a non-specific vestibular problem, the
other two a defect in the central nervous system. How-
ever, no firm conclusion could be reached due to the
small sample size. Ash-Bernal et al. [11] tested 11 CFS
subjects, specifically those who presented with dysequi-
librium. In order to examine their vestibular function
all subjects undertook a comprehensive battery of tests
including electronystagmography, earth vertical axis ro-
tation, earth horizontal axis rotation and posturogra-
phy. The study concluded that vestibular abnormalities
did exist in all subjects studied but that different sub-
jects had abnormalities in different tests and no consis-
tent pattern was found which could identify one specific
defect.
Gait is a fundamental activity and, like balance, can
be affected by virtually all neuromuscular disorders
[12]. Investigations of gait abnormalities in CFS are
also very scarce. Boda et al. [13] analysed CFS subjects’
gait at pre-determined speeds on a treadmill and also
timed the subjects’ running and walking for 30 m. The
study reported that CFS subjects’ running speed was
significantly slower than controls and, whilst walking
on the treadmill, CFS subjects had smaller stride
lengths at slower speeds. Although this study reported a
number of gait abnormalities in subjects with CFS, the
kinematic patterns of gait are different in free walking
and treadmill walking [14,15] and so these results may
not be representative of the subjects’ ‘normal’ gait
pattern.
Saggini et al. [16] examined the gait patterns of 12
subjects with CFS and compared their results to an
existing database of 596 normal subjects (aged 3–60
years). Subjects walked six times along a 2.5 m pressure
platform, then walked for 212 m and their gait was
reassessed. This protocol was repeated three times. The
study found that in the initial gait assessment no signifi-
cant differences were found in the gait parameters
between CFS subjects and controls. However, following
the 212 m walk the gait parameters of the CFS subjects
were altered with half displaying abnormalities in the
temporal phases of gait and 11 of the 12 subjects
showing abnormalities in the spatial phases of gait.
This study used a database of controls of varied age
and presumably fitness (although this was not specified)
and therefore presents a methodological problem. It is
recognised that the use of sedentary controls is essential
when studying subjects with CFS [17] and therefore it is
unclear whether such a group forms a suitable control
for comparisons with CFS patients.
It is generally agreed that the symptoms of CFS are
exacerbated by even minor activity [17–21]. McCully et
al. [17] reported that exacerbation of symptoms began
6–48 h after activity and may last 2–14 days. We have
recently demonstrated that recovery of muscle function
following fatiguing exercise is substantially reduced in
CFS patients [22] however, apart from this study little
has been done to examine this phenomenon of post-ex-
ertional malaise in those with CFS.
Gait and balance parameters in those with CFS have
not been extensively examined and the effect of exercise
on these basic pre-requisites for ADL has never been
systematically investigated. The aims of this study were
therefore to objectively examine the gait and balance of
subjects with CFS, and a suitable control group, and to
evaluate changes in these parameters at various time
intervals following a 15 min period of light exercise.
2. Methods
2.1. Subjects
Eleven subjects with CFS and 11 control subjects
participated in the study (Table 1). All patients fulfilled
the CDC criteria for CFS [5]. Age and sex matched
control subjects were healthy but sedentary individuals
who did not participate in any regular exercise and who
were previously unfamiliar with the equipment or pro-
tocols used in the study.
All testing was undertaken with informed consent
and with local Ethical Committee approval. Tests were
performed in the Clinical Research Centre of the
Southern General Hospital, NHS Trust, Glasgow.
2.2. Balance assessment
To measure postural sway, as a measure of balance,
subjects stood on a Kistler Force Platform (Model
9281C, Kistler Instruments Ltd, England) with their
feet together and arms comfortably by their sides. Each
test lasted 25 s and was performed under conditions of
eyes opened (EO) and eyes closed (EC). The output
from the Kistler Force Platform was digitised using a
CED 1401 Plus (Cambridge Electronic Design, Eng-
land), at a sampling frequency of 50 Hz, and stored on
an Elonex 486DX computer for off-line analysis.
Table 1
Description of the subjects participating in the study
ControlChronic fatigue
syndrome
Sex
Male 11
1010Female
33.91 (97.27)Mean age in years 33.09 (97.20)
(9SD)
163.64 (97.38)Mean height in cm 166.09 (98.23)
(9SD)
L.M. Paul et al. / Gait and Posture 14 (2001) 19–27 21
2.2.1. Dispersion X and dispersion Y
Dispersion X and Y describe the postural sway in the
anteroposterior and mediolateral directions, respec-
tively. The average positions of the centre of pressure in
both the anteroposterior (Ax) and mediolateral (Ay)
directions were calculated. The absolute difference be-
tween the average position of the centre of pressure and
each data point was calculated and averaged over the
25 s duration of the test. Dispersion was calculated
according to the following equation.
Dispersion X
=
%i=1
n
Absolute value of(Ax(i )−Average Ax)
n
,
where: dispersion X is the total movement (in cm) of
the subject’s centre of pressure in the anteroposterior
direction; Ax(i ) is the centre of pressure in the antero-
posterior direction for each sample i=1 to n; n is the
number of samples.
A similar calculation was performed for Dispersion Y
with respect to dispersion in the mediolateral direction.
2.2.2. Total dispersion
Total dispersion describes the overall postural sway
during the test. The total dispersion value was calcu-
lated by combining the excursion from the average
centre of pressure for each point. Therefore:
Dispersion=
%i=1
n

(Average Ay− Ay(i ))2
+(Average Ax−Ax(i ))2
n
,
where: dispersion is the total movement (in cm) of the
subject’s centre of pressure; Ax(i ) is the centre of
pressure in the anteroposterior direction for each sam-
ple; Ay(i ) is the centre of pressure in the mediolateral
direction for each sample; n is the number of samples.
2.3. Gait analysis
Gait was analysed on the CalMat, a computer con-
trolled, pressure sensitive, instrumented walkway which
is 4.5 m in length [23]. The active section is 3 m long
and consists of an array of 2.3 cm2
pressure sensitive
cells arranged along the length of the walkway. Contact
from the subject’s foot or shoe activates these cells and
produces data relating to the position and timing of
foot contact. Subjects are not attached to any appara-
tus and thus their gait is not impeded in any way.
Subjects walked along the walkmat three times at their
own preferred walking speed. On completion of each
test the data was verified to be complete and stored on
the hard disc of a Dan PC486 for off-line analysis using
custom written software. Parameters of step distance,
step time, time of single and double support, velocity,
relative velocity and cadence were recorded.
2.4. Exercise test
Following the initial assessment of balance and gait,
as described, subjects underwent a Sub-Anaerobic
Threshold Exercise Test (SATET) following the proto-
col described by Nashef and Lane and previously used
with CFS patients [24]. Subjects pedalled a bicycle
ergometer (Tunturi ECB Pro Ergometer 850E) for 15
min at 90% of their predicted work rate at their anaer-
obic threshold, based on sex, age and weight. A sub-
anaerobic threshold test was chosen to more closely
reflect the activities of daily living and to prevent the
possibility of overly exacerbating symptoms in the CFS
patients.
Just before the exercise test began and at 1 min
intervals during the steady state test, the subject’s heart
rate was recorded using a Polar heart rate monitor. At
the same time intervals subjects were asked to rate their
level of perceived exertion using the 15 point Borg scale
[25].
Following the 15 min exercise period each subject’s
balance and gait were reassessed as described above.
Balance and gait assessments were repeated at 20 min
intervals for the following hour with subjects resting,
seated on a chair between tests.
All subjects returned to the Clinical Research Centre
24 h following the exercise period for a further assess-
ment of balance and gait and to examine any longer
effects of the previous day’s exercise.
2.5. Statistical analysis
For each of the ten gait parameters, a ‘mixed model’
was fitted, which included case-control status and time-
point as fixed factors, case-control pair as a random
factor, together with its interactions with the fixed
factors, and (except for relative velocity) a single co-
variate, namely height. The statistical significance of
case-control differences, differences between time points
and the extent to which case-control effects depend on
time points was assessed using Analysis of Variance
(ANOVA), and specific comparisons were made using
follow-up t-tests. The same structure of mixed model
was used in the analysis of balance parameters (height
was not included as a covariate).
ANOVA was also used to examine heart rate and the
level of perceived exertion during the exercise test.
Fixed effects were subject group and time point, and
matched pairs were included as a random effect.
Matched cases and controls were compared, using
paired t-tests, on heart rate and level of perceived
exertion on the Borg scale.
L.M. Paul et al. / Gait and Posture 14 (2001) 19–2722
Table 2
Results of gait analysis with ANOVA comparing chronic fatigue syndrome and control group
Control subjects (n=11)Gait parameter P valueChronic fatigue syndrome patients (n=11)
Step distance-right (cm) 70.1559.51 0.006*
69.3459.74 0.008*Step distance-left (cm)
0.51Step time-right (s) 0.017*0.57
0.500.56 0.014*Step time-left (s)
0.48Single support time-right (s) 0.44 0.020*
0.450.47 0.088Single support time-left (s)
0.16Double support time (s) 0.0660.19
0.840.64 0.002*Relative velocity (stats/s)a
1.39Velocity (m/s) 0.002*1.05
120.3106.3 0.011*Cadence (steps/min)
* Denotes statistically significant value at PB0.05.
a
ANOVA calculation does not include height as a covariate.
3. Results
3.1. Balance results
Data was unavailable for one of the initial 11 sub-
jects due to problems with data storage on the com-
puter, and thus the results from 10 CFS subjects and 10
matched controls are presented.
Fig. 1 shows all the Dispersion measures for CFS
subjects and controls during eyes opened and eyes
closed conditions.
Under eyes open conditions (Fig. 1a, c, e) postural
sway was higher in the CFS subjects compared to the
control subjects up to 40 min after exercise. After this
the trend was reversed with postural sway being greater
in the control subjects at 60 min and 24 h after exercise.
The exception was postural sway in the anteroposterior
direction (Dispersion X) where postural sway remained
higher in the CFS subjects.
Under eyes closed conditions (Fig. 1b, d, f) postural
sway was generally higher in the CFS subjects through-
out each stage of the protocol. The exception being
postural sway in the anteroposterior direction 20 and
60 min following exercise where it was higher in the
control subjects.
For both CFS subjects and controls, postural sway
was greater with visual input eliminated and further-
more postural sway was increased following exercise.
The results from a two factor ANOVA (with means
adjusted for missing values) demonstrated that under
eyes opened conditions, for Dispersion X, Dispersion Y
and Total Dispersion averaged over time, there was no
statistically significant difference between the CFS
group and the control group (Dispersion X; P=0.695,
Dispersion Y; P=0.593, Total Dispersion; P=0.570).
In addition, for each of the three parameters, averaged
over the two groups there were no significant differ-
ences between time points (P=0.785, 0.874 and 0.856,
respectively). Finally there was no significant interac-
tion effect between group and time point for any of the
three balance parameters (P=0.650, 0.561 and 0.419,
respectively). The results therefore suggest that exercise
had no significant effect on the postural sway of either
CFS subjects or controls under eyes opened conditions.
Similarly under eyes closed conditions there was no
statistically significant difference in Dispersion, aver-
aged over time points, between CFS subjects and con-
trols (Dispersion X; P=0.669, Dispersion Y;
P=0.399, Total Dispersion; P=0.503). There were,
however, statistically significant differences between
time points for all three balance parameters (p=
0.030, 0.033 and 0.012, respectively) but there was no
evidence that this pattern was different for CFS sub-
jects and controls, as demonstrated by a non-significant
interaction effect (P=0.626, 0.686 and 0.533, respec-
tively). Thus whilst exercise may have had some effect
on postural stability with subjects’ eyes closed the effect
was similar for both CFS subjects and controls.
3.2. Gait results
Table 2 shows a summary of the gait results for 11
CFS subjects and 11 matched controls. An ANOVA
was performed on each of the gait parameters (with
height included as a covariate for all parameters except
relative velocity). The results of the ANOVA suggested
that there was a statistically significant difference be-
tween the two groups, averaged over time, for all of the
gait parameters measured, with the exception of single
support on the left side and the time of double support.
In clinical terms this means that CFS subjects walked
with smaller steps and the time taken by CFS subjects
for each step was more than that taken by control
subjects. As a consequence velocity and relative velocity
were reduced and cadence was increased in those with
CFS.
ANOVA showed that, with one exception, there were
no statistically significant differences between time
points for any of the gait parameters after exercise. This
would suggest that the period of exercise did not affect
L.M. Paul et al. / Gait and Posture 14 (2001) 19–27 23
Fig. 1. Dispersion for CFS patients (black bars) and control subjects (white bars) before, immediately after, and at various time points following
the Sub-Anaerobic Threshold Exercise Tolerance test. (a) Dispersion in the anteroposterior (X) direction with eyes open; (b) Dispersion in the
anteroposterior (X) direction with eyes closed; (c) Dispersion in the mediolateral (Y) direction with eyes open; (d) Dispersion in the mediolateral
(Y) direction with eyes closed; (e) Total dispersion with eyes open; (f) Total Dispersion with eyes closed. All values are mean9standard error,
n=10 in each group.
L.M. Paul et al. / Gait and Posture 14 (2001) 19–2724
the gait pattern of either the CFS or control group. The
exception was single support time on the right where
there was a statistically significant interaction between
CFS/control and time point (P=0.044). However, the
CFS/control differences did not follow any obvious
pattern with time elapsed following exercise. There is
no apparent explanation for this isolated effect and it
may be due to chance given the marginal P-value.
3.3. Heart rate and ratings of percei6ed exertion (RPE)
scores during exercise
All CFS and control subjects were able to complete
the exercise protocol. Fig. 2 shows the mean heart rate
and Fig. 3 the mean RPE scores taken during each
minute of the exercise period. Both responses were
analysed using ANOVA where fixed effects were sub-
ject group (CFS or control) and time point, and
matched pairs were included as a random effect. The
heart rate response of both the CFS and control group
were similar (Fig. 2) and this was confirmed by
ANOVA. The increasing trend in heart rate was statis-
tically significant (PB0.001) but the difference between
subject groups, averaged over time, was not (P=
0.230). In addition the interaction between time point
and subject group was not statistically significant (P=
0.789).
The mean RPE scores, however, were very different
in the two groups (Fig. 3) and ANOVA demonstrated
that there was a statistically significant difference be-
tween the two groups averaged over time points (PB
0.001). The difference between the CFS and control
groups in the slope of the trend lines was also statisti-
cally significant (PB0.001). Therefore, although the
physiological response to exercise appeared similar in
both groups, as demonstrated by the heart rate re-
sponse, the CFS group perceived the workload to be
significantly greater.
4. Discussion
The results of the present study demonstrate that
there was no significant difference in postural stability
between CFS and control subjects as evidenced by
differences in dispersion under eyes open and eyes
closed conditions (Fig. 1), and thus do not support the
suggestion that patients with CFS display some degree
of dysequilibrium [2,9]. Whilst exercise does affect pos-
tural stability to a significant extent, it does so for both
patients and controls and there is no significant differ-
ence in the degree of impairment observed between the
two groups. Some studies have previously demon-
strated balance problems in patients with CFS [10,11]
however, these abnormalities were non-specific and
were observed mainly in subjects who presented with
pre-existing balance problems. The present results sug-
gest that balance abnormalities, either at rest or after
Fig. 2. Heart rate response to exercise in CFS patients (white circles) and control subjects (black squares). Values are mean heart rate9standard
error, n=11 in each group. There was no significant difference between CFS patients and control subjects at any of the time points during the
exercise test.
L.M. Paul et al. / Gait and Posture 14 (2001) 19–27 25
Fig. 3. Ratings of perceived exertion-RPE (Borg Scale) during the exercise test for CFS patients (white circles) and control subjects (black squares).
Values are mean RPE scores9standard error, n=11 in each group. The RPE scores of the CFS patients were significantly higher than those of
the control group at all time points during the exercise test (PB0.001).
exercise, are not a feature of the general population of
CFS patients. It has been reported that postural sway,
measured in a stance position on a fixed force plate,
may be normal in the presence of many postural defects
[26] and it may be that the static balance tests employed
in the current study are not sensitive enough to detect
subtle balance abnormalities which may exist in these
subjects. It is hoped, in future research, to employ more
dynamic balance tests in order to observe if these reveal
more minor postural deficits which may exist.
The results of the gait analysis show that CFS pa-
tients demonstrate significant differences in many gait
parameters compared to control subjects (Table 2).
These differences are seen pre- and post-exercise, al-
though exercise does not exacerbate the effects in the
CFS patients. Only two of the measured gait parame-
ters — single support time on the left and double
support time — were not significantly different between
the CFS and control groups. These observations would
support the clinical impression that CFS subjects walk
more slowly and with smaller steps compared to normal
control subjects, and are consistent with slower move-
ments and reaction times observed in CFS patients [27].
Data relating to step width was also collected but,
because of the technical specification of the walkway,
this parameter was deemed to have too much associ-
ated measurement error and thus this data was not
formally analysed.
The results of the present study contrast with those
of Boda et al. [13] which did not demonstrate any
significant difference in walking times between CFS
patients and controls. However, the Calmat computer-
ised walkway used in the present study may allow for
more accurate timings of gait parameters than in previ-
ous studies. The smaller step length observed in the
current study is consistent with the findings of Boda et
al. [13], who demonstrated that the degree of hip and
knee movement was less in subjects with CFS, and
suggested that this may be an attempt to improve
overall stability during the gait cycle. Saggini et al. [16]
reported no difference in gait parameters between CFS
patients and controls before exercise but did demon-
strate some spatial and temporal abnormalities follow-
ing exercise. However, the lack of a sedentary control
group precludes any useful comparison with the present
study. This is considered to be a vital requirement in
selecting control subjects for studies involving CFS
patients due to the deconditioning effect of the disorder
[17]. The present study did use sedentary controls and
the results would therefore suggest that CFS patients,
similar to controls, do not have any significant alter-
ations in gait after exercise.
Gait changes may occur in CFS subjects as a result
of balance problems, peripheral neuromuscular dys-
function or abnormalities in the higher central nervous
system, acting either individually or in combination
L.M. Paul et al. / Gait and Posture 14 (2001) 19–2726
[13]. The results of the current study suggest that
balance problems may not be a contributory factor to
gait abnormalities since double support time in the CFS
subjects was not significantly different from controls
(although the differences did approach significance),
and static balance was not significantly affected in CFS
patients. We have previously demonstrated that there is
reduced voluntary muscle force in the quadriceps mus-
cle in CFS patients [22], which may contribute to
observed initial reductions in step length, cadence and
velocity in these patients. Fifteen minutes of sub-anaer-
obic exercise did not exacerbate the abnormal gait
parameters in the present study however, and therefore
does not support the anecdotal evidence that symptoms
of CFS, as evidenced by gait changes, are affected by a
period of sub-maximal exercise. This suggests that CFS
patients may be able to participate in light, sub-anaero-
bic exercise protocols without detrimental effects on
their gait or balance. This observation may therefore be
useful for health-care professionals wishing to educate
CFS patients on an appropriate level of exercise to
reduce the possible effects of deconditioning without
leading to worsening of symptoms [28].
The heart rate responses to exercise show that both
the CFS patients and the control subjects were exercis-
ing at similar physiological workload, since the steady
state heart rate achieved after 3 or so minutes was not
significantly different between the two groups, being
approximately 125–130 beats per min (Fig. 2). This
heart rate also confirms that subjects were exercising at
a fairly light intensity, well below anaerobic threshold.
It may be that exercising at a higher intensity would
have produced more demonstrable effects on the gait
abnormalities observed post-exercise.
Despite the fact that the CFS patients were exercising
at a clearly sub-maximal level, which was not signifi-
cantly different from the control subjects, the patients
reported a significantly greater perception of effort,
reflected in a mean RPE rating of 16 towards the end of
the exercise period compared to a mean rating of about
10 for the control group (Fig. 3). This rating for the
control group more accurately reflects the actual physi-
ological load undertaken by the subject. However, the
patient group obviously perceives this workload to be
much higher than it actually is. The RPE rating sug-
gests that the patients were working at close to maximal
levels, whilst the heart rate data demonstrates that they
were well below this level. This may be due to an
increased sense of effort [19,29] possibly linked to alter-
ations in 5-hydroxytryptamine (5HT) levels in the brain
[30] and increased sensitivity of the 5HT receptors [31],
or to a degree of hyperalgesia within the muscles them-
selves [32]. Since ratings of perceived exertion are often
used in many areas of rehabilitation to allow patients to
monitor their workload, the results of the present study
would suggest that this is inappropriate in CFS
patients.
5. Conclusion
In conclusion, the results presented here would sug-
gest that balance problems are not a consistent feature
in CFS patients. However, more dynamic assessments
of this patient group are required. CFS patients do tend
to walk with an altered gait pattern compared to nor-
mal controls and this concurs with the general notion
that these patients have slower movements than nor-
mal. This finding would suggest that gait analysis may
be a useful outcome measure with which to monitor the
progress of the disease or to determine the effectiveness
of treatment interventions, therapeutic or pharmacolog-
ical. Patients with CFS perceive the exercise load to be
considerably higher than the actual physiological load
thus the use of the RPE scale would not be a valid
method of monitoring exercise intensity in this group.
Acknowledgements
This research was supported by grants from Action
for ME and Women of Scotland Luncheon. Apprecia-
tion is extended to the technical staff within the depart-
ment of Physiotherapy, Podiatry and Radiography at
Glasgow Caledonian University with particular thanks
to Danny Rafferty and Gail Mackie. We are grateful to
Professor PO Behan for his co-operation and assistance
and to Dr Gordon Parish for his help and support.
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The effect of exercise on gait and balance in CFS patients

  • 1. Gait and Posture 14 (2001) 19–27 The effect of exercise on gait and balance in patients with chronic fatigue syndrome Lorna M. Paul a, *, Leslie Wood b , William Maclaren c a Department of Physiotherapy, Podiatry and Radiography, Glasgow Caledonian Uni6ersity, City Campus, Cowcaddens Road, Glasgow, Scotland G4 OBA, UK b School of Biological and Biomedical Sciences, Glasgow Caledonian Uni6ersity, City Campus, Cowcaddens Road, Glasgow, Scotland G4 OBA, UK c Department of Mathematics, Glasgow Caledonian Uni6ersity, City Campus, Cowcaddens Road, Glasgow, Scotland G4 OBA, UK Received 14 July 2000; accepted 25 November 2000 Abstract This study investigated anecdotal reports of gait and balance abnormalities in subjects with Chronic Fatigue Syndrome (CFS) by examining the effects of a light exercise test on postural sway and various gait parameters. Tests were performed on 11 CFS patients and 11 age- and sex-matched sedentary controls. Results demonstrated that postural sway was not significantly different in both groups before or after the exercise test. There were, however, significant differences in gait parameters between the two groups confirming anecdotal evidence, but these differences were not exacerbated by the exercise test. Heart rate responses demonstrated that both groups were exercising at similar loads, although this was perceived to be higher by the CFS group. © 2001 Elsevier Science B.V. All rights reserved. Keywords: Chronic fatigue syndrome; Gait analysis; Balance assessment; Exercise www.elsevier.com/locate/gaitpost 1. Introduction Chronic Fatigue Syndrome (CFS) is now the recog- nised term used to cover a number of previously re- ported conditions which had been named to reflect either the site of reported epidemics (e.g. Iceland Dis- ease, Royal Free Disease), the causative agent (e.g. Epstein–Barr Virus Disease) or the symptoms pro- duced (e.g. post-infection fatigue syndrome, effort syn- drome, myalgic encephalomyelitis). As infection often appears to be the precipitating factor, patients com- monly present with fever, sore throat, cervical adenopa- thy, cough or abdominal symptoms. Other clinical features associated with CFS are wide and varied and may fluctuate over time [1–3]. As the name suggests, fatigue is the primary and often the most debilitating symptom and anecdotally is reported to be exacerbated by mental and/or physical activity. The problem of diverse clinical presentations, lack of an objective test for diagnosis and a number of different terminologies led to a working case definition for Chronic Fatigue Syndrome being developed by the Centres for Disease Control (CDC) in the United States of America [4]. This case definition was more recently reviewed and updated [5]. The incidence of CFS in the population is difficult to determine accurately and has been reported to range from 0.86 to 2 per 1000 of the population [6,7]. There is, however, general agreement that females are more commonly affected than males [1,3] and that the condition most commonly affects those aged between 20 and 40 years [8]. Static and dynamic balance are essential elements for the performance of activities of daily living (ADL). Komaroff [2] estimated that between 30 and 50% of patients with CFS suffered some degree of dysequi- librium whilst Merry [9] suggested the incidence could be as high as 70% of all cases. Although impairment of balance appears to be a significant problem in patients with CFS, only a small number of studies have investi- gated this problem. Furman [10] used dynamic posturography to assess the vestibular function of three subjects with CFS and * Corresponding author. Tel.: +44-141-3318136; fax: +44-141- 3318130. E-mail address: l.paul@gcal.ac.uk (L.M. Paul). 0966-6362/01/$ - see front matter © 2001 Elsevier Science B.V. All rights reserved. PII: S0966-6362(00)00105-3
  • 2. L.M. Paul et al. / Gait and Posture 14 (2001) 19–2720 reported that all three had abnormal test results, one suggestive of a non-specific vestibular problem, the other two a defect in the central nervous system. How- ever, no firm conclusion could be reached due to the small sample size. Ash-Bernal et al. [11] tested 11 CFS subjects, specifically those who presented with dysequi- librium. In order to examine their vestibular function all subjects undertook a comprehensive battery of tests including electronystagmography, earth vertical axis ro- tation, earth horizontal axis rotation and posturogra- phy. The study concluded that vestibular abnormalities did exist in all subjects studied but that different sub- jects had abnormalities in different tests and no consis- tent pattern was found which could identify one specific defect. Gait is a fundamental activity and, like balance, can be affected by virtually all neuromuscular disorders [12]. Investigations of gait abnormalities in CFS are also very scarce. Boda et al. [13] analysed CFS subjects’ gait at pre-determined speeds on a treadmill and also timed the subjects’ running and walking for 30 m. The study reported that CFS subjects’ running speed was significantly slower than controls and, whilst walking on the treadmill, CFS subjects had smaller stride lengths at slower speeds. Although this study reported a number of gait abnormalities in subjects with CFS, the kinematic patterns of gait are different in free walking and treadmill walking [14,15] and so these results may not be representative of the subjects’ ‘normal’ gait pattern. Saggini et al. [16] examined the gait patterns of 12 subjects with CFS and compared their results to an existing database of 596 normal subjects (aged 3–60 years). Subjects walked six times along a 2.5 m pressure platform, then walked for 212 m and their gait was reassessed. This protocol was repeated three times. The study found that in the initial gait assessment no signifi- cant differences were found in the gait parameters between CFS subjects and controls. However, following the 212 m walk the gait parameters of the CFS subjects were altered with half displaying abnormalities in the temporal phases of gait and 11 of the 12 subjects showing abnormalities in the spatial phases of gait. This study used a database of controls of varied age and presumably fitness (although this was not specified) and therefore presents a methodological problem. It is recognised that the use of sedentary controls is essential when studying subjects with CFS [17] and therefore it is unclear whether such a group forms a suitable control for comparisons with CFS patients. It is generally agreed that the symptoms of CFS are exacerbated by even minor activity [17–21]. McCully et al. [17] reported that exacerbation of symptoms began 6–48 h after activity and may last 2–14 days. We have recently demonstrated that recovery of muscle function following fatiguing exercise is substantially reduced in CFS patients [22] however, apart from this study little has been done to examine this phenomenon of post-ex- ertional malaise in those with CFS. Gait and balance parameters in those with CFS have not been extensively examined and the effect of exercise on these basic pre-requisites for ADL has never been systematically investigated. The aims of this study were therefore to objectively examine the gait and balance of subjects with CFS, and a suitable control group, and to evaluate changes in these parameters at various time intervals following a 15 min period of light exercise. 2. Methods 2.1. Subjects Eleven subjects with CFS and 11 control subjects participated in the study (Table 1). All patients fulfilled the CDC criteria for CFS [5]. Age and sex matched control subjects were healthy but sedentary individuals who did not participate in any regular exercise and who were previously unfamiliar with the equipment or pro- tocols used in the study. All testing was undertaken with informed consent and with local Ethical Committee approval. Tests were performed in the Clinical Research Centre of the Southern General Hospital, NHS Trust, Glasgow. 2.2. Balance assessment To measure postural sway, as a measure of balance, subjects stood on a Kistler Force Platform (Model 9281C, Kistler Instruments Ltd, England) with their feet together and arms comfortably by their sides. Each test lasted 25 s and was performed under conditions of eyes opened (EO) and eyes closed (EC). The output from the Kistler Force Platform was digitised using a CED 1401 Plus (Cambridge Electronic Design, Eng- land), at a sampling frequency of 50 Hz, and stored on an Elonex 486DX computer for off-line analysis. Table 1 Description of the subjects participating in the study ControlChronic fatigue syndrome Sex Male 11 1010Female 33.91 (97.27)Mean age in years 33.09 (97.20) (9SD) 163.64 (97.38)Mean height in cm 166.09 (98.23) (9SD)
  • 3. L.M. Paul et al. / Gait and Posture 14 (2001) 19–27 21 2.2.1. Dispersion X and dispersion Y Dispersion X and Y describe the postural sway in the anteroposterior and mediolateral directions, respec- tively. The average positions of the centre of pressure in both the anteroposterior (Ax) and mediolateral (Ay) directions were calculated. The absolute difference be- tween the average position of the centre of pressure and each data point was calculated and averaged over the 25 s duration of the test. Dispersion was calculated according to the following equation. Dispersion X = %i=1 n Absolute value of(Ax(i )−Average Ax) n , where: dispersion X is the total movement (in cm) of the subject’s centre of pressure in the anteroposterior direction; Ax(i ) is the centre of pressure in the antero- posterior direction for each sample i=1 to n; n is the number of samples. A similar calculation was performed for Dispersion Y with respect to dispersion in the mediolateral direction. 2.2.2. Total dispersion Total dispersion describes the overall postural sway during the test. The total dispersion value was calcu- lated by combining the excursion from the average centre of pressure for each point. Therefore: Dispersion= %i=1 n (Average Ay− Ay(i ))2 +(Average Ax−Ax(i ))2 n , where: dispersion is the total movement (in cm) of the subject’s centre of pressure; Ax(i ) is the centre of pressure in the anteroposterior direction for each sam- ple; Ay(i ) is the centre of pressure in the mediolateral direction for each sample; n is the number of samples. 2.3. Gait analysis Gait was analysed on the CalMat, a computer con- trolled, pressure sensitive, instrumented walkway which is 4.5 m in length [23]. The active section is 3 m long and consists of an array of 2.3 cm2 pressure sensitive cells arranged along the length of the walkway. Contact from the subject’s foot or shoe activates these cells and produces data relating to the position and timing of foot contact. Subjects are not attached to any appara- tus and thus their gait is not impeded in any way. Subjects walked along the walkmat three times at their own preferred walking speed. On completion of each test the data was verified to be complete and stored on the hard disc of a Dan PC486 for off-line analysis using custom written software. Parameters of step distance, step time, time of single and double support, velocity, relative velocity and cadence were recorded. 2.4. Exercise test Following the initial assessment of balance and gait, as described, subjects underwent a Sub-Anaerobic Threshold Exercise Test (SATET) following the proto- col described by Nashef and Lane and previously used with CFS patients [24]. Subjects pedalled a bicycle ergometer (Tunturi ECB Pro Ergometer 850E) for 15 min at 90% of their predicted work rate at their anaer- obic threshold, based on sex, age and weight. A sub- anaerobic threshold test was chosen to more closely reflect the activities of daily living and to prevent the possibility of overly exacerbating symptoms in the CFS patients. Just before the exercise test began and at 1 min intervals during the steady state test, the subject’s heart rate was recorded using a Polar heart rate monitor. At the same time intervals subjects were asked to rate their level of perceived exertion using the 15 point Borg scale [25]. Following the 15 min exercise period each subject’s balance and gait were reassessed as described above. Balance and gait assessments were repeated at 20 min intervals for the following hour with subjects resting, seated on a chair between tests. All subjects returned to the Clinical Research Centre 24 h following the exercise period for a further assess- ment of balance and gait and to examine any longer effects of the previous day’s exercise. 2.5. Statistical analysis For each of the ten gait parameters, a ‘mixed model’ was fitted, which included case-control status and time- point as fixed factors, case-control pair as a random factor, together with its interactions with the fixed factors, and (except for relative velocity) a single co- variate, namely height. The statistical significance of case-control differences, differences between time points and the extent to which case-control effects depend on time points was assessed using Analysis of Variance (ANOVA), and specific comparisons were made using follow-up t-tests. The same structure of mixed model was used in the analysis of balance parameters (height was not included as a covariate). ANOVA was also used to examine heart rate and the level of perceived exertion during the exercise test. Fixed effects were subject group and time point, and matched pairs were included as a random effect. Matched cases and controls were compared, using paired t-tests, on heart rate and level of perceived exertion on the Borg scale.
  • 4. L.M. Paul et al. / Gait and Posture 14 (2001) 19–2722 Table 2 Results of gait analysis with ANOVA comparing chronic fatigue syndrome and control group Control subjects (n=11)Gait parameter P valueChronic fatigue syndrome patients (n=11) Step distance-right (cm) 70.1559.51 0.006* 69.3459.74 0.008*Step distance-left (cm) 0.51Step time-right (s) 0.017*0.57 0.500.56 0.014*Step time-left (s) 0.48Single support time-right (s) 0.44 0.020* 0.450.47 0.088Single support time-left (s) 0.16Double support time (s) 0.0660.19 0.840.64 0.002*Relative velocity (stats/s)a 1.39Velocity (m/s) 0.002*1.05 120.3106.3 0.011*Cadence (steps/min) * Denotes statistically significant value at PB0.05. a ANOVA calculation does not include height as a covariate. 3. Results 3.1. Balance results Data was unavailable for one of the initial 11 sub- jects due to problems with data storage on the com- puter, and thus the results from 10 CFS subjects and 10 matched controls are presented. Fig. 1 shows all the Dispersion measures for CFS subjects and controls during eyes opened and eyes closed conditions. Under eyes open conditions (Fig. 1a, c, e) postural sway was higher in the CFS subjects compared to the control subjects up to 40 min after exercise. After this the trend was reversed with postural sway being greater in the control subjects at 60 min and 24 h after exercise. The exception was postural sway in the anteroposterior direction (Dispersion X) where postural sway remained higher in the CFS subjects. Under eyes closed conditions (Fig. 1b, d, f) postural sway was generally higher in the CFS subjects through- out each stage of the protocol. The exception being postural sway in the anteroposterior direction 20 and 60 min following exercise where it was higher in the control subjects. For both CFS subjects and controls, postural sway was greater with visual input eliminated and further- more postural sway was increased following exercise. The results from a two factor ANOVA (with means adjusted for missing values) demonstrated that under eyes opened conditions, for Dispersion X, Dispersion Y and Total Dispersion averaged over time, there was no statistically significant difference between the CFS group and the control group (Dispersion X; P=0.695, Dispersion Y; P=0.593, Total Dispersion; P=0.570). In addition, for each of the three parameters, averaged over the two groups there were no significant differ- ences between time points (P=0.785, 0.874 and 0.856, respectively). Finally there was no significant interac- tion effect between group and time point for any of the three balance parameters (P=0.650, 0.561 and 0.419, respectively). The results therefore suggest that exercise had no significant effect on the postural sway of either CFS subjects or controls under eyes opened conditions. Similarly under eyes closed conditions there was no statistically significant difference in Dispersion, aver- aged over time points, between CFS subjects and con- trols (Dispersion X; P=0.669, Dispersion Y; P=0.399, Total Dispersion; P=0.503). There were, however, statistically significant differences between time points for all three balance parameters (p= 0.030, 0.033 and 0.012, respectively) but there was no evidence that this pattern was different for CFS sub- jects and controls, as demonstrated by a non-significant interaction effect (P=0.626, 0.686 and 0.533, respec- tively). Thus whilst exercise may have had some effect on postural stability with subjects’ eyes closed the effect was similar for both CFS subjects and controls. 3.2. Gait results Table 2 shows a summary of the gait results for 11 CFS subjects and 11 matched controls. An ANOVA was performed on each of the gait parameters (with height included as a covariate for all parameters except relative velocity). The results of the ANOVA suggested that there was a statistically significant difference be- tween the two groups, averaged over time, for all of the gait parameters measured, with the exception of single support on the left side and the time of double support. In clinical terms this means that CFS subjects walked with smaller steps and the time taken by CFS subjects for each step was more than that taken by control subjects. As a consequence velocity and relative velocity were reduced and cadence was increased in those with CFS. ANOVA showed that, with one exception, there were no statistically significant differences between time points for any of the gait parameters after exercise. This would suggest that the period of exercise did not affect
  • 5. L.M. Paul et al. / Gait and Posture 14 (2001) 19–27 23 Fig. 1. Dispersion for CFS patients (black bars) and control subjects (white bars) before, immediately after, and at various time points following the Sub-Anaerobic Threshold Exercise Tolerance test. (a) Dispersion in the anteroposterior (X) direction with eyes open; (b) Dispersion in the anteroposterior (X) direction with eyes closed; (c) Dispersion in the mediolateral (Y) direction with eyes open; (d) Dispersion in the mediolateral (Y) direction with eyes closed; (e) Total dispersion with eyes open; (f) Total Dispersion with eyes closed. All values are mean9standard error, n=10 in each group.
  • 6. L.M. Paul et al. / Gait and Posture 14 (2001) 19–2724 the gait pattern of either the CFS or control group. The exception was single support time on the right where there was a statistically significant interaction between CFS/control and time point (P=0.044). However, the CFS/control differences did not follow any obvious pattern with time elapsed following exercise. There is no apparent explanation for this isolated effect and it may be due to chance given the marginal P-value. 3.3. Heart rate and ratings of percei6ed exertion (RPE) scores during exercise All CFS and control subjects were able to complete the exercise protocol. Fig. 2 shows the mean heart rate and Fig. 3 the mean RPE scores taken during each minute of the exercise period. Both responses were analysed using ANOVA where fixed effects were sub- ject group (CFS or control) and time point, and matched pairs were included as a random effect. The heart rate response of both the CFS and control group were similar (Fig. 2) and this was confirmed by ANOVA. The increasing trend in heart rate was statis- tically significant (PB0.001) but the difference between subject groups, averaged over time, was not (P= 0.230). In addition the interaction between time point and subject group was not statistically significant (P= 0.789). The mean RPE scores, however, were very different in the two groups (Fig. 3) and ANOVA demonstrated that there was a statistically significant difference be- tween the two groups averaged over time points (PB 0.001). The difference between the CFS and control groups in the slope of the trend lines was also statisti- cally significant (PB0.001). Therefore, although the physiological response to exercise appeared similar in both groups, as demonstrated by the heart rate re- sponse, the CFS group perceived the workload to be significantly greater. 4. Discussion The results of the present study demonstrate that there was no significant difference in postural stability between CFS and control subjects as evidenced by differences in dispersion under eyes open and eyes closed conditions (Fig. 1), and thus do not support the suggestion that patients with CFS display some degree of dysequilibrium [2,9]. Whilst exercise does affect pos- tural stability to a significant extent, it does so for both patients and controls and there is no significant differ- ence in the degree of impairment observed between the two groups. Some studies have previously demon- strated balance problems in patients with CFS [10,11] however, these abnormalities were non-specific and were observed mainly in subjects who presented with pre-existing balance problems. The present results sug- gest that balance abnormalities, either at rest or after Fig. 2. Heart rate response to exercise in CFS patients (white circles) and control subjects (black squares). Values are mean heart rate9standard error, n=11 in each group. There was no significant difference between CFS patients and control subjects at any of the time points during the exercise test.
  • 7. L.M. Paul et al. / Gait and Posture 14 (2001) 19–27 25 Fig. 3. Ratings of perceived exertion-RPE (Borg Scale) during the exercise test for CFS patients (white circles) and control subjects (black squares). Values are mean RPE scores9standard error, n=11 in each group. The RPE scores of the CFS patients were significantly higher than those of the control group at all time points during the exercise test (PB0.001). exercise, are not a feature of the general population of CFS patients. It has been reported that postural sway, measured in a stance position on a fixed force plate, may be normal in the presence of many postural defects [26] and it may be that the static balance tests employed in the current study are not sensitive enough to detect subtle balance abnormalities which may exist in these subjects. It is hoped, in future research, to employ more dynamic balance tests in order to observe if these reveal more minor postural deficits which may exist. The results of the gait analysis show that CFS pa- tients demonstrate significant differences in many gait parameters compared to control subjects (Table 2). These differences are seen pre- and post-exercise, al- though exercise does not exacerbate the effects in the CFS patients. Only two of the measured gait parame- ters — single support time on the left and double support time — were not significantly different between the CFS and control groups. These observations would support the clinical impression that CFS subjects walk more slowly and with smaller steps compared to normal control subjects, and are consistent with slower move- ments and reaction times observed in CFS patients [27]. Data relating to step width was also collected but, because of the technical specification of the walkway, this parameter was deemed to have too much associ- ated measurement error and thus this data was not formally analysed. The results of the present study contrast with those of Boda et al. [13] which did not demonstrate any significant difference in walking times between CFS patients and controls. However, the Calmat computer- ised walkway used in the present study may allow for more accurate timings of gait parameters than in previ- ous studies. The smaller step length observed in the current study is consistent with the findings of Boda et al. [13], who demonstrated that the degree of hip and knee movement was less in subjects with CFS, and suggested that this may be an attempt to improve overall stability during the gait cycle. Saggini et al. [16] reported no difference in gait parameters between CFS patients and controls before exercise but did demon- strate some spatial and temporal abnormalities follow- ing exercise. However, the lack of a sedentary control group precludes any useful comparison with the present study. This is considered to be a vital requirement in selecting control subjects for studies involving CFS patients due to the deconditioning effect of the disorder [17]. The present study did use sedentary controls and the results would therefore suggest that CFS patients, similar to controls, do not have any significant alter- ations in gait after exercise. Gait changes may occur in CFS subjects as a result of balance problems, peripheral neuromuscular dys- function or abnormalities in the higher central nervous system, acting either individually or in combination
  • 8. L.M. Paul et al. / Gait and Posture 14 (2001) 19–2726 [13]. The results of the current study suggest that balance problems may not be a contributory factor to gait abnormalities since double support time in the CFS subjects was not significantly different from controls (although the differences did approach significance), and static balance was not significantly affected in CFS patients. We have previously demonstrated that there is reduced voluntary muscle force in the quadriceps mus- cle in CFS patients [22], which may contribute to observed initial reductions in step length, cadence and velocity in these patients. Fifteen minutes of sub-anaer- obic exercise did not exacerbate the abnormal gait parameters in the present study however, and therefore does not support the anecdotal evidence that symptoms of CFS, as evidenced by gait changes, are affected by a period of sub-maximal exercise. This suggests that CFS patients may be able to participate in light, sub-anaero- bic exercise protocols without detrimental effects on their gait or balance. This observation may therefore be useful for health-care professionals wishing to educate CFS patients on an appropriate level of exercise to reduce the possible effects of deconditioning without leading to worsening of symptoms [28]. The heart rate responses to exercise show that both the CFS patients and the control subjects were exercis- ing at similar physiological workload, since the steady state heart rate achieved after 3 or so minutes was not significantly different between the two groups, being approximately 125–130 beats per min (Fig. 2). This heart rate also confirms that subjects were exercising at a fairly light intensity, well below anaerobic threshold. It may be that exercising at a higher intensity would have produced more demonstrable effects on the gait abnormalities observed post-exercise. Despite the fact that the CFS patients were exercising at a clearly sub-maximal level, which was not signifi- cantly different from the control subjects, the patients reported a significantly greater perception of effort, reflected in a mean RPE rating of 16 towards the end of the exercise period compared to a mean rating of about 10 for the control group (Fig. 3). This rating for the control group more accurately reflects the actual physi- ological load undertaken by the subject. However, the patient group obviously perceives this workload to be much higher than it actually is. The RPE rating sug- gests that the patients were working at close to maximal levels, whilst the heart rate data demonstrates that they were well below this level. This may be due to an increased sense of effort [19,29] possibly linked to alter- ations in 5-hydroxytryptamine (5HT) levels in the brain [30] and increased sensitivity of the 5HT receptors [31], or to a degree of hyperalgesia within the muscles them- selves [32]. Since ratings of perceived exertion are often used in many areas of rehabilitation to allow patients to monitor their workload, the results of the present study would suggest that this is inappropriate in CFS patients. 5. Conclusion In conclusion, the results presented here would sug- gest that balance problems are not a consistent feature in CFS patients. However, more dynamic assessments of this patient group are required. CFS patients do tend to walk with an altered gait pattern compared to nor- mal controls and this concurs with the general notion that these patients have slower movements than nor- mal. This finding would suggest that gait analysis may be a useful outcome measure with which to monitor the progress of the disease or to determine the effectiveness of treatment interventions, therapeutic or pharmacolog- ical. Patients with CFS perceive the exercise load to be considerably higher than the actual physiological load thus the use of the RPE scale would not be a valid method of monitoring exercise intensity in this group. Acknowledgements This research was supported by grants from Action for ME and Women of Scotland Luncheon. Apprecia- tion is extended to the technical staff within the depart- ment of Physiotherapy, Podiatry and Radiography at Glasgow Caledonian University with particular thanks to Danny Rafferty and Gail Mackie. We are grateful to Professor PO Behan for his co-operation and assistance and to Dr Gordon Parish for his help and support. References [1] Majeed T, Behan PO. Clinical overview of chronic fatigue syn- drome. J Immunol Immunopharmacol 1995;145:8–14. 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