MEASURING
OXYGEN COST DURING LEVEL WALKING IN INDIVIDUALS WITH ACQUIRED BRAIN
INJURY IN THE CLINICAL SETTING
|
1Movement Science Group,
School of Biological and Molecular Sciences, Oxford Brookes University,
UK.
2Exercise Science Group, School of Biological and Molecular Sciences,
Oxford Brookes University, UK.
3School of Health Science, University of Birmingham, Birmingham,
UK.
4Oxford Centre for Enablement, Nuffield Orthopaedic Centre, Oxford,
UK.
| Received |
|
23 September 2004 |
| Accepted |
|
04
March 2004 |
| Published |
|
01
June 2004 |
©
Journal of Sports Science and Medicine (2004) 3, 76-82
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| ABSTRACT |
| This
study examined the test-retest reliability of oxygen cost (ml·kg-1·min-1)
during level walking in individuals with acquired brain injury (ABI).
Ten individuals with ABI (5 men, 5 women) (Traumatic brain injury,
1, central pontine myelinolysis, 1, stroke 8) and 21 healthy controls
(11 men, 10 women). Measurements of gross and net (walking minus resting)
oxygen consumption (ml·kg-1·min-1), and oxygen cost (ml·kg-1·min-1)
during level walking at self-selected speeds. Measurements were taken
on two occasions within one week. Oxygen cost was significantly lower
(p < 0.05) in individuals with ABI on the second test versus the
first test. Percentage variability in oxygen cost from test to re-test
ranged from 14.7 to 17.3% in the control group and from 17.4 to 20.8%
in the brain injury group. Clinical populations may demonstrate a
significant decrease in oxygen cost between testing occasions. Individuals
require at least one period of familiarisation if oxygen cost is used
as an outcome measure during level walking in clinical groups. The
amount of familiarisation has yet to be investigated in individuals
with ABI.
KEY
WORDS: Oxygen consumption brain injury, test re-test, level
walking.
|
| INTRODUCTION |
|
Pathology
that interrupts the normal energy conserving characteristics of
trunk and limb motion during the gait cycle may increase energy
expenditure during walking (Ralston, 1965;
Corcoran et al., 1970;
Inman et al., 1981;
Mattsson and Brostrom, 1990;
Hanada and Kerrigan, 2001).
One of the main aims of rehabilitation is to enable individuals
to walk safely and quickly in an energy efficient style that is
not excessively fatiguing (Kerrigan, 2001).
The energy cost of walking is usually determined by oxygen consumption
measures that are considered the criterion measure of internal work
during sub maximal exercise (Boyd et al., 1999). An increase in
energy expenditure, for walking a set distance, has been reported
in individuals with acquired brain injury (Zamparo et al., 1995;
Bernardi et al., 1999;
Waters and Mulroy, 1999).
Zamparo et al (1998)
reported decreases in energy cost (J·min-1·kg-1)
and Mattson (1990) decreases in oxygen cost (ml·kg-1·min-1)
of 5-17% during walking, as a result of treatment interventions.
However, no familiarisation session was reported in either of these
studies. When considering the findings, of such non-controlled intervention
studies it is interesting that there is little published data on
the test-retest reliability of oxygen cost during level walking
at self-selected speeds in clinical groups. The limited evidence
available in both healthy and clinical populations during level
walking suggests that oxygen cost at self-selected walking speeds
may vary from test to test (Corcoran et al., 1970;
Rieper et al., 1993;
Bowen et al., 1998).
For example, individuals with cerebral palsy recorded a percentage
variability from day to day of around 13% when level walking (Bowen
et al., 1998).
Closer test, re-test data has been reported in non-neurological
groups such as healthy volunteers and cardiac patients with a coefficient
of variation (CV) of less than 2% (Linnarsson et al., 1989)
and adolescents (CV 4.3%) (Rieper et al., 1993).
Intra-individual repeatability of oxygen consumption during treadmill
walking, has shown coefficients of variation as large as 15% in
women aged 20-65 years (Astrand, 1960)
and in adolescents (Wergel-Kolmert and Wohlfart, 1999).
A recent study of same day testing repeated under standard conditions
within a 30 minute period, in individuals with stroke, reported
moderate repeatability (da Cunha et al., 2003).
In practice, testing during intervention studies is carried out
on separate testing occasions and so knowledge of day to day or
test; re-test variation has clear clinical relevance. To date no
study has examined test, re-test data for oxygen consumption on
separate occasions in individuals with brain injury. In order to
make meaningful interpretation of therapeutic interventions it is
important to consider how repeatable oxygen consumption measures
are in this group.
The aim of this study was to examine test-retest reliability of
oxygen cost (ml·kg-1·min-1) during self-selected
walking in healthy controls and individuals recovering from brain
injury.
|
| METHODS |
|
Participants
Ten individuals with brain injury (5 men, 5 women) (traumatic brain
injury, 1, central pontine mylenosis, 1, stroke 8) and 21 healthy
controls (11 men, 10 women), age (years) mean ± SD: ABI 47.3 ± 18.0;
Control 35.1 ± 20.5. Individuals had a weight (kg) mean ± SD: ABI
78.1 ± 14.8, Control 74.9 ± 14.1; BMI (kg·m-2) mean ±
SD: ABI 27.94 ± 5.34, Control 24.6 ± 3.23. Individuals with ABI
were identified through consultant referral in a rehabilitation
centre. Consecutively referred individuals with acquired brain injury
scoring 7/15 or more on the Rivermead Mobility Index, who were able
to walk for 4 minutes and who had residual gait abnormalities, were
included. A heterogeneous sample was chosen in order to examine
reliability in a typical cohort of individuals receiving physiotherapy
in a rehabilitation centre. Healthy volunteer controls, with no
musculoskeletal or neurological pathologies, were recruited locally
from a sample known to the researchers.
Body mass was measured to the nearest 0.1 kg using a Seca weight
scale, wearing minimum clothing and without shoes. Height was measured
to the nearest 0.5 cm using a standard Seca stadiometer. Body mass
index (BMI) was calculated by dividing body weight in kilograms
by the square of body height in metres.
Informed consent was obtained, after receiving both oral and written
information about the study, from all individuals before participation
according to the Declaration of Helsinki (World Health Organisation,
1996). After
giving informed consent, individuals attended for testing. Subjects
were asked to refrain from the consumption of alcohol, cigarettes,
food, caffeine, medical drugs and to avoid exercise for a period
of two hours prior to testing. Findings from a pilot study and local
ethical committee concerns dictated that this period of abstinence
was both feasible and acceptable. Testing was carried out utilising
the following standardised testing protocol by the same two investigators,
at the same time, on two separate occasions within one week (room
temperature, 20-25oC). Individuals were asked to attend
wearing the same shoes. Information was recorded about age, height,
weight, compliance with pre-test requirements, physical activity
levels, medication, and general health.
Measurements of expired air were taken at rest and during level
walking at a constant walking speed. The expired air was collected
by means of light weight respiratory valves and hoses in a 100 litre
Douglas bag (Waters et al., 1988).
Individuals were initially familiarised to wearing the Hans Rudolf
face mask and then rested supine for a period of six minutes, immediately
followed by measurement of expired air for a further period of six-minutes.
The composition of the expired air was determined by oxygen and
carbon dioxide analysers (Servomex Series 1400, Crowborough, East
Sussex, UK) and the volume of expired air was determined by means
of a dry gas meter (Harvard Apparatus Limited, Edenbridge, Kent).
The gas analysers were calibrated at each testing occasion by means
of gas mixtures of known concentration. Oxygen consumption was calculated
using standard open circuit methodology and the values expressed
under standard conditions (STPD).
The walking test was explained verbally and demonstrated to each
individual. Subjects were then asked to walk at their normal, comfortable
walking speed around a predetermined 13m track in a physiotherapy
gymnasium. Self-selected walking speeds have been shown to coincide
with the lowest oxygen cost (ml·kg-1·min-1)
on the oxygen cost /walking velocity curve (Walters et al, 1988).
Pilot work showed that the clinical group examined in this study
could only manage to walk at one speed. During walking trials individuals
were accompanied by a researcher to ensure safety. Their self-selected
walking speed was determined with a calibrated speedometer (Cat
eye-astrale, Osaka, Japan) mounted on a wheelchair pushed behind
and out of sight of the subject by a researcher (Linnarsson et al.,
1989). To ensure
physiological steady state conditions all subjects walked for four
minutes in total. During the walking tests, the researcher continuously
monitored walking speed. Expired air was collected in a100-litre
Douglas bag, secured to the wheelchair, during min 3-4 of the walk
using light weight ducting and a respiratory valve for the determination
of oxygen consumption. Steady-state oxygen uptake was expressed
as gross (walking) and net (walking minus resting) (ml·kg-1·min-1).
From the steady-state oxygen uptake (ml·kg-1·min-1),
the oxygen cost (ml·kg-1·min-1) was calculated
from the mean walking speed during the 60 second sampling period.
Baseline walking measures were compared between ABI and Control
using a Student's t-test for independent data. To analyse the repeatability
between the measurements of oxygen consumption a plot was made of
the differences between the measurements against their mean (Bland
and Altman, 1996).
The data was tested for normality (Shapiro-Wilks test) and equal
variance (F-test). Pearson product moment correlation analysis
was performed on the absolute differences between measures taken
from test one and two against mean values of the two tests in order
to examine heteroscedascity of the data (systematic relationship
of size of difference between tests and the mean of the two tests).
No heteroscedascity was detected in the data, therefore the mean
of the differences between test 1 and 2 was calculated for measures.
The hypothesis of zero bias was then tested using a Student's t-test
for dependent data. A significance level of p
0.05 was chosen to indicate statistical significance. The upper
and lower limits of repeatability were calculated as differences
of the mean ± 1.96 SD and reported as bias and random error. Repeatability
between test 1 and 2 was further examined using the commonly used
intraclass correlation coefficient (ICC) [3, 1]. Finally in order
to enable direct comparisons with earlier studies, 'percentage variability'
was calculated (averaging the absolute value of the difference between
each measurement of the test, dividing this by the average for the
tests, and multiplying by 100) (Bowen et al., 1998).
|
| RESULTS |
|
Table
1 shows baseline measures for walking speed and oxygen consumption
during level walking in the control and ABI group. Independent,
one tailed, unequal variance t-tests revealed that the ABI group
walked slower (t (11.5) = 6.08, p < 0.05) with higher net oxygen
cost (t (8.3) = 3.35 (p < 0.05) than the control group. There
was no significant difference in net oxygen consumption per minute
between ABI and control groups (t (17.6) = 1.6, NS).
The intra-individual variance
Systematic bias
Both groups walked slightly faster on test 2 compared with test
1 (NS) (Table 2). Oxygen consumption
(ml·kg-1·min-1) (gross and net) was lower in test 2 compared with
test 1 in the ABI group (NS). The oxygen cost of ambulation (ml·kg-1·min-1)
was significantly lower in test 2 compared with test 1 in the ABI
group only (Table 2). In the
control group oxygen consumption was higher and oxygen cost lower
on test 2 (net and gross) (NS) (Table
2). There was less systematic error in net compared with gross
oxygen cost (ml·kg-1·min-1) of walking in both control and ABI groups
(Table 2).
Random error
The control group showed greater random error, percentage variability
and ICC [3,1] than the ABI group in oxygen consumption (ml kg-1·min-1) (Table 2). In contrast
the ABI group showed greater random error and percentage variability
than the control group in oxygen cost (ml·kg-1·min-1) (Table
2).
The high variability and small sample size within the ABI group,
may have increased the ICC [3,1] in this group in measures of oxygen
cost and walking speed (Table 2).
ICC 's of the intra-individual reliability ranged from moderate
to high in all measures except for gross oxygen cost in the control
group, which was low (Munro, 1993).
Net measures, showed less random error than gross measures in both
groups.
|
| DISCUSSION |
Individuals
in the control group walked around the indoor track for a period of
four minutes at self-selected speeds of 1.25 m·s-1 ± (SD)
0.15. Individuals in the ABI group walked at slower speeds of 0.61
m·s-1 ± 0.30 (p < 0.05). The self-selected speeds of
the control group were within the expected range for healthy walkers
(Waters et al., 1988).
The ABI group walked at speeds expected for this clinical group (Zamparo
et al., 1995).
The high inter- individual variability, in the ABI group, in self-selected
walking speed and oxygen cost reflects the wide range of physical
impairments affecting walking. The controls walked faster with lower
oxygen cost than the ABI group who walked slower at a greater oxygen
cost. This is in agreement with earlier studies that have recorded
high oxygen cost during level walking in individuals with brain injury
(Zamparo et al., 1995;
Bernardi et al., 1999;
Waters and Mulroy, 1999).
Intra-individual reliability
Walking speed did not change from the first to the second test in
either the control or ABI groups. There was no significant change
in either oxygen consumption or oxygen cost (gross and net) in the
control group. Our findings in the control group agree with earlier
studies that have found no significant difference in day to day testing
in either speed or oxygen consumption (Linnarsson et al., 1989;
Wergel-Kolmert and Wohlfart, 1999).
In contrast there was a significant reduction in oxygen cost, on the
second test in the ABI group (p < 0.05). The significant reduction
in oxygen cost in individuals with brain injury, recorded in test
2 may be due to a greater effect of familiarisation with the testing
equipment and procedures in this group.
Intra-class correlation coefficients of oxygen
consumption, from test 1 to test 2 in both the control and clinical
group, were rated as moderate to high ICC [3,1](Munro, 1993).
In our study the percentage variability of oxygen measures ranged
from 10-20%. Similar levels of percentage variability have been reported
for healthy women (15%; Astrand, 1960)
and for individuals with cerebral palsy (13%; Bowen et al., 1998)
during level walking. Less variation, together with higher levels
of reliability have been reported in non-neurological groups such
as healthy volunteers and cardiac patients (CV < 2%) (Linnarsson
et al., 1989)
and adolescents (CV 4.3%) (Rieper et al., 1993).
Certainly a high level of day-to-day variability in behaviour in individuals
with neurological
impairments is not unexpected after brain injury (Dawes, 2001).
The level of test, re-test variability reported in this study is similar
to the percentage reduction in energy cost (17%) recorded as a result
of treatment, in a study by Zamparo et al (1995).
Oxygen cost
Both groups showed less variation when net oxygen cost values were
used. This agrees with earlier studies in healthy individuals, which
reported lower variability when oxygen consumption measures during
walking were reported as net values (Baker et al., 2001).
Net values take into consideration changes in the testing condition,
such as variation in environmental factors and personal routines.
In our study we attempted to control individual behaviour for a period
of two hours prior to testing. This period of time was considered
the minimum required to standardise pre-test conditions that was feasible
within the rehabilitation setting. Earlier studies in this clinical
group have found controlling behaviour very labour intensive, requiring
full time supervision (Dawes, 2001).
Studies measuring oxygen consumption to examine the effectiveness
of treatment interventions in individuals with ABI, have not described
in detail pre-test conditions (Corcoran et al., 1970;
Mattsson et al., 1990;
Zamparo and Pagliaro, 1998).
As lowered oxygen cost of walking has been used as an outcome measure
of successful rehabilitation in these studies, the importance of testing
rigor in standardising conditions, and care with subject familiarisation
must be emphasised.
Walking speed
Although no significant changes in walking speed were recorded in
this study, the confounding variable of differing walking speeds when
testing individuals during self-selected level walking in repeated
measures designs needs careful consideration. Attempts to control
walking speed during testing may lead to altered style, which in turn
may affect oxygen consumption, and so is not ideal. During pilot work
different attempts to control walking speed by auditory feedback appeared
to affect spatio-temporal characteristics (Dawes et al., unpublished
data). These difficulties may have encouraged other researchers to
study walking utilising motorised treadmills, despite the lack of
ecological validity. The study of 'free' level walking is important,
as walking style measured during level walking differs from that observed
during treadmill walking (Dingwell et al., 2001).
Certainly further consideration of the optimal means of controlling
speed during level walking is required.
|
| CONCLUSIONS |
The
ABI group walked slower than the healthy controls consequently using
less oxygen per minute, but at a greater oxygen cost for every metre
walked. In both groups, there was less variation, from day to day,
when oxygen cost was reported as net values - supporting the use of
net oxygen cost as an outcome measure. There was a significant decrease
in oxygen cost on the second test in the ABI group. This fall, presumably
as a result of familiarisation, was similar to the previously reported
reduction in the oxygen cost of walking as a result of therapeutic
interventions. Considering the significant reduction in oxygen cost
in our ABI group when walking at self-selected speeds; one off measurements
before and following an intervention in studies with no control group
may lead to spurious interpretation of results. Further investigation
of the number of familiarisation periods is required but certainly
studies should ensure at least one period of familiarisation when
using novel testing procedures in this clinical group. Intervention
studies should ensure that there is a control group until there is
a greater understanding of the degree of familiarisation required.
|
| ACKNOWLEDGMENTS |
| This
study was funded by Oxford Brookes University, University of Oxford
Department of Primary Care. Ethical approval was granted by Oxfordshire
Applied and Qualitative Research Committee (AQREC). |
| KEY
POINTS |
|
Individuals
with brain injury during level walking
- May
demonstrate a significant decrease in oxygen cost between testing
occasions.
- May
require at least one period of familiarisation if oxygen cost
is used as an outcome measure
- The
degree of familiarisation required in this clinical group needs
further investigation
|
| AUTHORS
BIOGRAPHY |
Helen DAWES
Employment: Senior lecturer
Degree: PhD
Research interests: Movement science in rehabiiltation
Email: hdawes@brookes.ac.uk |
|
Johnathen COLLETT
Employment: PhD student
Degree: Bsc
Research interests: Gait |
|
Roger RAMSBOTTOM
Employment: Senior lecturer
Degree: PhD
Research interests: Exercise physiology |
|
Ken HOWELLS
Employment: Principal lecturer
Degree: PhD
Research interests: Movement Science |
Cath SACKLEY
Employment: Professor of Rehabilitation
Degree: PhD
Research interests: Rehabilitation |
Derick WADE
Employment: Consultant and Professor of Neurorehabilitation
Degree: MD
Research interests: Neurological rehabilitation |
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