Multiple
Sclerosis
http://msj.sagepub.com/
Can aerobic treadmill training reduce the effort of walking and fatigue in people with multiple sclerosis:
a pilot study
M A Newman, H Dawes, M van den Berg, D T Wade, J Burridge and H Izadi
Mult Scler 2007 13: 113
DOI: 10.1177/1352458506071169
The online version of this article can be found at:
http://msj.sagepub.com/content/13/1/113
Published by:
http://www.sagepublications.com
Additional services and information for Multiple Sclerosis can be found at:
Email Alerts: http://msj.sagepub.com/cgi/alerts
Subscriptions: http://msj.sagepub.com/subscriptions
Reprints: http://www.sagepub.com/journalsReprints.nav
Permissions: http://www.sagepub.com/journalsPermissions.nav
Citations: http://msj.sagepub.com/content/13/1/113.refs.html
Downloaded from msj.sagepub.com at UNIV OF DELAWARE LIB on February 4, 2011
ARTICLE
Multiple Sclerosis 2007; 13: 113119
Can aerobic treadmill training reduce the effort of
walking and fatigue in people with multiple sclerosis:
a pilot study
MA Newman1, H Dawes2, M van den Berg3, DT Wade4, J Burridge5 and H Izadi6
Impaired mobility in multiple sclerosis (MS) is associated with high-energy costs and effort when
walking, gait abnormalities, poor endurance and fatigue. This repeated measures trial with
blinded assessments investigated the effect of treadmill walking at an aerobic training intensity in
16 adults with MS. The intervention consisted of 12 sessions of up to 30 minutes treadmill
training (TT), at 55 85% of age-predicted maximum heart rate. The primary outcome measure
was walking effort, measured by oxygen consumption (mL/kg per metre), during treadmill
walking at comfortable walking speed (CWS). Associated changes in gait parameters using the
‘Gait-Rite’ mat, 10-m time and 2-minute distance, and Fatigue Severity Scale were examined.
Following training, oxygen consumption decreased at rest (P/0.008), CWS increased (P /0.002),
and 10-m times (P/0.032) and walking endurance (P/0.020) increased. At increased CWS,
oxygen consumption decreased (P/0.020), with a decreased time spent in stance in the weaker
leg (P /0.034), and a greater stride distance with the stronger leg (P/0.044). Reported fatigue
levels remained the same. Aerobic TT presents the opportunity to alter a motor skill and reduce
the effort of walking, whilst addressing cardiovascular de-conditioning, thereby, potentially
reducing effort and fatigue for some people with MS. Multiple Sclerosis 2007; 13: 113 119.
http://msj.sagepub.com
Key words: energy cost; gait; multiple sclerosis; oxygen consumption; treadmill training
Introduction
The performance of everyday movements, motor
skills, appears to be influenced by the drive to
minimize metabolic energy expenditure. This is
observed during normal walking, with individuals
selecting comfortable walking speeds (CWS) that
coincide with the lowest energy (oxygen) cost on
the oxygen cost-walking speed curve [1,2]. Gaits
altered by disease are mainly linked to increased
costs, fatigue and restricted capacity [1]. People
with multiple sclerosis (MS) present with a range
of symptoms, but reduced mobility and fatigue are
key problems, with up to 85% of people with MS
reporting difficulty walking [3,4]. In individuals
with MS, walking effort as measured by oxygen
cost (CW: mL/kg per metre), has been shown to be
up to four times greater than in healthy individuals [5,6]. Even mildly-impaired people with MS
are found to have sedentary lifestyles, low cardiovascular fitness and muscle characteristics typical
of disuse [3,7 9]. These problems are likely to
1
Physiotherapy Research Unit, NOC NHS Trust, Oxford, OX3 7LD, UK
Department of Clinical Neurology, University of Oxford Movement Science Group, School of Biological and
Molecular Sciences, Oxford Brookes University, Headington, Oxford, OX3 0BP, UK
3
School of Health Sciences, University of Birmingham, Birmingham, B15 2TT, UK
4
Oxford Centre for Enablement, Windmill Road, Oxford, OX3 7LD, UK
5
School of Health Professions and Rehabilitation Sciences, University of Southampton, Southampton, SO17 1BJ, UK
6
Department of Mathematical Sciences, Oxford Brookes University, Oxford, OX33 1HX, UK
Author for correspondence: Dr H Dawes, Senior Lecturer and Associate Research Fellow, Department of Clinical
Neurology, Movement Science Group, School of Biological and Molecular Sciences, Oxford Brookes University;
Headington, Oxford, OX3 0BP, UK. E-mail: hdawes@brookes.ac.uk
Received 9 February 2006; accepted 30 May 2006
2
– 2007 SAGE Publications
10.1177/1352458506071169
Downloaded from msj.sagepub.com at UNIV OF DELAWARE LIB on February 4, 2011
114
MA Newman et al.
increase the relative effort of energy expensive
activities, such as walking, and compound limitations [1,3].
More recent evidence suggests that exercise,
such as cycling, aquatic and strength training,
may be helpful to individuals with MS [10 17].
Current consensus is that exercise does no harm
and may benefit an individual’s fitness, well-being
and strength, whilst reducing their pain and fatigue
[10 17]. Treadmill training (TT) has provoked
interest as an intervention for neurological conditions because it is a highly repetitive form of
gait training that promotes both specific practice
and use of systems concerned with walking [18],
and can provide an aerobic training stimulus.
Aerobic TT following stroke has been associated
with improved walking speed, endurance and energy efficiency [19 22], and in a pilot RCT for
people with MS, was well tolerated and improved
walking speed without increasing fatigue [23].
Whether exercise can reduce the effort required to
walk, as well as induce cardiovascular changes in
people with MS, has not been established, although
a single study that included four minimally-impaired people with MS reported no change in
oxygen cost after hydrotherapy [24].
We set out to investigate whether four weeks of
TT, which trains the motor skill of walking and is
designed to improve aerobic fitness, could reduce
the effort, as measured by oxygen consumption
of walking CW: (mL/kg per metre), for people with
MS with mild to moderate disability, and secondarily, to investigate the associated affects on temporo-spatial gait parameters, endurance and levels
of fatigue.
Methods and materials
Ethical approval for this study was granted by the
Local Applied Research and Ethics Committee.
From March to June 2003, 19 participants were
recruited in a non-consecutive manner, from a
regional neurological rehabilitation centre, community physiotherapists, and the local MS Society.
Participants were recruited if they had a confirmed
diagnosis of MS and could walk 10 m (using aids if
required) in B/60 seconds, could walk safely on the
treadmill without support from a therapist or
partial body weight support harness, and could
follow any safety or training instructions. Participants were excluded if they had a MS exacerbation
within the preceding eight weeks (determined by
interview and medical note review) or had comorbidities, such as unstable cardiovascular disease,
diabetes or lower limb arthritis, that might prevent
them safely participating in aerobic TT.
Procedures
This was a prospective, single-centre trial, with a
repeated measures design and blinded assessments.
Prior to any testing, participants were asked to
refrain from consumption of alcohol, cigarettes,
food and caffeine, and to avoid strenuous exercise
for 2 hours. After giving signed informed consent,
each potential participant completed a screening
assessment; details of medical history, therapy and
exercise routines were taken, they were asked to
identify their stronger leg and then completed the
Guy’s Neurological Disability Scale (GNDS) and
the Rivermead Mobility Index (RMI) to indicate
levels of disability and functional mobility [25,26].
Those who fulfilled all of the selection criteria were
recruited and then familiarized to all protocols. All
participants were then assessed immediately prior
to (baseline) and following the four-week training
intervention.
Expired air and heart rate (HR) were collected to
describe energy demands at rest and when walking.
Participants sat resting in a chair with arms while a
HR chest strap transmitter (Polar-Vantage 2000)
and facemask were applied. Expired air was gathered via light-weight respiratory valves and plastic
hoses into a 100-L Douglas Bag for 6 minutes, and
HR (beats/minute) was monitored every minute
until the last minute when three records were
made at 15, 30 and 45 seconds [27,28]. A submaximal treadmill test (Power jog 600) was then
completed at a self-selected comfortable walking
speed (CWS) for 4 minutes. To determine their CWS
[29], individuals walked at a range of speeds with
the treadmill display covered. To obtain steadystate conditions, participants walked for 3 minutes
before expired air and HR were collected for the
final minute [27].
For each test, gas analysers were calibrated, then
the temperature and volume of expired air collected
was measured using a dry gas meter (Harvard
Apparatus Ltd, Edenbridge, UK) and gas compositions determined by oxygen and carbon dioxide
analysers (Servomex 1400B4 O2/CO2 analyser,
Crowborough, East Sussex, UK) with values expressed in standard conditions (standard correction
for temperature, air pressure, humidity; STPD).
From these, measures were made of minute ventilation: V̇E (L/min) at rest, the rate of oxygen used per
unit of body weight over a given time at rest and
when walking: V̇O2 (L/min, mL/kg per minute), of
net (walking minus resting) V̇O2 (L/min, mL/kg per
minute), and of the oxygen cost of walking or
the net oxygen consumption per metre walked: Cw
(mL/kg per metre) [1,2].
On re-assessment after training, physiological
measures were completed again with one addition,
a sub-maximal treadmill test completed at the
Multiple Sclerosis 2007; 13: 113 119
Downloaded from msj.sagepub.com at UNIV OF DELAWARE LIB on February 4, 2011
http://msj.sagepub.com
Treadmill training and the effect of walking and fatigue
original CWS to permit direct comparison of effort
of moving at the same speed. After a short rest,
participants were asked to select their current CWS
[29]. If the speed was different from their original
CWS, participants then completed a second treadmill test at this new speed.
At all assessments, fatigue levels were monitored
using the Fatigue Severity Scale (FSS), and the 10-m
timed walk and 2-minute walk evaluated walking
speed and endurance [30,31]. Participants completed the FSS independently following a standardized explanation by the researcher [30]. The time
taken to walk 10 m over a straight track, and the
distance completed walking for 2 minutes around a
shuttle corridor track were recorded [31]. During
the first half of the 2-minute walk, participants
walked over a thin pressure-sensitive mat (GAITRite, SMS) and the following gait parameters
were recorded: cadence (steps/min), gait cycle
(GC) time, duty factor (foot contact time, calculated as a percentage of time in swing and stance
(%GC)), and stride length (cm) [32,33]. In all
walking tests, participants were asked to walk at
their usual CWS; testers walked behind to avoid
pacing and walking aids were used if required [34].
All participants received 12 sessions of supervised TT in a physiotherapy gymnasium, for up to
30 minutes on each occasion. As maximal exercise
testing was not practical, intensities were calculated
using age predicted maximal heart rate (APMHR).
Participants were encouraged to train above
55% APMHR, but prevented from training above
85% of APMHR [35]. Initial speed was based on
baseline CWS, and during training, participants
were allowed to rest when they wished, with a
maximum of three rests before stopping. Speed was
increased as directed by participants once they were
able to walk for 30 minutes continuously. To
monitor exercise intensity, HR, time, speed and
ratings of perceived exertion using the CR10-RPE
scale, were recorded [35].
Study sample characteristics were analysed using
descriptive statistics. Before undertaking repeated
measures analysis, one-tailed data was tested for
normality. Parametric paired sample t -tests were
used for measures of walking speed and endurance, and all other measures were analysed using
Wilcoxon’s signed rank test. Scores from familiarization were not included in the analysis as this
period was designed to decrease learning effects
on the dependent variable, but the stability of
measures was checked from familiarization to
baseline. All pre-training measures were compared
with all post-training measures. Data was analysed
with SPSS version 11.0, using a significance level
of P/0.05.
http://msj.sagepub.com
115
Results
Of the 19 participants, three dropped out for
reasons unrelated to training or to their MS, leaving
16 to complete training (Table 1 provides demographic data). All but two participants used a
walking aid, most used a single stick (43.7%). No
participant received other physiotherapy during
the study or in the four weeks before recruitment.
Nine did no exercise, but three attended a weekly
MS exercise class, two went swimming and two
swam and visited the gymnasium weekly. None had
used a treadmill in the past two years. During
training, participants spent a mean 310 minutes
(SD: 50.8, range: 207 360 minutes) walking on the
treadmill. Of this time, a mean 180 minutes (SD:
104, range 2 330 minutes) or 58.5% of possible
time was spent at aerobic intensities, as defined by
55 85% of APMHR.
Over-ground speed and endurance improved
significantly post-training. Mean 10-m time reduced from 15.6 seconds (SD: 5.6, range: 7.8 28.1
seconds) to 13.9 seconds (SD: 5.3, range: 7.5 27.0
seconds), P/0.016, and 2-minute walk distance
increased from a mean 88.2 m (SD: 32.2, range:
44.6 154.0 m) to 94.3 m (SD: 32.2, range: 55.2 156.1 m), P/0.020. The median FSS score reduced
from 30 points (IQR: 22 37) to 27.5 points (IQR:
12 32), but this change was not significant (P/
0.178).
Physiological measures
All metabolic and HR measures (resting and walking), from familiarization to baseline, were checked
for stability and no differences were found (P /
0.05). Pre- and post-training measures are presented
in Table 2. Expired air measures for one participant
at baseline were discarded due to a bag leak, and
one participant was unable to complete the second
treadmill test post-training, reducing sample sizes.
At baseline, a significant decrease in oxygen
consumption (mL/kg per minute) and minute
ventilation (L/min) was observed at rest without a
Table 1 Participants (n/16; 13 female and three male)
demographic and disability measures
Mean9/SD
Age (years)
53.69/8.67
Time since first symptoms 17.39/8.3
(years)
Height (cm)
168.29/9.49
GDNS (0 55)
RMI (0 15)**
Range
30 65
7 37
Median
54.5
16
154 185 167.2
7 19
13
7 14
12
GNDS, Guy’s Neurological Disability Scale; RMI, Rivermead
Mobility Index.
Multiple Sclerosis 2007; 13: 113 119
Downloaded from msj.sagepub.com at UNIV OF DELAWARE LIB on February 4, 2011
116
MA Newman et al.
Table 2 Oxygen costs, oxygen consumption and heart rate pre- and post-training
n
At rest
Weight (kg)
RER
/V̇O2 (mL/kg per
minute)
/V̇E (L/min)
HR (bpm)
Walking: original CWS
Gross V̇O2 (mL/kg per
minute)
Nett V̇O2 (mL/kg per
minute)
Cw (mL/kg per metre)
HR (bpm)
Walking: new CWS
Cw (mL/kg per
minute)
Pre-training
mean9/SD (range)
Post-training
mean9/SD (range)
95%
Confidence
P value interval
Difference
16 70.889/13.30 (47.80 92.10) 70.589/12.82 (48.60 91.60) /0.39/1.22
0.969/0.07 (0.85 1.15)
0.009/0.09
15 0.969/0.09 (0.79 1.20)
15 2.109/0.58 (1.19 3.03)
1.549/0.85 (0.58 3.89)
/0.539/4.80
0.34
0.89
0.01
15
16
5.699/1.29 (3.40 7.79)
749/8 (59 84)
4.619/1.74 (1.69 8.40)
719/10 (55 85)
/1.089/1.47
/2.399/4.80
0.01
0.06
/0.3 to 1.9
15
6.309/2.01 (3.66 10.14)
4.979/2.17 (1.94 11.38)
/1.319/1.96
0.03
/0.1 to /2.5
15
4.209/1.99 (1.15 7.11)
3.439/2.03 (1.36 9.79)
/-0.789/2.08
0.21
/0.2 to /0.9
15 0.3009/0.215 (0.10 0.79)
16
919/11 (72 107)
0.2619/0.183 (0.05 0.75)
869/12 (68 110)
/0.0449/0.131 0.23
/5.39/6.6
0.01
/1.5 to /9.1
14 0.3009/0.215 (0.10 0.79)
0.1479/0.831 (0.02/0.29)
/0.0959/0.133 0.02
0.0 to /0.2
Gross oxygen consumption: V̇O2 (mL/kg per minute); Nett (walking resting) oxygen consumption: V̇O2 (mL/kg per minute).
Oxygen cost of walking: nett oxygen consumption per metre walked: Cw (mL/kg per metre).
Wilcoxon’s signed rank test, P/0.05 significance level.
Discussion
We observed that four-weeks of aerobic TT resulted
in a reduction in resting metabolism, an increase in
walking endurance, a more normal temporo-spatial
gait pattern, increased self-selected walking speed
and a decrease in walking effort. Self-reported
fatigue was not significantly different. Training
appears to have benefited individuals by making
walking less energy expensive, as a result of both
lower resting metabolism and an ability to achieve
faster walking speeds. Even small savings in energy
for those with more restricted mobility could
be functionally important, eg, allowing activity
for a longer. In summary, our findings suggest
that aerobic TT could improve the motor skill of
walking and address cardiovascular de-conditioning, thereby potentially reducing effort and fatigue
for some people with MS.
The significant improvement in walking speed
agrees with the findings of increased speed and
Oxygen Cost of Walking
Self - Selected Speed
1.0
Oxygen Cost (ml/kg/m)
significant change in resting HR. When walking
at original CWS, gross oxygen consumption (mL/kg
per minute) also decreased significantly. However,
when resting values of oxygen consumption were
considered (walking resting oxygen consumption),
no change in nett oxygen consumption (mL/kg per
minute) was noted. The mean pre-training original
CWS was 0.62 mph (SD: 0.31, range: 0.3 1.30 mph). After training, the new self-selected
CWS was significantly faster (P/0.002) at a mean
1.05 mph (SD: 0.45, range: 0.50 2.10 mph). There
was no change in oxygen cost (mL/kg per minute)
at original CWS, but a reduction at the new CWS
(P /0.019); Figure 1 shows the CW (mL/kg per
minute) pre- and post-training in relation to comfortable walking speed and movement of individual
participants along the oxygen cost-walking speed
curve.
Table 3 shows the results of the gait parameters
examined, with significant differences seen in all
measures except cadence, duty factor as represented
by swing and stance of the stronger leg, and stride
length of the weaker leg.
Pre and Post Training
.8
.6
.4
.2
0.0
0.0
.2
.4
.6
.8
1.0
Speed m/sec
Pre training
Post training
Figure 1 Oxygen costs walking at self-selected CWS preand post-training.
Multiple Sclerosis 2007; 13: 113 119
Downloaded from msj.sagepub.com at UNIV OF DELAWARE LIB on February 4, 2011
http://msj.sagepub.com
Treadmill training and the effect of walking and fatigue
117
Table 3 Temporal-spatial gait parameters pre/post-training
Gait measure
Pre-training mean9/SD (range)
Post-training mean9/SD (range)
P value
Duty factor
% Time in swing (wk)
% Time in stance (wk)
% Time in swing (st)
% Time in stance (st)
Stride length (str)
Stride length (wk)
Cadence
339/9.3 (1.7 42.7)
679/9.3 (57.3 98.3)
33.59/5.1 (25.9 46.1)
66.59/5.1 (53.9 74.1)
98.79/21 (65.5 135.0)
98.69/21.9 (62 136)
929/21 (63 132)
369/4.5 (26.7 41.7)
63.89/4.5 (58.3 73.4)
33.39/7.1 (12.2 42.6)
66.69/7.1 (57.4 87.7)
104.09/21 (75.4 146.0)
103.29/21.5 (74.7 143.8)
919/17 (62 119)
0.03
0.03
0.90
0.10
0.04
0.06
0.76
endurance following TT after stroke [18 22], and
demonstrates a transfer of the training on a treadmill to improvements in over ground walking
performance. Faster walking and increased endurance are certainly clinically relevant, being associated with increased function and independence.
Improvements in endurance were relatively greater,
probably reflecting our training emphasis on walking for 30 minutes. Even though the training
protocol did not emphasize speed, mean 10-m
times reduced by 12%, a level equal to the reduction in mean 7.62 m walk time observed by
Rhomberg et al . [16], after six months aquatic
and strengthening exercise. As TT achieved this
improvement after only one month it may be that
TT, being more task specific, prompted more rapid
changes. Further ongoing investigations are needed
to clarify optimal training protocols. TT regimes
emphasizing speed following stroke have reported
particular improvements, but the suitability of
these for people with MS is uncertain. Fatigue
levels remained unchanged in common with other
research into exercise and MS [11 15], and suggest
the training regime was well tolerated.
The small, but statistically significant, reductions
in ventilation [/V̇E (L/min)] and gross oxygen consumption [/V̇O2 (mL/kg per minute)] at rest is an
intriguing and potentially important finding, with
implications for overall fatigue levels in this group.
With resting metabolic rate normally constant,
significant reduction post-training of such a
short duration was unexpected from the literature.
Ongoing test familiarization is a possible extraneous factor that may have shown such an effect,
although with pre-training values in V̇E and V̇O2
not significantly changing from familiarization to
baseline testing, ongoing familiarization changes
are unlikely.
Examining oxygen cost when individuals were
walking at post-training, self-selected speeds
showed significant reductions in walking effort,
even when resting changes were considered.
When individuals were made to walk at their pretraining self-selected speed, there was no reduction
in walking effort after training. Reductions in
oxygen cost were linked to participants walking
http://msj.sagepub.com
faster in a more optimal (lower oxygen cost) part of
the oxygen cost-walking speed curve, as CWS
was significantly faster post-training at a mean
of 0.43 mph (Figure 1). Individuals were able to
walk faster and further after training, with no
increases in fatigue associated with this increased
activity. Our findings agree with observations in
chronic stroke patients with aerobic TT reducing
sub-maximal oxygen consumption [19].
Although our sample was small and the evidence
from a repeated measures analysis is less powerful
than that of a RCT, this study of 16 participants is
larger than any other investigations about the
impact of exercise on CW in MS identified in the
literature [24]. We also recruited a sample of
participants that were on average older at 53.6
years and reported symptoms longer at 17.3 years
compared to Romberg et al . (43.8 and 9.7 years) and
other studies about exercise and MS [10 17].
Although no systematic analysis was made, higher
mean age and disease duration per se did not appear
to be barriers to exercise, supporting proposals that
exercise is also useful for older adults with MS [36].
A convenience sample was used, necessarily as
participants needed to be able to walk on a treadmill, but as such it may be unrepresentative of other
MS populations, eg, perhaps participants were more
motivated to exercise. However, no participant
reported changing their exercise routine or receiving any therapy during the study. The outcome
measures that were used have been demonstrated to
be reliable and were applied in the standardized
format, but no investigation of inter-rater reliability
was made. Further work would ideally use consecutive sampling and establish inter-rater reliability.
We did not measure actual mobility at home
or in the community, and the impact of TT on
daily life requires further investigation. Participants spent a mean 58% of time training above
aerobic thresholds, but their ability to achieve these
intensities varied widely. For some, weakness and
peripheral muscle fatigue may have limited training
before demand reached aerobic levels, for others
the training duration may have been insufficient. A
larger trial with a sample stratified by mobility level
could evaluate these aspects. Additionally, the
Multiple Sclerosis 2007; 13: 113 119
Downloaded from msj.sagepub.com at UNIV OF DELAWARE LIB on February 4, 2011
118
MA Newman et al.
presence of a physiotherapist and monitoring during training may have increased confidence and
motivation to exercise. This could particularly
influence factors, such as fatigue, that have links
to mood.
Conclusions
We found the exercise programme feasible and
well-tolerated in people with mild to moderate
MS. Such a programme is practical and could be
easily implemented in community fitness centres
where treadmills are freely available. Further investigation of optimal prescription and implementation in a more representative sample is warranted.
Acknowledgements
The authors would like to thank the Oxford Centre
for Enablement staff, the patients who volunteered
to take part in the study, and the Oxford MS group.
References
1. Waters RL, Mulroy S. The energy expenditure of
normal and pathologic gait. Gait Posture 1999; 9: 207 31.
2. Rose J, Ralston H, Gamble J. Energetics of walking. In
Human walking . Williams & Wilkins, 1994: 45 72.
3. White LJ, Dressendorfer RH. Exercise and multiple
sclerosis. Sports Med 2004; 34: 1077 100.
4. Morris ME, Vowels L, Dodd K. Changes in gait and
fatigue from morning to afternoon in people with multiple sclerosis. J Neurol Neurosurg Psychiatry 2002; 72: 361 65.
5. Olgiati R, Burgunder JM, Mumenthaler M. Increased energy cost of walking in multiple sclerosis: effect
of spasticity, ataxia, and weakness. Arch Phys Med Rehabil
1988; 69: 846 49.
6. Olgiati R, Jacquet J, Di Prampero PE. Energy cost of
walking and exertional dyspnea in multiple sclerosis. Am
Rev Respir Dis 1986; 134: 1005 10.
7. Ng AV, Miller RG, KentBraun JA. Central motor drive
is increased during voluntary muscle contractions in
multiple sclerosis. Muscle Nerve 1997; 20: 1213 18.
8. KentBraun JA, Ng AV, Castro M, Weiner MW,
Gelinas D, Dudley GA et al . Strength, skeletal muscle
composition, and enzyme activity in multiple sclerosis.
J Appl Physiol 1997; 83: 1998 2004.
9. Tantucci C, Massucci M, Piperno R, Grassi V,
Sorbini C. Energy cost of exercise in multiple sclerosis
patients with a low degree of disability. Mult Scler 1996; 2:
161 67.
10. Gehlsen G, Assmann N, Winant D, Seidle M. Gait
characteristics in multiple sclerosis: progressive changes
and effects of exercise on parameters. Arch Phys Med
Rehabil 1986; 67: 536 39.
11. Petajan JH, Gappmaier E, White AT, Spencer MK,
Mino L, Hicks RW et al . Impact of aerobic training on
fitness and quality of life in multiple sclerosis. Ann Neurol
1996; 39: 432 41.
12. Mostert S, Kesselring J. Effects of a short-term exercise
training program on aerobic fitness, fatigue, health
perception and activity level of subjects with multiple
sclerosis. Mult Scler 2002; 8: 161 68.
13. Rodgers MM, Mulcare JA, King DL, Mathews T,
Gupta SC, Glaser RM et al . Gait characteristics of
individuals with multiple sclerosis before and after a
6-month aerobic training program. J Rehabil Res Dev
1999; 36: 183 88.
14. Sutherland G, Andersen MB. Exercise and multiple
sclerosis: physiological, psychological, and quality of life
issues. J Sports Med Phys Fit 2001; 41: 421 32.
15. Surakka J, Romberg A, Ruutiainen J, Surakka J,
Aunola S, Karppi SL et al . Effects of aerobic and
strength exercise on motor fatigue in men and women
with multiple sclerosis: a randomized controlled trial.
Clin Rehabil 2004; 18: 737 46.
16. Romberg A, Virtanen A, Ruutiainen J, Aunola J,
Karppi S, Vaara SL et al . Effects of a 6-month exercise
program on patients with multiple sclerosis a randomized study. Neurology 2004; 63: 2034 38.
17. Gehlsen G, Grigsby S, Winant D. Effects of an aquatic
fitness program on the muscular strength and endurance
of patients with multiple sclerosis. Phys Ther 1984; 64:
653 57.
18. Manning CD, Pomeroy VM. Effectiveness of treadmill
retraining on gait of hemiparetic stroke patients. Systematic review of current evidence. Physiotherapy 2003;
89: 337 49.
19. Macko RF, Smith GV, Dobrovolny CL, Sorkin JO,
Goldberg AP, Silver KH et al . Treadmill training
improves fitness reserve in chronic stroke patients. Arch
Phys Med Rehabil 2001; 82: 879 84.
20. Pohl M, Mehrholz J, Ritschel C, Rückriem S. Speeddependent treadmill training in ambulatory hemiparetic
stroke patients: a randomized controlled trial. Stroke
2002; 33: 553 58.
21. Visintin M, Barbeau H, Korner-Bitensky N, Mayo
NE. A new approach to retrain gait in stroke patients
through body weight support and treadmill stimulation.
Stroke 1998; 29: 1122 28.
22. Sullivan KJ, Knowlton BJ, Dobkin BH. Step training
with body weight support: effect of treadmill speed and
practice paradigms on poststroke locomotor recovery.
Arch Phys Med Rehabil 2002; 83: 683 91.
23. Van den Berg M, Dawes H, Wade DT, Newman M,
Burridge J, Izadi H. Treadmill training for people with
multiple sclerosis; a pilot randomised trial. J Neurol
Neurosurg Psychiatry 2006; 77: 531 533.
24. Zamparo P, Pagliaro P. The energy cost of level
walking before and after hydro-kinesi therapy in patients
with spastic paresis. Scand J Med Sci Sports 1998; 8: 222 28.
25. Rossier P, Wade DT. The Guy’s Neurological Disability
Scale in patients with multiple sclerosis: a clinical
evaluation of its reliability and validity. Clin Rehabil
2002; 16: 75.
26. Vaney C. Assessing mobility in multiple sclerosis using
the Rivermead Mobility Index and gait speed. Clin
Rehabil 1996; 10: 216 26.
27. Linnarsson DE, Mattsson L, Eklof, Broman L,
Broman M, Brostrom LA et al . Determination of the
oxygen cost of level walking. Clin Physiol 1989; 9: 1 10.
28. Waters RL, Lunsford BR, Perry J, Byrd R. Energyspeed relationship of walking: standard tables. J Orthop
Res 1988; 6: 215 22.
29. Holt KG, Hamill J, Andres RO. Predicting the minimal energy costs of human walking. Med Sci Sports Exer
1991; 23: 491 98.
Multiple Sclerosis 2007; 13: 113 119
Downloaded from msj.sagepub.com at UNIV OF DELAWARE LIB on February 4, 2011
http://msj.sagepub.com
Treadmill training and the effect of walking and fatigue
30. Rossier P, Wade DT. Validity and reliability comparison of 4 mobility measures in patients presenting with
neurologic impairment. Arch Phys Med Rehabil 2001; 82:
9 13.
31. Krupp LB, La Rocca NG, Muir-Nash J, Steinberg
AD. The fatigue severity scale. Application to patients
with multiple sclerosis and systemic lupus erythematosus. Arch Neurol 1989; 46: 1121 23.
32. Menz HB, Latt MD, Tiedemann A, Mun San Kwan
M and Lord SR. Reliability of the GAITRite walkway
system for the quantification of temporo-spatial parameters of gait in young and older people. Gait Posture
2004; 20: 20 25.
33. McDonough AL, Batavia M, Chen FC, Kwon S and
Ziai J. The validity and reliability of the GAITRite
http://msj.sagepub.com
119
system’s measurements: a preliminary evaluation. Arch
Phys Med Rehabil 2001; 82: 419 25.
34. Guyatt GH, Pugsley SO, Sullivan MJ, Thompson P,
Berman LB, Jones NL et al . Effect of encouragement on walking test performance. Thorax 1984; 39:
818 22.
35. American College of Sports Medicine. Guidelines
for graded exercise testing and training. In Franklin BA,
Whaley MH, Howley ET eds. ACSM’s guidelines for exercise
testing and prescription , sixth edition. Lippincott Williams
& Wilkins, 2002: 368.
36. Eldar R, Marincek C. Physical activity for elderly
persons with neurological impairment: a review. Scand J
Rehabil Med 2000; 32: 99 103.
Multiple Sclerosis 2007; 13: 113 119
Downloaded from msj.sagepub.com at UNIV OF DELAWARE LIB on February 4, 2011