Thigh
muscle strength and endurance in patients with COPD compared with healthy
controls
Janaudis-Ferreira, Tania;
Wadell, Karin
; Sundelin, Gunnevi; Lindström, Britta.
Respiratory Medicine
100. 8 (Aug 2006): 1451-1457.
; Sundelin, Gunnevi; Lindström, Britta.
Respiratory Medicine100. 8 (Aug 2006): 1451-1457.
Abstract
(summary)
The aim of this study was to
evaluate thigh muscle strength and endurance
in patients with COPD compared with healthy controls. Forty-two patients (26
women; 16 men) with moderate to severe COPD and 53 (29 women; 24 men) age-matched
healthy controls participated in the study. The subjects were tested for
maximum voluntary contractions (MVC), endurance
and fatigue of the thigh muscles on an isokinetic dynamometer (KinCom ®
). Endurance was expressed as the number of
attained repetitions of knee extension and muscle fatigue as a fatigue index
(FI).
MVC in knee extension was 17% lower
in female patients () but no difference was found in male patients () compared
to controls. MVC in knee flexion was lower both in female (51%) () and male
patients (40%) () compared to controls. Both female and male patients had
significantly lower muscle endurance compared
to controls. Female patients had a higher FI (22.5%) than female controls (10%)
() while no difference was found regarding FI between male patients (15%) and
male controls (10%) (). The level of self-reported everyday physical activity
did not differ between groups.
The results showed impaired skeletal
muscle function in COPD, except for MVC in knee extension in male patients.
Female patients seemed to be more prone to decrease in thigh muscle function.
More focus on improving muscle strength and muscle endurance
should be considered when designing pulmonary
rehabilitation programs. Patients with preserved level of physical activity can
be included in exercise programs and gender-related differences should be taken
into account.
Full
Text
|
COPD patients ()
|
Controls ()
|
|||
|
Men ()
|
Women ()
|
Men ()
|
Women ()
|
|
|
Age (yr)
|
66±6
|
64±5
|
67±5
|
64±6
|
|
BMI (kg/m2 )
|
26±3
|
28±5a
|
25±3
|
25±2
|
|
PA score
|
3.47±0.8
|
3.30±0.7
|
3.63±1
|
3.36±0.7
|
|
FEV1(l)
|
1.5±0.40
|
1.2±0.24
|
||
|
FEV1% pred.
|
50±11.5
|
56±11
|
||
|
VC (l)
|
3.7±0.9
|
2.6±0.6
|
||
|
VC% pred.
|
92±15b
|
100±21
|
||
|
FEV1/VC%
|
40±12
|
45±9.5
|
||
|
(b) Significantly different from
female COPD patients ().
|
Table 1 - Characteristics of the
study population.
Data are presented as mean±SD.
BMI=body mass index; PA score=physical activity score
|
Men
|
Women
|
|||
|
COPD
|
Controls
|
COPD
|
Controls
|
|
|
Maximal strength in extension
(Newton)
|
274±83
|
289±70
|
225±61a
|
272±77
|
|
Maximal strength in flexion
(Newton)
|
121±51b
|
203±46
|
87±34c
|
179±47
|
|
Intercept (Newton)
|
243 (51-349)
|
271 (177-446)
|
198 (89-337)
|
230 (96-380)
|
|
Fatigue index (FI%)
|
15 (-222-27)
|
10 (-90-25)
|
22.5 (-39-33)c
|
10 (-54-25)
|
|
Borg ratings at 30th contraction
|
4 (2-10)
|
4 (0-9)
|
6 (2-10)c
|
3 (0-10)
|
|
(b) Significantly different from
male controls ().
(c) Significantly different from female controls (). |
Table 2 - Maximal strength of the
thigh muscles and fatigue during the 30 first contractions of the endurance test.
Data are presented as mean±SD for
maximal strength and as median (minimum-maximum) for intercept, FI and Borg.
Introduction
Exercise intolerance in patients
with chronic obstructive pulmonary disease
(COPD) contributes to a poor quality of life in these patients and an increased
need for medical assistance.1-3 This exercise limitation has
traditionally been explained by the impairment of ventilatory function.4
However, studies have suggested that many patients with COPD may stop
exercising because of leg muscle fatigue prior to ventilatory limitation.5,6
Furthermore, skeletal muscle dysfunction is common in patients with COPD and
might be explained by muscle atrophy, reduced oxidative metabolism, reduced
muscle capillarization and change in muscle fiber type, i.e., reduced
proportion of type I fibers and increased proportion of type IIb. 7,8
Inactivity is often assumed to be
one of the main reasons for these peripheral muscle abnormalities in patients
with COPD.9 Exercise training has been shown to improve muscle
function in patients with COPD, suggesting that deconditioning is an important
contributor to the skeletal muscle dysfunction.10-13 Coronell et al.14
showed that despite relatively preserved level of physical activity, patients
with COPD have reduced muscle function compared to healthy age-matched
controls, suggesting that other factors than inactivity may contribute to the
alterations in peripheral muscle function. These factors, related to the
disease, are suggested to be malnutrition, exposure to systemic
corticosteroids, tissue hypoxia, coexisting heart disease, systemic
inflammation, skeletal muscle apoptosis, oxidative stress, tobacco use,
individual susceptibility and hormone alterations. 4,8 In addition,
some authors have found elevated levels of inflammatory cytokines indicating
presence of systemic myopathy.15
The majority of the studies on
lower-extremity muscle function in COPD are focused on muscle strength rather
than muscle endurance. Furthermore, it is
still unclear which modality of physical training is the best to increase
muscle function in these patients. Defining whether patients with COPD have
reduced muscle strength and/or muscle endurance
compared to healthy controls is necessary in order to be able to find the best
exercise modality for these patients. The level of everyday physical activity
is important to assess when comparing skeletal muscle dysfunction in patients
with COPD with healthy controls. To our knowledge, there are not many studies
that have taken this issue into consideration. Moreover, to the authors'
knowledge, only Van't Hul et al. 16 have investigated gender-related
differences regarding muscle strength and endurance
of lower extremities in patients with COPD.
Our hypothesis is that peripheral
muscle abnormalities found in patients with COPD might lead to decrease in
muscle strength and endurance which
consequently results in increased muscle fatigability. The aim of this study
was thus (i) to determine whether patients with COPD have impaired strength and
endurance in the thigh muscles compared to
age-matched healthy controls, (ii) to investigate if the level of self-reported
everyday physical activity was decreased in patients with COPD and (iii)
whether gender-related differences in muscle performance exist compared to a
control group.
Material and methods
Study population
Forty-two patients (26 women and 16
men) aged 53-74 years with moderate to severe, stable COPD and 53 (29 women and
24 men) age-matched healthy controls were included in the study. The patients
were clinically diagnosed with COPD according to GOLD criteria17 and
recruited from outpatients on treatment at two Hospitals in Northern Sweden.
The inclusion criteria used to select the patients were FEV1/VC<0.7,
FEV1<80% of predicted, stable medication and no infection during the last
month before participating in the study, and absence of cardiac, orthopaedic, neurological
or psychological disorders. All patients performed an exercise
electrocardiogram test on a cycle ergometer (Rodby TM, RE 829, Enhörna, Sweden)
and a spirometry test (Spirolab, Medical International Research, Roma, Italy)
before entering the study. The patients were ex-smokers and none of them were
treated with long-term oxygen therapy. Thirty-three patients were using inhaled
corticosteroids and one used daily oral corticosteroids. None of them was
engaged in any organized physical activity before the study. The patients were
referred to the clinic to participate in a pulmonary
rehabilitation program and were tested, in addition to other tests, for muscle
strength and endurance. The healthy control
group was recruited from pensioner's associations in Umeå, Sweden. The controls
had to meet the following criteria: age between 53 and 74 and no presence of pulmonary, cardiac, orthopaedic, neurological or
psychological disorders. The controls should not have smoked in the last 10
years and should not be participants in any organized physical activity. All
subjects gave their informed consent before the study. The Research Ethics
Committee of Umeå University, Sweden approved the study (Um dnr 99-067).
One patient was not included in the
analyses because he did not understand the instructions and could not complete
the protocol. One subject in the control group dropped out because she admitted
she had pain in the hips during the tests. Two other control subjects were
excluded from the analyses of the endurance test
because of technical problems. Anthropometric data for patients with COPD and
controls are presented in Table 1.
Isokinetic tests
The tests were performed using an
isokinetic dynamometer (KinCom® , Chattanoga, IL) and the dominant
leg was evaluated. The test consisted of two different parts: maximal
contractions of the thigh muscles and an endurance
test. Standardized verbal encouragement and instructions were strictly applied
for both groups. During the measurements, the subjects were seated according to
the recommendation by the manufacturer. Before the experiment the subjects
performed a 5min warm up on a cycle ergometer (Monark 818E, ergomedic, Sweden)
with a light load. In order to become familiar with the test procedure the
subjects performed four knee extensions at an angular velocity of 60°/s on
KinCom ® . The subjects rested at least 2min before starting the
test.
The isokinetic dynamometers are a
valid and reliable method for assessing strength and endurance
of the thigh muscles.18-20 The protocol used for the tests has been
found to be reliable and has previously been used to evaluate muscle
performance in healthy young and elderly persons and patients with ischemic
stroke.21-23
Maximal voluntary contractions (MVC)
The subjects performed four
repetitions of maximal knee extension at 90°/s. They were instructed to extend
the leg four times in a row with maximal effort and to rest on the way back
(flexion phase). They rested at least 2min before performing the maximal
dynamic flexion.
Four repetitions of maximal knee
flexion were performed at 90o /s with a passive extension phase. The
subjects were instructed to flex the leg four times in a row with maximal
effort and to rest on the way back (extension phase). The subjects rested at
least 5min before the endurance test.
The highest mean force value
(Newton) of the four repetitions obtained in the isokinetic device for maximal
contractions in extension and flexion was chosen as the outcome measure.
Endurance test
The endurance
test consisted of maximally 100 maximal knee extensions at 90o /s.
The subjects were instructed to extend the leg as many times as possible and
the maximal effort in the extension phase was required. They were supposed to
continue until the test leader asked them to stop (when 100 repetitions were
attained) or, if less than 100, until exhaustion. No rest was allowed between
the passive flexion phase and the active extension phase. The 0-10 category
ratio scale by Borg (CR10) 24 was used to rate perceived exertion of
the thigh muscles throughout the 100 maximal contractions. The subjects rated
their perceived exertion at every fifth contraction until the 60th and,
thereafter, at every tenth contraction until exhaustion or at 100th repetition.
Muscle endurance
was expressed as the number of attained repetitions of knee extension. Muscle
fatigue was expressed as a fatigue index (FI) and was analysed using the first
30 contractions of the endurance test.
Level of self-reported physical
activity
A questionnaire, validated to
evaluate level of self-reported physical activity in healthy elderly people,
was applied.25 It has also been used for patients with COPD in a
previous study.13 This questionnaire concerns household activities,
leisure-time and sports activities during the previous 4 weeks. The level of
self-reported physical activity (PA score) was ranging from 1 to 6. Scores 1-2
were classified as low level of physical activity, scores 3-4 were classified
as medium level of physical activity and scores 5-6 as high level of physical
activity.
Data acquisition and statistics
Based on previous studies, the mean
force during the endurance test shows a
pattern with a steep decrease during the first 30-50 contractions (fatigue
phase) and, after that, a stable level (endurance
level).22 The reason we decided to evaluate fatigue only during the
first 30 contractions was because all patients with COPD succeeded to attain at
least this number of contractions. For evaluation of fatigue we formed a FI.
This index was a slight modification of the dimensionless index suggested by
Merletti. 26 To form the FI, the intercept (m ) from the
regression analysis of the initial 30 contractions of the endurance test was calculated for each subject. The
intercept represents the intial value of the endurance
test. From m and the force values of each individual, the FI was
calculated as[Formula omitted. See PDF]where X is mean force value, i
is the contraction number, and N is the number of contractions. Higher
values for FI indicate increased muscle fatigue. FI represents the relative
loss in mean force throughout the 30 first contractions and is presented in
percentage (%).
For statistical analysis the SPSS
version 11.5 for Windows was used. Tests of normality (Kolmogorov-Smirnov and
Shapiro-Wik) were used to check whether the data were normally distributed or
not. In case of normal distribution, independent parametric sample t
-test was used to compare the two groups. When data were not normally
distributed, as for FI, or data on ordinal level, as CR-10, the non-parametric
Mann-Whitney U -test was used to compare differences between groups.
Power was calculated when non-significant differences were found. The results
are presented as mean and standard deviation (sd) and median, minimum and
maximum values for parametric and non-parametric tests, respectively.
Results
Patients with COPD and healthy
controls were well matched for age and level of self-reported physical
activity. However, a significant difference was found regarding body mass index
(BMI) between female patients with COPD and female controls.
MVC in knee extension was 17% lower
() in female patients but no difference was found in male patients () compared
with controls (Table 2). The statistical power of this variable in males was
9%. MVC in flexion was 51% lower in female () and 40% lower in male () patients
compared with controls.
Muscle endurance
was lower in patients with COPD. All controls performed 100 repetitions in the endurance test while only 27% of the female patients
and 53% of the male patients were able to attain this number (Fig. 1). FI was
found to be higher in female patients with COPD (22.5%) compared to female
controls (10%) () (Fig. 2b and Table 2). No significant difference was found
regarding FI between male patients (15%) and male controls (10%) () (Fig. 2a
and Table 2). Both female patients and female controls started the endurance test with approximately 80% of what they
performed in the test of maximal contractions in extension. Male controls
started the endurance test at their maximum
force in extension while male patients began the test at approximately 80% of
their maximal force in extension (). Female patients rated higher perceived
exertion at the 30th contraction compared to female controls () while male
patients and male controls rated approximately the same perceived exertion at
the 30th contraction (Table 2).
Discussion
The major finding of this study was
that thigh muscle function is impaired in patients with COPD both in muscle
strength (except for extension in male patients) and muscle endurance compared to age-matched healthy controls.
However, the level of self-reported everyday physical activity did not differ
between groups. We also found gender-related differences in patients with COPD
regarding skeletal muscle dysfunction where women seem to be more prone to
decrease in thigh muscle function. There was a significant difference in BMI
between female patients and female controls, but this difference (25-28) is
probably not of clinical relevance that it could explain the results.
Maximal strength of the thigh
muscles was found to be impaired in our group of patients with COPD which
agrees with results of previous studies.14,16,27,28 This muscle
weakness may be related to the reduced muscle cross-sectional area (muscle
atrophy) previously reported in patients with COPD.8,29
Interestingly, we did not find any weakness of the thigh muscles in extension
in male patients compared to male controls. The reason for this relatively
preserved maximal strength in extension of male patients compared to controls
is not clear. The small sample of men with COPD might have contributed to this
finding. Because of the statistical power for this variable (strength in extension
in males) was 9%, we cannot affirm that this non-significant result really
exists.
We found that muscle endurance was impaired both in female and male
patients compared to controls. This finding is in accordance with results of
previous studies.9,14,16,30,31 . Also, female patients were found to
have greater degree of fatigue (FI) during the first 30 contractions of the endurance test compared to female controls, but this
was not the case in male patients. Our results differ from findings by Zattara-Hartman
et al. 32 who did not find any reduction in endurance
of vastus lateralis in patients with COPD compared to controls. Staron et al.33
studied muscle fiber-type composition of the vastus lateralis in healthy young
men and women and showed that the percentage area of the fast oxidative type
IIa fibers were the largest for men, whereas the percentage area of the slow
oxidative type I fibers were the largest for women. This may explain why we did
not find any difference in degree of fatigue (FI) during the first 30
contractions in male patients compared to male controls. Male subjects might
preferentially use a greater proportion of type IIa fibers and may, therefore,
not be affected to a great extent by a reduced proportion of type I fibers that
is present in chronic obstructive pulmonary
disease. Another reason might be that the subjects worked at different
intensities of their maximal force in extension during the endurance test, a difference that possibly could
have accounted for the observed difference. Male controls started the endurance test at their maximal force in extension
whereas male patients began the test at approximately 80% of their maximal
force in extension. Although this difference was not significant (), it might
have contributed to a greater fatigue of the control subjects during the 30
first contractions. However, despite the fact that we did not find any
difference in FI between male patients and male controls, the patients did not
manage to attain 100 repetitions which indicates impaired endurance of the thigh muscles.
In our study, the questionnaire used
to evaluate PA score between the two groups has been shown to be a good
instrument because it was developed for elderly people and the alternatives
were not only about sport and leisure-time activities but also about household
activities. 25 Although some subjects in our study cannot be
considered elderly, the average age of the groups was approximately 65 years
old. In the present study, the questionnaire showed that the patients and the
controls had the same score of level of self-reported physical activity and
thus no indication of a more sedentary lifestyle was found. In the patient
group our results showed impaired strength and endurance
of the thigh muscles despite their relatively preserved level of physical
activity. Coronell et al., 14 using another questionnaire, also
indicated that dysfunction in strength and endurance
of quadriceps can be found in patients with relatively normal level of physical
activity. This finding suggests that other factors than inactivity may
contribute to the alterations in peripheral muscle function in patients with
COPD. However, the PA questionnaire might be sensitive to determine differences
regarding what the patients perform, e.g. type, frequency and duration of
physical activity but not regarding how they perform the activity, e.g. which
intensity. A recent study 34 has showed that patients with COPD walk
with lower movement intensity compared to healthy controls. Despite the
preserved level of self-reported physical activity, we believe that these
patients might experience the exercise as more demanding than healthy controls.
Furthermore, female patients had greater degree of fatigue and rated higher
perceived exertion at the 30th contraction than female controls. Besides, the
main reported reason for the patients with COPD to stop the endurance test before completing 100 repetitions was
perceived fatigue and discomfort in the leg and not dyspnoea.
In this study, peripheral muscle
dysfunction was found in patients with COPD. Female patients seemed to be more
prone to decrease in thigh muscle function. These findings are of clinical
importance since muscle weakness is associated with exercise intolerance, poor
quality of life and an increased need for medical assistance 1-3 .
Based on our findings, pulmonary
rehabilitation should be more focused on improving skeletal muscle function.
Both muscle strength and muscle endurance
training should be included in the exercise training programs. In accordance
with our results, two recent reviews 10,35 showed that muscle
strength training should be part of the pulmonary
rehabilitation. Endurance training has also
been shown to be of benefit for patients with COPD.35 Currently, endurance training programs used for patients with
COPD consist mainly of walking and cycling exercises that improve the
cardio-respiratory system. However, to improve muscular endurance, specific muscle endurance
trainings with many repetitions and low loads are required. Not only sedentary
patients with COPD but also non-sedentary patients should be considered for
physical training. Moreover, since we found gender-related differences of
muscle performance, this issue also needs to be considered when designing
rehabilitation programs for these patients.
Acknowledgments
This work was supported by Swedish
Heart- and Lung Foundation.
References
Decramer M, Gosselink R, Troosters
T, Verschueren M, Evers G: Muscle weakness is related to utilization of health
care resources in COPD patients . Eur Respir J 10 417-423, 1997.
Ferrer MA, Alonso J, Morera J:
Chronic obstructive pulmonary disease Stage
and health-related quality of life . Ann Intern Med 127 (12): 1072-1079, 1997.
Yohannes AM, Roomi J, Waters K,
Connolly MJ: Quality of life in elderly patients with COPD: measurement and
predictive factors . Respir Med 92 (10): 1231-1236, 1998.
Agusti AG, Noguera A, Sauleda J,
Sala E, Pons J, Busques X: Systemic effects of chronic obstructive pulmonary disease . Eur Respir J 21 (2): 347-360,
2003.
Killian KJ, Leblanc P, Martin DH,
Summers E, Jones NL, Campbell EJ: Exercise capacity and ventilatory,
circulatory, and symptom limitation in patients with chronic airflow limitation
. Am Rev Respir Dis 146 (4): 935-940, 1992.
Mador MJ, Kufel TJ, Pineda L:
Quadriceps fatigue after cycle exercise in patients with chronic obstructive pulmonary disease . Am J Respir Crit Care Med 161
447-453, 2000.
Casaburi R: Skeletal muscle function
in COPD . Chest 117 (5, Suppl 1): 267S-271S, 2000.
Mador MJ, Bozkanat E: Skeletal
muscle dysfunction in chronic obstructive pulmonary
disease . Respir Res 2 (4): 216-224, 2001.
Serres I, Gautier V, Varray A,
Préfaut C: Impaired skeletal muscle endurance
related to physical inactivity and altered lung function in COPD patients .
Chest 113 (4): 900-905, 1998.
O'Shea SD, Taylor NF, Paratz J:
Peripheral muscle strength training in COPD: a systematic review . Chest 126
(3): 903-914, 2004.
Ortega F, Toral J, Cejudo P:
Comparison of effects of strength and endurance
training in patients with chronic obstructive pulmonary
disease . Am J Respir Crit Care Med 166 (5): 669-674, 2002.
Serres I, Varray A, Vallet G,
Micallef JP, Préfaut C: Improved skeletal muscle performance after
individualized exercise training in patients with chronic obstructive pulmonary disease . J Cardiopulm Rehabil 17 (4):
232-238, 1997.
Wadell K, Sundelin G, Lundgren R,
Henriksson-Larsén K, Lindström B: Muscle performance in patients with chronic
obstructive pulmonary disease--effects of a
physical training programme . Adv Physiother 7 51-59, 2005.
Coronell C, Orozco-Levi M, Méndez R,
Ramírez-Sarmiento A, Gáldiz JB, Gea J: Relevance of assessing quadriceps endurance in patients with COPD . Eur Respir J 24
(1): 129-136, 2004.
Gosker HR, Wouters EFM, van der
Vusse GJ, Schols AMWJ: Skeletal muscle dysfunction in chronic obstructive pulmonary disease and chronic heart failure:
underlying mechanisms and therapy perspectives . Am J Clin Nutr 71 (5):
1033-1047, 2000.
Van't Hul A, Harlaar J, Gosselink R,
Hollander P, Postmus P, Kwakkel G: Quadriceps muscle endurance
in patients with chronic obstructive pulmonary
disease . Muscle Nerve 29 (2): 267-274, 2004.
Pauwels RA, Buist AS, Calverley PMA,
Jenkins CR, Hurd SS: Global strategy for the diagnosis, management, and
prevention of chronic obstructive pulmonary
disease. NHLBI/WHO global initiative for chronic obstructive lung disease
(GOLD) workshop summary . Am J Respir Crit Care Med 163 (5): 1256-1276, 2001.
Cole B: Physical rehabilitation
outcomes measures . 3 ed; Ontario: Canadian Physiotherapy Association, 1995.
Farrel M, Richards JG: Analysis of
the reliability and validity of the kinetic communicator exercise device . Med
Sci Sports Exerc 18 44-50, 1985.
Dvir Z: Muscle testing,
interpretation, and clinical applications . 1 ed; Singapore: Longman Publishers
Singapore Pvt Ltd, 1995.
Lindstrom B, Lexell J, Gerdle B,
Downham D: Skeletal muscle fatigue and endurance
in young and old men and women . J Gerontol A Biol Sci Med Sci 52 (1): 59-66,
1997.
Lindstrom B, Kristensen B, Gerdle B:
Dynamic strength and endurance of the thigh
muscles in patients with minimun sequel after ischaemic stroke .
Neurorehabilitation 12 157-167, 1999.
Larsson B, Karlsson S, Eriksson M,
Gerdle B: Test-retest reliability of EMG and peak torque during repetitive
maximum concentric knee extensions . J Electromyogr Kinesiol 13 (3): 281-287,
2003.
Borg GAV: Psychophysical bases of
perceived exertion . Med Sci Sports Exerc 14 377-381, 1982.
Frändin K, Grimby G: Assessment of
physical activity, fitness and performance in 76-years-olds . Scand J Med Sci
Sports 4 41-46, 1994.
Merletti R, LoConte LR, Orizio C:
Indices of muscle fatigue . J Electromyogr Kinesiol 1 (1): 20-33, 1991.
Gosselink R, Troosters T, Decramer
M: Distribution of muscle weakness in patients with stable chronic obstructive pulmonary disease . J Cardiopulm Rehabil 20 (6):
353-360, 2000.
Man WD, Soliman MGG, Nikoletou D:
Non-volitional assessment of skeletal muscle strength in patients with chronic
obstructive pulmonary disease . Thorax 58 (8):
665-669, 2003.
Casaburi R: Skeletal muscle
dysfunction in chronic obstructive pulmonary
disease . Med Sci Sports Exerc 33 (7 Suppl): S662-S670, 2001.
Couillard A, Maltais F, Saey D:
Exercise-induced quadriceps oxidative stress and peripheral muscle dysfunction
in patients with chronic obstructive pulmonary
disease . Am J Respir Crit Care Med 167 (12): 1664-1669, 2003.
Clark CJ, Cochrane LM, Mackay E,
Paton B: Skeletal muscle strength and endurance
in patients with mild COPD and the effects of weight training . Eur Respir J 15
(1): 92-97, 2000.
Zattara-Hartmann MC, Badier M,
Guillot C, Tomei C, Jammes Y: Maximal force and endurance
to fatigue of respiratory and skeletal muscles in chronic hypoxemic patients:
the effects of oxygen breathing . Muscle Nerve 18 (5): 495-502, 1995.
Staron RS, Hagerman FC, Hikida RS:
Fiber type composition of the vastus lateralis muscle of young men and women .
J Histochem Cytochem 48 (5): 623-629, 2000.
Pitta F, Troosters T, Martijn A,
Probst VS, Decramer M, Gosselink R: Characteristics of physical activities in
daily life in chronic obstructive pulmonary
disease . Am J Respir Crit Care Med 171 (9): 972-977, 2005.
Puhan MA, Schunemann HJ, Frey M,
Scharplatz M, Bachmann LM: How should COPD patients exercise during respiratory
rehabilitation? Comparison of exercise modalities and intensities to treat
skeletal muscle dysfunction . Thorax 60 367-375, 2005.
© 2005 Elsevier Ltd
Word count: 4101
Identifier / keyword
Title
Thigh muscle strength and endurance in patients with COPD compared with
healthy controls
Author
Publication title
Volume
Issue
Pages
1451-1457
Publication year
2006
Publication date
Aug 2006
Year
2006
Elsevier Limited
Place of publication
Oxford
Country of publication
United States
Journal subject
ISSN
09546111
Source type
Scholarly Journals
Language of publication
English
Document type
EDB, Journal Article
DOI
ProQuest document ID
1035045504
Document URL
http://search.proquest.com/docview/1035045504?accountid=34598
Copyright
© 2005 Elsevier Ltd
Last updated
2012-08-26
Database
ProQuest Research Library
Tidak ada komentar:
Posting Komentar