Journal Information
Vol. 44. Issue 6.
Pages 328-337 (January 2008)
Share
Share
Download PDF
More article options
Vol. 44. Issue 6.
Pages 328-337 (January 2008)
Review Articles
Full text access
Update on the Mechanisms of Muscle Dysfunction in COPD
Visits
5232
Joaquim Gea
Corresponding author
jgea@imim.es

Correspondence: Dr J. Gea Servicio de Neumología Hospital Mar Pg Marítim, 2708003 Barcelona, Spain
, Esther Barreiro
Servicio de Neumología, Hospital del Mar, Unidad de Investigación en Músculo y Aparato Respiratorio (URMAR), IMIM, Departamentode Ciencias Experimentales y de la Salud (CEXS), Universidad Pompeu Fabra, CIBER en Enfermedades Respiratorias, Barcelona, Spain
This item has received
Article information

Muscle function is essential for both ventilation (respiratorymuscles) and interacting with the environment (peripheralmuscles). One of the systemic manifestations of chronicobstructive pulmonary disease (COPD) is skeletal muscledysfunction. While the causes of this dysfunction are poorlyunderstood, various local and systemic factors appear to playa role. Among the systemic factors are those arising from thelung disease itself, which increases respiratory muscle activity, leads to unfavorable geometric relationships, and results in areduction in the patient's use of the peripheral musculature. Other systemic factors include inflammation and oxidativestress, malnutrition, impaired gas exchange, comorbidity, andcertain myotoxic drugs. Local factors include muscleinflammation and oxidative stress, apoptosis, injury, andimpaired regenerative capacity. All of these factors interactin different ways in each muscle group, giving rise to variousphenotypes and specific contractile capacities.

Key words:
Respiratory muscles
Peripheral muscles
Muscledysfunction
Lung disease

La función muscular es esencial tanto para la ventilación(músculos respiratorios) como para la vida de relación(músculos periféricos). Los pacientes con enfermedad pul-monar obstructiva crónica (EPOC), en el contexto de suafectación sistémica, presentan disfunción muscular. Lascausas de ésta no están totalmente definidas, aunque pare-cen intervenir diferentes factores tanto sistémicos como lo-cales. Entre los primeros figuran los derivados de la propiaenfermedad pulmonar: aumento de la actividad y geometríadesfavorable para los músculos respiratorios, y disminuciónde la actividad para los periféricos. También son factoresgenerales la inflamación-estrés oxidativo, las alteracionesnutricionales y del intercambio de gases, la comorbilidad ylos fármacos miotóxicos. En cuanto a los locales, incluyeninflamación-estrés oxidativo en los músculos, apoptosis ydaño con baja capacidad regenerativa. Estos factores inter-accionarían de forma diferenciada en cada grupo musculary darían lugar a fenotipos y capacidad contráctil específicos.

Palabras clave:
Músculos respiratorios
Músculos periféricos. Disfunción muscular
Enfermedad pulmonar
Full text is only aviable in PDF
References
[1]
Global Initiative for Chronic Obstructive Lung Disease.
Global Strategy for the Diagnosis, Management and Prevention of Chronic Obstructive Pulmonary Disease. National Heart, Lung and Blood Institute. Update of the Management Sections.
[2]
AG Agustí, A Noguera, J Sauleda, E Sala, J Pons, X Busquets.
Systemic effects of chronic obstructive pulmonary disease.
Eur Respir J, 21 (2003), pp. 347-360
[3]
American Thoracic Society.
Skeletal muscle dysfunction in chronic obstructive pulmonary disease: a statement of the American Thoracic Society and European Respiratory Society.
Am J Respir Crit Care Med, 159 (1999), pp. S1-S40
[4]
J Gea, M Orozco-Levi, E Barreiro.
Skeletal and respiratory muscle dysfunction in the systemic inflammatory response syndrome associated with COPD.
COPD as a systemic disease,
[5]
J Gea, E Barreiro, M Orozco-Levi.
Skeletal muscle adaptation to disease states.
Skeletal muscle plasticity in health and disease: from genes to whole muscle, pp. 315-360
[6]
EB Swallow, D Reyes, NS Hopkinson, WD Man, R Porcher, EJ Cetti, et al.
Quadriceps strength predicts mortality in patients with moderate to severe chronic obstructive pulmonary disease.
Thorax, 62 (2007), pp. 115-120
[7]
WB Kibler.
Normal shoulder mechanics and function.
Instr Course Lect, 46 (1997), pp. 39-42
[8]
CL Vaughan.
Theories of bipedal walking: an odyssey.
J Biomech, 36 (2003), pp. 513-523
[9]
BQ Banker, AG Engel.
The muscle biopsy & basic reactions of muscle.
Myology, pp. 822-888
[10]
J Gea, M Orozco-Levi, E Barreiro, A Ferrer, J Broquetas.
Structural and functional changes in the skeletal muscles of COPD patients: the “compartments” theory.
Monaldi Arch Chest Dis, 56 (2001), pp. 214-224
[11]
RHT Edwards, JA Faulkner.
Structure and function of the respiratory muscles.
The thorax. Part A: Physiology, pp. 185-217
[12]
JP Derenne, PT Macklem, C Roussos.
The respiratory muscles: mechanics, control, and pathophysiology.
Am Rev Respir Dis, 118 (1978), pp. 119-133
[13]
A de Troyer, PA Kirkwood, TA Wilson.
Respiratory action of the intercostal muscles.
Physiol Rev, 85 (2005), pp. 717-756
[14]
F Hug, M Raux, M Prella, C Morelot-Panzini, C Straus, T Similowski.
Optimized analysis of surface electromyograms of the scalenes during quiet breathing in humans.
Respir Physiol Neurobiol, 150 (2006), pp. 75-81
[15]
A Legrand, E Schneider, PA Gevenois, A De Troyer.
Respiratory effects of the scalene and sternomastoid muscles in humans.
J Appl Physiol, 94 (2003), pp. 1467-1472
[16]
M Orozco-Levi, J Gea, J Monells, X Arán, M Aguar, J Broquetas.
Activity of latissimus dorsi muscle during inspiratory threshold loads.
Eur Respir J, 8 (1995), pp. 441-445
[17]
M Orozco-Levi, J Gea.
Músculos respiratorios: biología y fisiología.
Fisiología y biología respiratorias en la práctica clínica. I. Fisiología y biología respiratorias, pp. 41-60
[18]
F Bellemare, D Bono, E D'Angelo.
Electrical and mechanical output of the expiratory muscles in anesthetized dogs.
Respir Physiol, 84 (1991), pp. 171-183
[19]
AB Chang.
The physiology of cough.
Paediatr Respir Rev, 7 (2006), pp. 2-8
[20]
MD Goldman, A Grassino, J Mead, A Sears.
Mechanics of the human diaphragm during voluntary contraction: dynamics.
J Appl Physiol, 44 (1978), pp. 840-848
[21]
DF Rochester, NMT Braun, NS Arora.
Respiratory muscle strength in chronic obstructive pulmonary disease.
Am Rev Respir Dis, 119 (1979), pp. 151-154
[22]
T Similowski, S Yan, AP Gaithier, PT Macklem.
Contractile properties of the human diaphragm during chronic hyperinflation.
N Engl J Med, 325 (1991), pp. 917-923
[23]
R Gosselink, T Troosters, M Decramer.
Peripheral muscle weakness contributes to exercise limitation in COPD.
Am J Respir Crit Care Med, 153 (1996), pp. 976-980
[24]
S Levine, T Nguyen, LR Kaiser, NA Rubinstein, G Maislin, C Gregory, et al.
Human diaphragm remodeling associated with chronic obstructive pulmonary disease: clinical implications.
Am J Respir Crit Care Med, 168 (2003), pp. 706-713
[25]
A Ramírez-Sarmiento, M Orozco-Levi, E Barreiro, R Méndez, A Ferrer, JM Broquetas, et al.
Expiratory muscle endurance in chronic obstructive pulmonary disease.
Thorax, 57 (2002), pp. 132-136
[26]
JS Arnold, AJ Thomas, SG Kelsen.
Length-tension relations of abdominal expiratory muscles: effect of emphysema.
J Appl Physiol, 62 (1987), pp. 739-745
[27]
G Le Bourdelles, N Viires, J Boczkowski, N Seta, D Pavlovic, M Aubier.
Effects of mechanical ventilation on diaphragmatic contractile properties in rats.
Am J Respir Crit Care Med, 149 (1994), pp. 1539-1544
[28]
E Barreiro, AS Comtois, S Mohammed, LC Lands, SN Hussain.
Role of heme oxygenases in sepsis-induced diaphragmatic contractile dysfunction and oxidative stress.
Am J Physiol Lung Cell Mol Physiol, 283 (2002), pp. L476-LL84
[29]
N Deconinck, V van Parijs, G Beckers-Bleukx, P van den Bergh.
Critical illness myopathy unrelated to corticosteroidsor neuromuscular blocking agents.
Neuromuscul Disord, 8 (1998), pp. 186-192
[30]
C Coronell, M Orozco-Levi, R Méndez, A Ranmírez-Sarmineto, JB Gladis, J Gea.
Relevance of assessing quadriceps endurance in patients with COPD.
Eur Respir J, 24 (2004), pp. 129-136
[31]
I Serres, V Gautier, A Varray, C Prefaut.
Impaired skeletal muscle endurance related to physical inactivity and altered lung function in COPD patients.
Chest, 113 (1998), pp. 900-905
[32]
E Sala, J Roca, RM Marrades, J Alonso, JM González de Suso, A Moreno, et al.
Effects of endurance training on skeletal muscle bioenergetics in chronic obstructive pulmonary disease.
Am J Respir Crit Care Med, 159 (1999), pp. 1726-1734
[33]
MP Engelen, AM Schols, JD Does, HR Gosker, NE Deutz, EF Wouters.
Exercise-induced lactate increase in relation to muscle substrates in patients with chronic obstructive pulmonary disease.
Am J Respir Crit Care Med, 162 (2000), pp. 1697-1704
[34]
S Bernard, P leBlanc, F Whittom, G Carrier, J Jobin, R Belleau, et al.
Peripheral muscle weakness in patients with chronic obstructive pulmonary disease.
Am J Respir Crit Care Med, 158 (1998), pp. 629-634
[35]
AL Hamilton, KJ Killian, E Summers, NL Jones.
Muscle strength, symptom intensity, and exercise capacity in patients with cardiorespiratory disorders.
Am J Respir Crit Care Med, 152 (1995), pp. 2021-2031
[36]
KJ Killian, P leBlanc, DH Martin, E Summers, NL Jones, EJ Campbell.
Exercise capacity and ventilatory, circulatory, and symptom limitation in patients with chronic airflow limitation.
Am Rev Respir Dis, 146 (1992), pp. 935-940
[37]
American Association of Cardiovascular and Pulmonary Rehabilitation (AACVPR).
Guidelines for pulmonary rehabilitation programs, Human Kinetics, (2004),
[38]
SA Bloomfield.
Changes in musculoskeletal structure and function with prolonged bed rest.
Med Sci Sports Exerc, 29 (1997), pp. 197-206
[39]
F Maltais, P leBlanc, C Simard, J Jobin, C Berube, J Bruneau, et al.
Skeletal muscle adaptation to endurance training in patients with chronic obstructive pulmonary disease.
Am J Respir Crit Care Med, 154 (1996), pp. 442-447
[40]
J Gea, M Orozco-Levi, E Barreiro.
Particularidades fisiopatológicas de las alteraciones musculares en el paciente con EPOC.
Nutr Hosp, 21 (2006), pp. 62-68
[41]
EC Creutzberg, EF Wouters, IM Vanderhoven-Augustin, MA Dentener, AM Schols.
Disturbances in leptin metabolism are related to energy imbalance during acute exacerbations of chronic obstructive pulmonary disease.
Am J Respir Crit Care Med, 162 (2000), pp. 1239-1245
[42]
M Di Francia, D Barbier, JL Mege, J Orehek.
Tumor necrosis factor-alpha levels and weight loss in chronic obstructive pulmonary disease.
Am J Respir Crit Care Med, 150 (1994), pp. 1453-1455
[43]
WQ Gan, WQ Man, A Senthilselvan, DD Sin.
Association between chronic obstructive pulmonary disease and systemic inflammation: a systematic review and a meta-analysis.
Thorax, 59 (2004), pp. 574-580
[44]
J Sauleda, FJ García-Palmer, G González, A Palou, AG Agustí.
The activity of cytochrome oxidase is increased in circulating lymphocytes of patients with chronic obstructive pulmonary disease, asthma, and chronic arthritis.
Am J Respir Crit Care Med, 161 (2000), pp. 32-35
[45]
EA Flores, BR Bristain, JJ Pomposelli, CA Dinarello, GL Blackburn, NW Istfan.
Infusion of tumor necrosis factor/cachectin promotes muscle metabolism in the rat.
J Clin Invest, 83 (1989), pp. 1614-1622
[46]
M Montes de Oca, SH Torres, J De Sanctis, A Mata, N Hernández, C Tálamo.
Skeletal muscle inflammation and nitric oxide in patients with COPD.
Eur Respir J, 26 (2005), pp. 390-397
[47]
E Barreiro, B de la Puente, C Coronell, M Polkey, A Schols, J Gea.
Description of the cytokine profile using antibody arrays of peripheral muscles in severe COPD patients.
Eur Respir J, 26 (2005), pp. 363
[48]
C Casadevall, C Coronell, J Minguella, L Blanco, M Orozco-Levi, E Barreiro, et al.
Análisis estructural y expresión de los factores de necrosis tumoral y crecimiento insulina-like en los músculos respiratorios de pacientes con EPOC. ¿Son válidas las muestras obtenidas en el curso de una toracotomía por neoplasia pulmonar localizada?.
Arch Bronconeumol, 40 (2004), pp. 209-217
[49]
J Zhang, Y Liu, J Shi, DF Larson, RR Watson.
Side-stream cigarette smoke induces dose-response in systemic inflammatory cytokine production and oxidative stress.
Exp Biol Med, 227 (2002), pp. 823-829
[50]
BK Nordskog, WR Fields, GM Hellmann.
Kinetic analysis of cytokine response to cigarette smoke condensate by human endothelial and monocytic cells.
Toxicology, 212 (2005), pp. 87-97
[51]
M Orozco-Levi, C Coronell, B Abeijon, A Ramírez-Sarmiento, G Ercilla, J Broquetas, et al.
Smoking and MIC-A expression in bronchial epithelium: a sign of induced autoimmune mechanisms?.
Proceedings of the ATS, 2 (2005), pp. A140
[52]
AT Hill, EJ Campbell, SL Hill, DL Bayley, RA Stockley.
Association between airway bacterial load and markers of airway inflammation in patients with stable chronic bronchitis.
Am J Med, 109 (2000), pp. 288-295
[53]
JM Martínez-Llorens, M Orozco-Levi, MJ Masdeu, C Coronell, A Ramírez-Sarmiento, C Sanjuas, et al.
Disfunción muscular global durante la exacerbación de la EPOC: un estudio de cohortes.
Med Clin (Barc), 122 (2004), pp. 521-527
[54]
J García-Aymerich, E Farrero, MA Félez, J Izquierdo, RM Marrades, JM Antó, the EFRAM investigators.
Risk factors of readmission to hospital for a COPD exacerbation: a prospective study.
Thorax, 58 (2003), pp. 100-105
[55]
G Supinski.
Free radical-induced respiratory muscle dysfunction.
Mol Cell Biochem, 179 (1998), pp. 99-110
[56]
J Gea, E Barreiro, M Orozco-Levi.
Free radicals, cytokines and respiratory muscles in COPD patients.
Clin Pulm Med, 14 (2007), pp. 117-126
[57]
MB Reid, KE Haack, KM Franchek, PA Valberg, L Kobzik, MS West.
Reactive oxygen in skeletal muscle: I. Intracellular oxidant kinetics and fatigue in vitro.
J Appl Physiol, 73 (1992), pp. 1797-1804
[58]
L Kobzik, MB Reid, DS Bredt, JS Stamler.
Nitric oxide in skeletal muscle.
Nature, 372 (1994), pp. 546-548
[59]
E Barreiro, B de la Puente, J Minguella, JM Corominas, S Serrano, SN Hussain, et al.
Oxidative stress and respiratory muscle dysfunction in severe chronic obstructive pulmonary disease.
Am J Respir Crit Care Med, 171 (2005), pp. 1116-1124
[60]
E Barreiro, J Gea, JM Corominas, SN Hussain.
Nitric oxide synthases and protein oxidation in the quadriceps femoris of patients with chronic obstructive pulmonary disease.
Am J Respir Cell Mol Biol, 29 (2003), pp. 771-778
[61]
HR Gosker, A Bast, GR Haenen, MA Fischer, GJ van der Vusse, EF Wouters, et al.
Altered antioxidant status in peripheral skeletal muscle of patients with COPD.
Respir Med, 99 (2005), pp. 118-125
[62]
E Barreiro, JB Gáldiz, M Mariñán, FJ Álvarez, SN Hussain, J Gea.
Respiratory loading intensity and diaphragm oxidative stress: N-acetylcysteine effects.
J Appl Physiol, 100 (2006), pp. 555-563
[63]
E Barreiro, J Gea, G Matar, SN Hussain.
Expression and carbonylation of creatine kinase in the quadriceps femoris muscles of patients with chronic obstructive pulmonary disease.
Am J Respir Cell Mol Biol, 33 (2005), pp. 636-642
[64]
AM Schols.
Nutrition in chronic obstructive pulmonary disease.
Curr Opin Pulm Med, 6 (2000), pp. 110-115
[65]
AM Schols, EF Wouters.
Nutritional abnormalities and supplementation in chronic obstructive pulmonary disease.
Clin Chest Med, 21 (2000), pp. 753-762
[66]
C Coronell, M Orozco-Levi, A Ramírez-Sarmiento, J Martínez-Llorens, J Broquetas, J Gea.
Síndrome de bajo peso asociado a la EPOC en nuestro medio.
Arch Bronconeumol, 38 (2002), pp. 580-584
[67]
AM Schols, J Slangen, L Volovics, EF Wouters.
Weight loss is a reversible factor in the prognosis of chronic obstructive pulmonary disease.
Am J Respir Crit Care Med, 157 (1998), pp. 1791-1797
[68]
AM Schols, R Broekhuizen, CA Welling-Scheepers, EF Wouters.
Body composition and mortality in chronic obstructive pulmonary disease.
Am J Clin Nutr, 82 (2005), pp. 53-59
[69]
SG Kelsen, M Ference, S Kapoor.
Effects of prolonged undernutrition on structure and function of the diaphragm.
J Appl Physiol, 58 (1985), pp. 1354-1359
[70]
J Lopes, DM Russell, J Whitwell, KN Jeejeebhoy.
Skeletal muscle function in malnutrition.
Am J Clin Nutr, 36 (1982), pp. 602-610
[71]
AM Schols, R Mostert, PB Soeters, EF Wouters.
Body composition and exercise performance in patients with chronic obstructive pulmonary disease.
Thorax, 46 (1991), pp. 695-699
[72]
A Schols, W Buurman, S van den Brekel, MA Dentener, EF Wouters.
Evidence for a relation between metabolic derangements and increased levels of inflammatory mediators in a subgroup of patients with chronic obstructive pulmonary disease.
Thorax, 51 (1996), pp. 819-824
[73]
O Pastoris, M Dossena, P Foppa, R Arnaboldi, A Gorini, RF Villa, et al.
Modifications by chronic intermittent hypoxia and drug treatment on skeletal muscle metabolism.
Neurochem Res, 20 (1995), pp. 143-150
[74]
LM Romer, HC Haverkamp, M Amann, AT Lovering, DF Pegelow, JA Dempsey.
Effect of acute severe hypoxia on peripheral fatigue and endurance capacity in healthy humans.
Am J Physiol Regul Integr Comp Physiol, 292 (2007), pp. R598-R606
[75]
F Caquelard, H Burnet, F Tagliarini, E Cauchy, JP Richalet, Y Jammes.
Effects of prolonged hypobaric hypoxia on human skeletal muscle function and electromyographic events.
Clin Sci (Lond), 98 (2000), pp. 329-337
[76]
MC Aguar, J Gea, X Aran, R Guiu, M Orozco-Levi, JM Broquetas.
Modificaciones de la actividad mecánica del diafragma inducidas por la inhalación de CO2 en pacientes con EPOC.
Arch Bronconeumol, 29 (1993), pp. 226-228
[77]
GF Rafferty, M Lou Harris, MI Polkey, A Greenough, J Moxham.
Effect of hypercapnia on maximal voluntary ventilation and diaphragm fatigue in normal humans.
Am J Respir Crit Care Med, 160 (1999), pp. 1567-1571
[78]
M Decramer, V deBock, R Dom.
Functional and histologic picture of steroid-induced myopathy in chronic obstructive pulmonary disease.
Am J Respir Crit Care Med, 153 (1996), pp. 1958-1964
[79]
J Gea, Q Hamid, G Czaika, E Zhu, V Mohan-Ram, G Goldspink, et al.
Expression of myosin heavy-chain isoforms in the respiratory muscles following inspiratory resistive breathing.
Am J Respir Crit Care Med, 161 (2000), pp. 1274-1278
[80]
E Zhu, BJ Petrof, J Gea, N Comtois, AE Grassino.
Diaphragm muscle fiber injury after inspiratory resistive breathing.
Am J Respir Crit Care Med, 155 (1997), pp. 1110-1116
[81]
M Orozco-Levi, J Lloreta, J Minguella, S Serrano, JM Broquetas, J Gea.
Injury of the human diaphragm associated with exertion and chronic obstructive pulmonary disease.
Am J Respir Crit Care Med, 164 (2001), pp. 1734-1739
[82]
S Levine, L Kaiser, J Leferovich, B Tikunov.
Cellular adaptations in the diaphragm in chronic obstructive pulmonary disease.
N Engl J Med, 337 (1997), pp. 1799-1806
[83]
M Orozco-Levi, J Gea, J Lloreta, M Félez, J Minguella, S Serrano, et al.
Subcellular adaptation of the human diaphragm in chronic obstructive pulmonary disease.
Eur Respir J, 13 (1999), pp. 371-378
[84]
JM Hards, WD Reid, RL Pardy, PD Paré.
Respiratory muscle morphometry: correlation with pulmonary function and nutrition.
Chest, 97 (1990), pp. 1037-1044
[85]
J Lloreta, M Orozco-Levi, J Gea, J Broquetas.
Selective diaphragmatic mitochondrial abnormalities in a patient with marked airflow obstruction.
Ultrastruct Pathol, 20 (1996), pp. 67-71
[86]
J Gea.
Myosin gene expression in the respiratory muscles.
Eur Respir J, 10 (1997), pp. 2404-2410
[87]
JA Campbell, RL Hughes, V Shagal, J Frederiksen, TW Shields.
Alterations in intercostal muscle morphology and biochemistry in patients with chronic obstructive lung disease.
Am Rev Respir Dis, 122 (1980), pp. 679-686
[88]
MA Jiménez-Fuentes, J Gea, MC Aguar, J Minguella, J Lloreta, M Félez, et al.
Densidad capilar y función respiratoria en el músculo intercostal externo.
Arch Bronconeumol, 35 (1999), pp. 471-476
[89]
S Levine, T Nguyen, M Friscia, J Zhu, W Szeto, BA Tikunov, et al.
Parasternal intercostal muscle remodeling in severe chronic obstructive pulmonary disease.
J Appl Physiol, 101 (2006), pp. 1297-1302
[90]
RL Hughes, H Katz, V Sahgal, JA Campbell, R Hartz, TW Shields.
Fiber size and energy metabolites in five separate muscles from patients with chronic obstructive lung diseases.
Respiration, 44 (1983), pp. 321-328
[91]
P Jakobsson, L Jorfeldt, A Brundin.
Skeletal muscle metabolites and fiber types in patients with advanced chronic obstructive pulmonary disease (COPD), with and without chronic respiratory failure.
Eur Respir J, 3 (1990), pp. 192-196
[92]
P Jakobsson, L Jordfelt, J Henriksson.
Metabolic enzyme activity in the quadriceps femoris muscle in patients with severe chronic obstructive pulmonary disease.
Am J Respir Crit Care Med, 151 (1995), pp. 374-377
[93]
C Simard, F Maltais, P Leblanc, PM Simard, J Jobin.
Mitochondrial and capillarity changes in vastus lateralis muscle of COPD patients: electron microscopy study.
Med Sci Sports Exerc, 28 (1996), pp. S95
[94]
F Whittom, J Jobin, PM Simard, P leBlanc, C Simard, S Bernard, et al.
Histochemical and morphological characteristics of the vastus lateralis muscle in COPD patients.
Med Sci Sports Exerc, 30 (1998), pp. 1467-1474
[95]
J Gea, M Pasto, M Carmona, M Orozco-Levi, J Palomeque, J Broquetas.
Metabolic characteristics of the deltoid muscle in patients with chronic obstructive pulmonary disease.
Eur Respir J, 17 (2001), pp. 939-945
[96]
N Hernández, M Orozco-Levi, V Belalcazar, M Pasto, J Minguella, JM Broquetas, et al.
Dual morphometrical changes of the deltoid muscle in patients with COPD.
Respir Physiol Neurobiol, 134 (2003), pp. 219-229
[97]
Y Sato, T Asoh, Y Honda, Y Fujimatso, I Higuchi, K Oizumi.
Morphologic and histochemical evaluation of biceps muscle in patients with chronic pulmonary emphysema manifesting generalized emaciation.
Eur Neurol, 37 (1997), pp. 116-121
[98]
A Schols.
Nutritional modulation as part of the integrated management of chronic obstructive pulmonary disease.
Proc Nutr Soc, 62 (2003), pp. 783-791
[99]
G Goldspink.
Research on mechano growth factor: its potential for optimising physical training as well as misuse in doping.
Br J Sports Med, 39 (2005), pp. 787-788
[100]
GL Warren, T Hulderman, N Jensen, M McKinstry, M Mishra, MI Luster, et al.
Physiological role of tumor necrosis factor alpha in traumatic muscle injury.
FASEB J, 16 (2002), pp. 1630-1632
[101]
S Kuru, A Inukai, T Kato, Y Liang, S Kimura, G Sobue.
Expression of tumor necrosis factor-alpha in regenerating muscle fibers in inflammatory and non-inflammatory myopathies.
Acta Neuropathol (Berl), 105 (2003), pp. 217-224
[102]
PJ Barnes.
Cytokine modulators as novel therapies for airway disease.
Eur Respir J Suppl, 34 (2001), pp. 67S-77S
[103]
GS Supinski, D Stofan, R Ciufo, A DiMarco.
N-acetylcysteine administration alters the response to inspiratory loading in oxygen-supplemented rats.
J Appl Physiol, 82 (1997), pp. 1119-1125
[104]
RB Gorman, DK McKenzie, JE Butler, JF Tolman, SC Gandevia.
Diaphragm length and neural drive after lung volume reduction surgery.
Am J Respir Crit Care Med, 172 (2005), pp. 1259-1266
[105]
R Casaburi, A Patessio, F Ioli, S Zanaboni, CF Donner, K Wasserman.
Reduction in exercise lactic acidosis and ventilation as a result of exercise training in patients with chronic obstructive pulmonary disease.
Am Rev Respir Dis, 143 (1991), pp. 9-18
[106]
Y Lacasse, E Wong, GH Guyatt, D King, DJ Cook, RS Goldstein.
Meta-analysis of respiratory rehabilitation in chronic obstructive pulmonary disease.
Lancet, 348 (1996), pp. 1115-1119
[107]
GF Salman, MC Mosier, BW Beasley, DR Clakins.
Rehabilitation for patients with chronic obstructive pulmonary disease: meta-analysis of randomized controlled trials.
J Gen Intern Med, 18 (2003), pp. 213-221
[108]
A Ramírez-Sarmiento, M Orozco-Levi, R Güell, E Barreiro, N Hernández, S Mota, et al.
Inspiratory muscle training in patients with chronic obstructive pulmonary disease: structural adaptation and physiologic outcomes.
Am J Respir Crit Care Med, 166 (2002), pp. 1491-1497
[109]
FM Franssen, R Broekhuizen, PP Janssen, EF Wouters, AM Schols.
Effects of whole-body exercise training on body composition and functional capacity in normal-weight patients with COPD.
Chest, 125 (2004), pp. 2021-2028
[110]
BR Celli, W MacNee, Committee members.
ATS/ERS Task Force. Standards for the diagnosis and treatment of patients with COPD: a summary of the ATS/ERS position paper.
Eur Respir J, 23 (2004), pp. 932-946
[111]
C Kasapis, PD Thompson.
The effects of physical activity on serum C-reactive protein and inflammatory markers: a systematic review.
J Am Coll Cardiol, 45 (2005), pp. 1563-1569
[112]
R Garrod, P Ansley, J Canavan, A Jewell.
Exercise and the inflammatory response in chronic obstructive pulmonary disease (COPD) – Does training confer anti-inflammatory properties in COPD?.
Med Hypotheses, 68 (2007), pp. 291-298
[113]
FS Ram, J Picot, J Lightowler, JA Wedzicha.
Non-invasive positive pressure ventilation for treatment of respiratory failure due to exacerbations of chronic obstructive pulmonary disease.
Cochrane Database Syst Rev, (2004), pp. CD004104
[114]
PJ Wijkstra.
Non-invasive positive pressure ventilation (NIPPV) in stable patients with chronic obstructive pulmonary disease (COPD).
Respir Med, 97 (2003), pp. 1086-1093
Copyright © 2008. Sociedad Española de Neumología y Cirugía Torácica (SEPAR)
Archivos de Bronconeumología
Article options
Tools

Are you a health professional able to prescribe or dispense drugs?