Update on the mechanisms of muscle dysfunction in COPD;Actualización en los mecanismos de disfunción muscular en la EPOC

Archivos de Bronconeumologia

Volumn 44, Issue 6, 2008, Pages 328-337

  Gea, Joaquim ^a   Barreiro, Esther ^b  

^a HOSPITAL DEL MAR   (Spain)

^b NONE

Author keywords

Lung disease; Muscle dysfunction; Peripheral muscles; Respiratory muscles

Indexed keywords

NITROUS OXIDE; REACTIVE OXYGEN METABOLITE; SCAVENGER; SUPEROXIDE;

APOPTOSIS; BREATHING MUSCLE; CHRONIC OBSTRUCTIVE LUNG DISEASE; COMORBIDITY; ENDURANCE; GAS EXCHANGE; GEOMETRY; HUMAN; HYPERCAPNIA; HYPOXIA; INFLAMMATION; INJURY; LUNG DISEASE; LUNG RESISTANCE; MALNUTRITION; MUSCLE CONTRACTION; MUSCLE FATIGUE; MUSCLE FUNCTION; OXIDATIVE STRESS; POSITIVE END EXPIRATORY PRESSURE; RESPIRATORY AIRFLOW; RESPIRATORY FUNCTION; REVIEW; SKELETAL MUSCLE;

HUMANS; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE;

EID: 48249088095     PISSN: 03002896     EISSN: 15792129     Source Type: Journal    
DOI: 10.1157/13123091     Document Type: Review

References (114)

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. Disponible en: www.goldcopd.com
2. Agustí AG, Noguera A, Sauleda J, Sala E, Pons J, Busquets X. Systemic effects of chronic obstructive pulmonary disease. Eur Respir J. 2003;21:347-60.
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. 1999;159:S1-S40.
4. Gea J, Orozco-Levi M, Barreiro E. Skeletal and respiratory muscle dysfunction in the systemic inflammatory response syndrome associated with COPD. En: Cazzola M, Stockley RA, Wouters EFM, editors. COPD as a systemic disease. Boca Raton: Clinical Publishing; 2008.
5. Gea J, Barreiro E, Orozco-Levi M. Skeletal muscle adaptation to disease states. En: Bottinelli R, Reggiani C, editors. Skeletal muscle plasticity in health and disease: from genes to whole muscle. Doordrecht: Springer; 2006. p. 315-60.
6. Swallow EB, Reyes D, Hopkinson NS, Man WD, Porcher R, Cetti EJ, et al. Quadriceps strength predicts mortality in patients with moderate to severe chronic obstructive pulmonary disease. Thorax. 2007;62:115-20.
7. Kibler WB. Normal shoulder mechanics and function. Instr Course Lect. 1997;46:39-42.
8. Vaughan CL. Theories of bipedal walking: an odyssey. J Biomech. 2003;36:513-23.
9. Banker BQ, Engel AG. The muscle biopsy & basic reactions of muscle. En: Engel AG, Franzini-Armstrong C, editors. Myology. New York: McGraw-Hill Inc.; 1994. p. 822-88.
10. Gea J, Orozco-Levi M, Barreiro E, Ferrer A, Broquetas J. Structural and functional changes in the skeletal muscles of COPD patients: the "compartments" theory. Monaldi Arch Chest Dis. 2001;56:214-24.
11. Edwards RHT, Faulkner JA. Structure and function of the respiratory muscles. En: Roussos C, editor. The thorax. Part A: Physiology. New York: Marcel Dekker Inc.; 1995. p. 185-217.
12. Derenne JP, Macklem PT, Roussos C. The respiratory muscles: mechanics, control, and pathophysiology. Am Rev Respir Dis. 1978;118:119-33.
13. De Troyer A, Kirkwood PA, Wilson TA. Respiratory action of the intercostal muscles. Physiol Rev. 2005;85:717-56.
14. Hug F, Raux M, Prella M, Morelot-Panzini C, Straus C, Similowski T. Optimized analysis of surface electromyograms of the scalenes during quiet breathing in humans. Respir Physiol Neurobiol. 2006;150:75-81.
15. Legrand A, Schneider E, Gevenois PA, De Troyer A. Respiratory effects of the scalene and sternomastoid muscles in humans. J Appl Physiol. 2003;94:1467-72.
16. Orozco-Levi M, Gea J, Monells J, Arán X, Aguar M, Broquetas J. Activity of latissimus dorsi muscle during inspiratory threshold loads. Eur Respir J. 1995;8:441-5.
17. Orozco-Levi M, Gea J. Músculos respiratorios: biología y fisiología. En: Casan P, Gea J, Gracia Río F, SEPAR, editores. Fisiología y biología respiratorias en la práctica clínica. I. Fisiología y biología respiratorias. Madrid: Ergon; 2007. p. 41-60.
18. Bellemare F, Bono D, D'Angelo E. Electrical and mechanical output of the expiratory muscles in anesthetized dogs. Respir Physiol. 1991;84:171-83.
19. Chang AB. The physiology of cough. Paediatr Respir Rev. 2006;7:2-8.
20. Goldman MD, Grassino A, Mead J, Sears A. Mechanics of the human diaphragm during voluntary contraction: dynamics. J Appl Physiol. 1978;44:840-8.
21. Rochester DF, Braun NMT, Arora NS. Respiratory muscle strength in chronic obstructive pulmonary disease. Am Rev Respir Dis. 1979;119:151-4.
22. Similowski T, Yan S, Gaithier AP, Macklem PT. Contractile properties of the human diaphragm during chronic hyperinflation. N Engl J Med. 1991;325:917-23.
23. Gosselink R, Troosters T, Decramer M. Peripheral muscle weakness contributes to exercise limitation in COPD. Am J Respir Crit Care Med. 1996;153:976-80.
24. Levine S, Nguyen T, Kaiser LR, Rubinstein NA, Maislin G, Gregory C, et al. Human diaphragm remodeling associated with chronic obstructive pulmonary disease: clinical implications. Am J Respir Crit Care Med. 2003;168:706-13.
25. Ramírez-Sarmiento A, Orozco-Levi M, Barreiro E, Méndez R, Ferrer A, Broquetas JM, et al. Expiratory muscle endurance in chronic obstructive pulmonary disease. Thorax. 2002;57:132-6.
26. Arnold JS, Thomas AJ, Kelsen SG. Length-tension relations of abdominal expiratory muscles: effect of emphysema. J Appl Physiol. 1987;62:739-45.
27. Le Bourdelles G, Viires N, Boczkowski J, Seta N, Pavlovic D, Aubier M. Effects of mechanical ventilation on diaphragmatic contractile properties in rats. Am J Respir Crit Care Med. 1994;149:1539-44.
28. Barreiro E, Comtois AS, Mohammed S, Lands LC, Hussain SN. Role of heme oxygenases in sepsis-induced diaphragmatic contractile dysfunction and oxidative stress. Am J Physiol Lung Cell Mol Physiol. 2002;283:L476-L84.
29. Deconinck N, Van Parijs V, Beckers-Bleukx G, Van den Bergh P. Critical illness myopathy unrelated to corticosteroids or neuromuscular blocking agents. Neuromuscul Disord. 1998;8:186-92.
30. Coronell C, Orozco-Levi M, Méndez R, Ranmírez-Sarmineto A, Gladis JB, Gea J. Relevance of assessing quadriceps endurance in patients with COPD. Eur Respir J. 2004;24:129-36.
31. Serres I, Gautier V, Varray A, Prefaut C. Impaired skeletal muscle endurance related to physical inactivity and altered lung function in COPD patients. Chest. 1998;113:900-5.
32. Sala E, Roca J, Marrades RM, Alonso J, González de Suso JM, Moreno A, et al. Effects of endurance training on skeletal muscle bioenergetics in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1999;159:1726-34.
33. Engelen MP, Schols AM, Does JD, Gosker HR, Deutz NE, Wouters EF. Exercise-induced lactate increase in relation to muscle substrates in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2000;162:1697-704.
34. Bernard S, LeBlanc P, Whittom F, Carrier G, Jobin J, Belleau R, et al. Peripheral muscle weakness in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1998;158:629-34.
35. Hamilton AL, Killian KJ, Summers E, Jones NL. Muscle strength, symptom intensity, and exercise capacity in patients with cardiorespiratory disorders. Am J Respir Crit Care Med. 1995;152:2021-31.
36. 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. 1992;146:935-40.
37. American Association of Cardiovascular and Pulmonary Rehabilitation (AACVPR). Guidelines for pulmonary rehabilitation programs. Champaign, IL: Human Kinetics; 2004.
38. Bloomfield SA. Changes in musculoskeletal structure and function with prolonged bed rest. Med Sci Sports Exerc. 1997;29: 197-206.
39. Maltais F, LeBlanc P, Simard C, Jobin J, Berube C, Bruneau J, et al. Skeletal muscle adaptation to endurance training in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1996;154:442-7.
40. Gea J, Orozco-Levi M, Barreiro E. Particularidades fisiopatoló gicas de las alteraciones musculares en el paciente con EPOC. Nutr Hosp. 2006;21 Supl 3:62-8.
41. Creutzberg EC, Wouters EF, Vanderhoven-Augustin IM, Dentener MA, Schols AM. Disturbances in leptin metabolism are related to energy imbalance during acute exacerbations of chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2000;162:1239-45.
42. Di Francia M, Barbier D, Mege JL, Orehek J. Tumor necrosis factor-alpha levels and weight loss in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1994;150:1453-5.
43. Gan WQ, Man WQ, Senthilselvan A, Sin DD. Association between chronic obstructive pulmonary disease and systemic inflammation: a systematic review and a meta-analysis. Thorax. 2004;59:574-80.
44. Sauleda J, García-Palmer FJ, González G, Palou A, Agustí AG. 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. 2000;161:32-5.
45. Flores EA, Bristain BR, Pomposelli JJ, Dinarello CA, Blackburn GL, Istfan NW. Infusion of tumor necrosis factor/cachectin promotes muscle metabolism in the rat. J Clin Invest. 1989;83:1614-22.
46. Montes de Oca M, Torres SH, De Sanctis J, Mata A, Hernández N, Tálamo C. Skeletal muscle inflammation and nitric oxide in patients with COPD. Eur Respir J. 2005;26:390-7.
47. Barreiro E, De la Puente B, Coronell C, Polkey M, Schols A, Gea J. Description of the cytokine profile using antibody arrays of peripheral muscles in severe COPD patients. Eur Respir J. 2005;26 Suppl 49:363.
48. Casadevall C, Coronell C, Minguella J, Blanco L, Orozco-Levi M, Barreiro E, 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. 2004;40:209-17.
49. Zhang J, Liu Y, Shi J, Larson DF, Watson RR. Side-stream cigarette smoke induces dose-response in systemic inflammatory cytokine production and oxidative stress. Exp Biol Med. 2002;227:823-9.
50. Nordskog BK, Fields WR, Hellmann GM. Kinetic analysis of cytokine response to cigarette smoke condensate by human endothelial and monocytic cells. Toxicology. 2005;212:87-97.
51. Orozco-Levi M, Coronell C, Abeijon B, Ramírez-Sarmiento A, Ercilla G, Broquetas J, et al. Smoking and MIC-A expression in bronchial epithelium: a sign of induced autoimmune mechanisms? Proceedings of the ATS. 2005;2:A140.
52. Hill AT, Campbell EJ, Hill SL, Bayley DL, Stockley RA. Association between airway bacterial load and markers of airway inflammation in patients with stable chronic bronchitis. Am J Med. 2000;109:288-95.
53. Martínez-Llorens JM, Orozco-Levi M, Masdeu MJ, Coronell C, Ramírez-Sarmiento A, Sanjuas C, et al. Disfunción muscular global durante la exacerbación de la EPOC: un estudio de cohortes. Med Clin (Barc). 2004;122:521-7.
54. García-Aymerich J, Farrero E, Félez MA, Izquierdo J, Marrades RM, Antó JM, the EFRAM investigators. Risk factors of readmission to hospital for a COPD exacerbation: a prospective study. Thorax. 2003;58:100-5.
55. Supinski G. Free radical induced respiratory muscle dysfunction. Mol Cell Biochem. 1998;179:99-110.
56. Gea J, Barreiro E, Orozco-Levi M. Free radicals, cytokines and respiratory muscles in COPD patients. Clin Pulm Med. 2007;14:117-26.
57. Reid MB, Haack KE, Franchek KM, Valberg PA, Kobzik L, West MS. Reactive oxygen in skeletal muscle: I. Intracellular oxidant kinetics and fatigue in vitro. J Appl Physiol. 1992;73:1797-804.
58. Kobzik L, Reid MB, Bredt DS, Stamler JS. Nitric oxide in skeletal muscle. Nature. 1994;372:546-8.
59. Barreiro E, De la Puente B, Minguella J, Corominas JM, Serrano S, Hussain SN, et al. Oxidative stress and respiratory muscle dysfunction in severe chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2005;171:1116-24.
60. Barreiro E, Gea J, Corominas JM, Hussain SN. Nitric oxide synthases and protein oxidation in the quadriceps femoris of patients with chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol. 2003;29:771-8.
61. Gosker HR, Bast A, Haenen GR, Fischer MA, Van der Vusse GJ, Wouters EF, et al. Altered antioxidant status in peripheral skeletal muscle of patients with COPD. Respir Med. 2005;99:118-25.
62. Barreiro E, Gáldiz JB, Mariñán M, Álvarez FJ, Hussain SN, Gea J. Respiratory loading intensity and diaphragm oxidative stress: N-acetylcysteine effects. J Appl Physiol. 2006;100:555-63.
63. Barreiro E, Gea J, Matar G, Hussain SN. Expression and carbonylation of creatine kinase in the quadriceps femoris muscles of patients with chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol. 2005;33:636-42.
64. Schols AM. Nutrition in chronic obstructive pulmonary disease. Curr Opin Pulm Med. 2000;6:110-5.
65. Schols AM, Wouters EF. Nutritional abnormalities and supplementation in chronic obstructive pulmonary disease. Clin Chest Med. 2000;21:753-62.
66. Coronell C, Orozco-Levi M, Ramírez-Sarmiento A, Martínez-Llorens J, Broquetas J, Gea J. Síndrome de bajo peso asociado a la EPOC en nuestro medio. Arch Bronconeumol. 2002;38:580-4.
67. Schols AM, Slangen J, Volovics L, Wouters EF. Weight loss is a reversible factor in the prognosis of chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1998;157:1791-7.
68. Schols AM, Broekhuizen R, Welling-Scheepers CA, Wouters EF. Body composition and mortality in chronic obstructive pulmonary disease. Am J Clin Nutr. 2005;82:53-9.
69. Kelsen SG, Ference M, Kapoor S. Effects of prolonged undernutrition on structure and function of the diaphragm. J Appl Physiol. 1985;58:1354-9.
70. Lopes J, Russell DM, Whitwell J, Jeejeebhoy KN. Skeletal muscle function in malnutrition. Am J Clin Nutr. 1982;36:602-10.
71. Schols AM, Mostert R, Soeters PB, Wouters EF. Body composition and exercise performance in patients with chronic obstructive pulmonary disease. Thorax. 1991;46:695-9.
72. Schols A, Buurman W, Van den Brekel S, Dentener MA, Wouters EF. Evidence for a relation between metabolic derangements and increased levels of inflammatory mediators in a subgroup of patients with chronic obstructive pulmonary disease. Thorax. 1996;51:819-24.
73. Pastoris O, Dossena M, Foppa P, Arnaboldi R, Gorini A, Villa RF, et al. Modifications by chronic intermittent hypoxia and drug treatment on skeletal muscle metabolism. Neurochem Res. 1995;20:143-50.
74. Romer LM, Haverkamp HC, Amann M, Lovering AT, Pegelow DF, Dempsey JA. Effect of acute severe hypoxia on peripheral fatigue and endurance capacity in healthy humans. Am J Physiol Regul Integr Comp Physiol. 2007;292:R598-R606.
75. Caquelard F, Burnet H, Tagliarini F, Cauchy E, Richalet JP, Jammes Y. Effects of prolonged hypobaric hypoxia on human skeletal muscle function and electromyographic events. Clin Sci (Lond). 2000;98:329-37.
76. 2 en pacientes con EPOC. Arch Bronconeumol. 1993;29:226-8.
77. Rafferty GF, Lou Harris M, Polkey MI, Greenough A, Moxham J. Effect of hypercapnia on maximal voluntary ventilation and diaphragm fatigue in normal humans. Am J Respir Crit Care Med. 1999;160:1567-71.
78. Decramer M, DeBock V, Dom R. Functional and histologic picture of steroid-induced myopathy in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1996;153:1958-64.
79. Gea J, Hamid Q, Czaika G, Zhu E, Mohan-Ram V, Goldspink G, et al. Expression of myosin heavy-chain isoforms in the respiratory muscles following inspiratory resistive breathing. Am J Respir Crit Care Med. 2000;161:1274-8.
80. Zhu E, Petrof BJ, Gea J, Comtois N, Grassino AE. Diaphragm muscle fiber injury after inspiratory resistive breathing. Am J Respir Crit Care Med. 1997;155:1110-6.
81. Orozco-Levi M, Lloreta J, Minguella J, Serrano S, Broquetas JM, Gea J. Injury of the human diaphragm associated with exertion and chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2001;164:1734-9.
82. Levine S, Kaiser L, Leferovich J, Tikunov B. Cellular adaptations in the diaphragm in chronic obstructive pulmonary disease. N Engl J Med. 1997;337:1799-806.
83. Orozco-Levi M, Gea J, Lloreta J, Félez M, Minguella J, Serrano S, et al. Subcellular adaptation of the human diaphragm in Chronic Obstructive Pulmonary Disease. Eur Respir J. 1999;13:371-8.
84. Hards JM, Reid WD, Pardy RL, Paré PD. Respiratory muscle morphometry: correlation with pulmonary function and nutrition. Chest. 1990;97:1037-44.
85. Lloreta J, Orozco-Levi M, Gea J, Broquetas J. Selective diaphragmatic mitochondrial abnormalities in a patient with marked airflow obstruction. Ultrastruct Pathol. 1996;20:67-71.
86. Gea J. Myosin gene expression in the respiratory muscles. Eur Respir J. 1997;10:2404-10.
87. Campbell JA, Hughes RL, Shagal V, Frederiksen J, Shields TW. Alterations in intercostal muscle morphology and biochemistry in patients with chronic obstructive lung disease. Am Rev Respir Dis. 1980;122:679-86.
88. Jiménez-Fuentes MA, Gea J, Aguar MC, Minguella J, Lloreta J, Félez M, et al. Densidad capilar y función respiratoria en el músculo intercostal externo. Arch Bronconeumol. 1999;35:471-6.
89. Levine S, Nguyen T, Friscia M, Zhu J, Szeto W, Tikunov BA, et al. Parasternal intercostal muscle remodeling in severe chronic obstructive pulmonary disease. J Appl Physiol. 2006;101:1297-302.
90. Hughes RL, Katz H, Sahgal V, Campbell JA, Hartz R, Shields TW. Fiber size and energy metabolites in five separate muscles from patients with chronic obstructive lung diseases. Respiration. 1983;44:321-8.
91. Jakobsson P, Jorfeldt L, Brundin A. Skeletal muscle metabolites and fiber types in patients with advanced chronic obstructive pulmonary disease (COPD), with and without chronic respiratory failure. Eur Respir J. 1990;3:192-6.
92. Jakobsson P, Jordfelt L, Henriksson J. Metabolic enzyme activity in the quadriceps femoris muscle in patients with severe chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1995;151:374-7.
93. Simard C, Maltais F, Leblanc P, Simard PM, Jobin J. Mitochondrial and capillarity changes in vastus lateralis muscle of COPD patients: electron microscopy study. Med Sci Sports Exerc. 1996;28:S95.
94. Whittom F, Jobin J, Simard PM, LeBlanc P, Simard C, Bernard S, et al. Histochemical and morphological characteristics of the vastus lateralis muscle in COPD patients. Med Sci Sports Exerc. 1998;30:1467-74.
95. Gea J, Pasto M, Carmona M, Orozco-Levi M, Palomeque J, Broquetas J. Metabolic characteristics of the deltoid muscle in patients with chronic obstructive pulmonary disease. Eur Respir J. 2001;17:939-45.
96. Hernández N, Orozco-Levi M, Belalcazar V, Pasto M, Minguella J, Broquetas JM, et al. Dual morphometrical changes of the deltoid muscle in patients with COPD. Respir Physiol Neurobiol. 2003;134:219-29.
97. Sato Y, Asoh T, Honda Y, Fujimatso Y, Higuchi I, Oizumi K. Morphologic and histochemical evaluation of biceps muscle in patients with chronic pulmonary emphysema manifesting generalized emaciation. Eur Neurol. 1997;37:116-21.
98. Schols A. Nutritional modulation as part of the integrated management of chronic obstructive pulmonary disease. Proc Nutr Soc. 2003;62:783-91.
99. Goldspink G. Research on mechano growth factor: its potential for optimising physical training as well as misuse in doping. Br J Sports Med. 2005;39:787-8.
100. Warren GL, Hulderman T, Jensen N, McKinstry M, Mishra M, Luster MI, et al. Physiological role of tumor necrosis factor alpha in traumatic muscle injury. FASEB J. 2002;16:1630-2.
101. Kuru S, Inukai A, Kato T, Liang Y, Kimura S, Sobue G. Expression of tumor necrosis factor-alpha in regenerating muscle fibers in inflammatory and non-inflammatory myopathies. Acta Neuropathol (Berl). 2003;105:217-24.
102. Barnes PJ. Cytokine modulators as novel therapies for airway disease. Eur Respir J Suppl. 2001;34:67S-77S.
103. Supinski GS, Stofan D, Ciufo R, DiMarco A. N-acetylcysteine administration alters the response to inspiratory loading in oxygen-supplemented rats. J Appl Physiol. 1997;82:1119-25.
104. Gorman RB, McKenzie DK, Butler JE, Tolman JF, Gandevia SC. Diaphragm length and neural drive after lung volume reduction surgery. Am J Respir Crit Care Med. 2005;172:1259-66.
105. Casaburi R, Patessio A, Ioli F, Zanaboni S, Donner CF, Wasserman K. Reduction in exercise lactic acidosis and ventilation as a result of exercise training in patients with chronic obstructive pulmonary disease. Am Rev Respir Dis. 1991;143:9-18.
106. Lacasse Y, Wong E, Guyatt GH, King D, Cook DJ, Goldstein RS. Meta-analysis of respiratory rehabilitation in chronic obstructive pulmonary disease. Lancet. 1996;348:1115-9.
107. Salman GF, Mosier MC, Beasley BW, Clakins DR. Rehabilitation for patients with chronic obstructive pulmonary disease: meta-analysis of randomized controlled trials. J Gen Intern Med. 2003;18:213-21.
108. Ramírez-Sarmiento A, Orozco-Levi M, Güell R, Barreiro E, Hernández N, Mota S, et al. Inspiratory muscle training in patients with chronic obstructive pulmonary disease: structural adaptation and physiologic outcomes. Am J Respir Crit Care Med. 2002;166:1491-7.
109. Franssen FM, Broekhuizen R, Janssen PP, Wouters EF, Schols AM. Effects of whole-body exercise training on body composition and functional capacity in normal-weight patients with COPD. Chest. 2004;125:2021-8.
110. Celli BR, MacNee W, and 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. 2004;23:932-46.
111. Kasapis C, Thompson PD. The effects of physical activity on serum C-reactive protein and inflammatory markers: a systematic review. J Am Coll Cardiol. 2005;45:1563-9.
112. Garrod R, Ansley P, Canavan J, Jewell A. Exercise and the inflammatory response in chronic obstructive pulmonary disease (COPD) - Does training confer anti-inflammatory properties in COPD? Med Hypotheses. 2007;68:291-8.
113. Ram FS, Picot J, Lightowler J, Wedzicha JA. Non-invasive positive pressure ventilation for treatment of respiratory failure due to exacerbations of chronic obstructive pulmonary disease. Cochrane Database Syst Rev. 2004;(3):CD004104.
114. Wijkstra PJ. Non-invasive positive pressure ventilation (NIPPV) in stable patients with chronic obstructive pulmonary disease (COPD). Respir Med. 2003;97:1086-93.