Structural and functional changes of peripheral muscles in chronic obstructive pulmonary disease patients

Current Opinion in Pulmonary Medicine

Volumn 16, Issue 2, 2010, Pages 123-133

  Rabinovich, Roberto A ^a   Vilaró, Jordi ^b  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITAT RAMON LLULL   (Spain)

Author keywords

Chronic obstructive pulmonary disease; Muscle dysfunction; Muscle wasting; Systemic effects

Indexed keywords

CHRONIC OBSTRUCTIVE LUNG DISEASE; DISEASE ASSOCIATION; HUMAN; MUSCLE ATROPHY; MUSCLE DISEASE; MUSCLE HYPERTROPHY; PROGNOSIS; REVIEW; SYSTEMIC DISEASE;

ATROPHY; EXERCISE THERAPY; HUMANS; MITOCHONDRIA, MUSCLE; MUSCLE WEAKNESS; MUSCLE, SKELETAL; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE;

EID: 76449084395     PISSN: 10705287     EISSN: 15316971     Source Type: Journal    
DOI: 10.1097/MCP.0b013e328336438d     Document Type: Review

References (183)

1. Mannino DM, Homa DM, Akinbami LJ, et al. Chronic obstructive pulmonary disease surveillance: United States, 1971-2000. MMWR Surveill Summ 2002; 51:1-16.
2. Menezes AM, Perez-Padilla R, Jardim JR, et al. Chronic obstructive pulmonary disease in five Latin American cities (the PLATINO study): a prevalence study. Lancet 2005; 366:1875-1881.
3. de Marco R, Accordini S, Cerveri I, et al. An international survey of chronic obstructive pulmonary disease in young adults according to GOLD stages. Thorax 2004; 59:120-125.
4. World Health Organization. Annex Table 2. Deaths by cause, sex and mortality stratum in WHO regions, estimates for 2002. World Health Report Statistical Annex; 2004. pp. 120-124.
5. Killian KJ, Summers E, Jones NL, et al. Dyspnea and leg efforts during incremental cycle ergometry. Am Rev Respir Dis 1992; 145:1339-1345.
6. Mador MJ, Kufel TJ, Pineda L. Quadriceps fatigue after cycle exercise in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2000; 161:447-453. (Pubitemid 30129451)
7. Gagnon P, Saey D, Vivodtzev I, et al. Impact of preinduced quadriceps fatigue on exercise response in chronic obstructive pulmonary disease and healthy subjects. J Appl Physiol 2009; 107:832-840.
8. Saey D, Debigare R, Leblanc P, et al. Contractile leg fatigue after cycle exercise: a factor limiting exercise in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2003; 168:425-430.
9. Flaherty KR, Kazerooni EA, Curtis JL, et al. Short-term and long-term outcomes after bilateral lung volume reduction surgery: prediction by quantitative CT. Chest 2001; 119:1337-1346.
10. Theodore J, Robin ED, Morris AJ, et al. Augmented ventilatory response to exercise in pulmonary hypertension. Chest 1986; 89:39-44.
11. Williams TJ, Patterson GA, Mcclean PA, et al. Maximal exercise testing in single and double lung transplant recipients. Am Rev Respir Dis 1992; 145:101-105.
12. Lacasse Y, Wong E, Guyatt GH, et al. Meta-analysis of respiratory rehabilitation in chronic obstructive pulmonary disease. Lancet 1996; 348:1115-1119.
13. Munro PE, Holland AE, Bailey M, et al. Pulmonary rehabilitation following lung transplantation. Transplant Proc 2009; 41:292-295.
14. Celli BR, MacNee W. Standards for the diagnosis and treatment of patients with COPD: a summary of the ATS/ERS position paper. Eur Respir J 2004; 23:932-946.
15. Celli BR, Cote CG, Marin JM, et al. The body-mass index, airflow obstruction, dyspnea, and exercise capacity index in chronic obstructive pulmonary disease. N Engl J Med 2004; 350:1005-1012.
16. Puhan MA, Garcia-Aymerich J, Frey M, et al. Expansion of the prognostic assessment of patients with chronic obstructive pulmonary disease: the updated BODE index and the ADO index. Lancet 2009; 374:704-711.
17. Decramer M, Gosselink LE, Troosters T, et al. Muscle weakness is related to utilization of healthcare resources in COPD patients. Eur Respir J 1997; 10:417-423.
18. Agusti AG, Noguera A, Sauleda J, et al. Systemic effects of chronic obstructive pulmonary disease. Eur Respir J 2003; 21:347-360.
19. Bernard S, Leblanc P, Whittom F, et al. Peripheral muscle weakness in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1998; 158:629-634.
20. Man WD, Soliman MG, Nikoletou D, et al. Nonvolitional assessment of skeletal muscle strength in patients with chronic obstructive pulmonary disease. Thorax 2003; 58:665-669.
21. Man WD, Hopkinson NS, Harraf F, et al. Abdominal muscle and quadriceps strength in chronic obstructive pulmonary disease. Thorax 2005; 60:718-722.
22. Coronell C, Orozco-Levi M, Mendez R, et al. Relevance of assessing quadriceps endurance in patients with COPD. Eur Respir J 2004; 24:129-136.
23. Serres I, Gautier V, Varray A, et al. Impaired skeletal muscle endurance related to physical inactivity and altered lung function in COPD patients. Chest 1998; 113:900-905.
24. Allaire J, Maltais F, Doyon JF, et al. Peripheral muscle endurance and the oxidative profile of the quadriceps in patients with COPD. Thorax 2004; 59:673-678.
25. Swallow EB, Gosker HR, Ward KA, et al. A novel technique for nonvolitional assessment of quadriceps muscle endurance in humans. J Appl Physiol 2007; 103:739-746.
26. Mador MJ, Bozkanat E, Kufel TJ. Quadriceps fatigue after cycle exercise in patients with COPD compared with healthy control subjects. Chest 2003; 123:1104-1111.
27. Engelen MPKJ, Schols AMWJ, Baken WC, et al. Nutritional depletion in relation to respiratory and peripheral skeletal muscle function in out-patients with COPD. Eur Respir J 1994; 7:1793-1797.
28. Schols AMWJ, Soeters PB, Dingemans AMC, et al. Prevalence and characteristics of nutritional depletion in patients with stable COPD eligible for pulmonary rehabilitation. Am Rev Respir Dis 1993; 147:1151-1156.
29. Eid AA, Ionescu AA, Nixon LS, et al. Inflammatory response and body composition in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2001; 164:1414-1418.
30. Braun SR, Keim NL, Dixon RM, et al. The prevalence and determinants of nutritional changes in chronic obstructive pulmonary disease. Chest 1984; 86:558-563.
31. Gray-Donald K, Gibbons L, Shapiro SH, et al. Effect of nutritional status on exercise performance in patients with chronic obstructive pulmonary disease. Am Rev Respir Dis 1989; 140:1544-1548.
32. Gosselink R, Troosters T, Decramer M. Peripheral muscle weakness contributes to exercise limitation in COPD. Am J Respir Crit Care Med 1996; 153:976-980. (Pubitemid 26081648)
33. Engelen MPKJ, Schols AMWJ, Does JD, et al. Skeletal muscle weakness is associated with wasting of extremity fat-free mass but not with airflow obstruction in patients with chronic obstructive pulmonary disease. Am J Clin Nutr 2000; 71:733-738.
34. Baarends EM, Schols AM, Mostert R, et al. Peak exercise response in relation to tissue depletion in patients with chronic obstructive pulmonary disease. Eur Respir J 1997; 10:2807-2813.
35. Kobayashi A, Yoneda T, Yoshikawa M, et al. The relation of fat-free mass to maximum exercise performance in patients with chronic obstructive pulmonary disease. Lung 2000; 178:119-127.
36. Schols AM, Mostert R, Soeters PB, et al. Body composition and exercise performance in patients with chronic obstructive pulmonary disease. Thorax 1991; 46:695-699.
37. Mostert R, Goris A, Weling-Scheepers C, et al. Tissue depletion and health related quality of life in patients with chronic obstructive pulmonary disease. Respir Med 2000; 94:859-867.
38. Marquis K, Debigare R, Lacasse Y, et al. Midthigh muscle cross-sectional area is a better predictor of mortality than body mass index in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2002; 166:809-813.
39. Mador MJ. Muscle mass, not body weight, predicts outcome in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2002; 166:787-789.
40. Seymour JM, Ward K, Sidhu PS, et al. Ultrasound measurement of rectus femoris cross-sectional area and the relationship with quadriceps strength in COPD. Thorax 2009; 64:418-423.
41. Vilaro J, Rabinovich R, Gonzalez-deSuso JM, et al. Clinical assessment of peripheral muscle function in patients with chronic obstructive pulmonary disease. Am J Phys Med Rehabil 2009; 88:39-46.
42. Hopkinson NS, Tennant RC, Dayer MJ, et al. A prospective study of decline in fat free mass and skeletal muscle strength in chronic obstructive pulmonary disease. Respir Res 2007; 8:25.
43. ShrikrishnaD,Albert P, Calverley P, et al. Quadriceps weakness in gold stage II COPD: data from the ECLIPSE study. Eur Respir J 2009; 34 (Suppl 53):3811
44. Hopkinson NS, Nickol AH, Payne J, et al. Angiotensin converting enzyme genotype and strength in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2004; 170:395-399.
45. Hopkinson NS, Li KW, Kehoe A, et al. Vitamin D receptor genotypes influence quadriceps strength in chronic obstructive pulmonary disease. Am J Clin Nutr 2008; 87:385-390.
46. Hughes RL, Katz H, Sahgal V, et al. Fiber size and energy metabolites in five separate muscles from patients with chronic obstructive lung diseases. Respiration 1983; 44:321-328.
47. Whittom F, Jobin J, Simard PM, et al. Histochemical and morphological characteristics of the vastus lateralis muscle in patients with chronic obstructive pulmonary disease. Med Sci Sports Exerc 1998; 30:1467-1474. (Pubitemid 28465510)
48. Maltais F, Sullivan MJ, Leblanc P, et al. Altered expression of myosin heavy chain in the vastus lateralis muscle in patients with COPD. Eur Respir J 1999; 13:850-854.
49. Satta A, Migliori GB, Spanevello A, et al. Fibre types in skeletal muscles of chronic obstructive pulmonary disease patients related to respiratory function and exercise tolerance. Eur Respir J 1997; 10:2853-2860.
50. Jobin J, Maltais F, Doyon JF, et al. Chronic obstructive pulmonary disease: capillarity and fiber characteristics of skeletal muscle. J Cardiopulm Rehabil 1998; 18:432-437. (Pubitemid 29024891)
51. Jakobsson P, Jorfeldt L, Brundin A. Skeletal muscle metabolites and fibre types in patients with advanced chronic obstructive pulmonary disease (COPD), with and without chronic respiratory failure. Eur Respir J 1990; 3:192-196.
52. Hildebrand IL, Sylven C, Esbjornsson M, et al. Does chronic hypoxaemia induce transformations of fibre types? Acta Physiol Scand 1991; 141:435- 439.
53. Richardson RS, Leek BT, Gavin TP, et al. Reduced mechanical efficiency in chronic obstructive pulmonary disease but normal peak VO2 with small muscle mass exercise. Am J Respir Crit Care Med 2004; 169:89-96.
54. Gosker HR, Engelen MP, van Mameren H, et al. Muscle fiber type IIX atrophy is involved in the loss of fat-free mass in chronic obstructive pulmonary disease. Am J Clin Nutr 2002; 76:113-119.
55. Gosker HR, van Mameren H, van Dijk PJ, et al. Skeletal muscle fibre-type shifting and metabolic profile in patients with chronic obstructive pulmonary disease. Eur Respir J 2002; 19:617-625.
56. Booth FW, Gollnick PD. Effects of disuse on the structure and function of skeletal muscle. Med Sci Sports Exerc 1983; 15:415-420.
57. Itoh K, Moritani T, Ishida K, et al. Hypoxia-induced fibre type transformation in rat hindlimb muscles. Histochemical and electro-mechanical changes. Eur J Appl Physiol Occup Physiol 1990; 60:331-336.
58. Lindboe CF, Askevold F, Slettebo M. Changes in skeletal muscles of young women with anorexia nervosa. An enzyme histochemical study. Acta Neuropathol (Berl) 1982; 56:299-302.
59. Fiaccadori E, Del Canale S, Vitali P, et al. Skeletal muscle energetics, acidbase equilibrium and lactate metabolism in patients with severe hypercapnia and hypoxemia. Chest 1987; 92:883-887.
60. Sala E, Roca J, Marrades RM, et al. Effects of endurance training on skeletal muscle bioenergetics in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1999; 159:1726-1734.
61. Maltais F, Leblanc P, Whittom F, et al. Oxidative enzyme activities of the vastus lateralis muscle and the functional status in patients with COPD. Thorax 2000; 55:848-853.
62. Maltais F, Jobin J, Sullivan MJ, et al. Lower limb metabolic and hemodynamic responses during exercise in normal subjects and in COPD. J Appl Physiol 1998; 84:1573-1580.
63. Casaburi R, Patessio A, Ioli F, et al. Reductions in exercise lactic acidosis and ventilation as a result of exercise training in patients with obstructive lung disease. Am Rev Respir Dis 1991; 143:9-18.
64. Patessio A, Casaburi R, Carone M, et al. Comparison of gas exchange, lactate, and lactic acidosis thresholds in patients with chronic obstructive pulmonary disease. Am Rev Respir Dis 1993; 148:622-626.
65. Engelen MP, Casaburi R, Rucker R, et al. Contribution of the respiratory muscles to the lactic acidosis of heavy exercise in COPD. Chest 1995; 108:1246-1251.
66. Hunter GR, Newcomer BR, Larson-Meyer DE, et al. Muscle metabolic economy is inversely related to exercise intensity and type II myofiber distribution. Muscle Nerve 2001; 24:654-661.
67. Sauleda J, Garcia-Palmer F, Wiesner RJ, et al. Cytochrome oxidase activity and mitochondrial gene expression in skeletal muscle of patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1998; 157: 1413-1417.
68. Green HJ, Burnett ME, D'Arsigny CL, et al. Vastus lateralis Na(t)-K(t)- ATPase activity, protein, and isoform distribution in chronic obstructive pulmonary disease. Muscle Nerve 2009; 40:62-68.
69. Simard C, Maltais F, Leblanc P, et al. Mitochondrial and capillarity changes in vastus lateralis muscle of COPD patients: electron microscopy study. Med Sci Sports Exerc 1996; 28:S95.
70. Engelen MPKJ, Deutz NEP, Wouters EFM, et al. Enhanced levels of wholebody protein turnover in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2000; 162:1488-1492.
71. Morrison WL, Gibson J, Scrimegeour C, et al. Muscle wasting in emphysema. Clin Sci 1988; 75:415-420.
72. Aguilaniu B, Goldstein-Shapses S, Pajon A, et al. Muscle protein degradation in severely malnourished patients with chronic obstructive pulmonary disease subject to short-term total parenteral nutrition. JPEN J Parenter Enteral Nutr 1992; 16:248-254.
73. NaderGA. Molecular determinants of skeletal muscle mass: getting the 'AKT' together. Int J Biochem Cell Biol 2005; 37:1985-1996.
74. Frost RA, Lang CH. Protein kinase B/Akt: a nexus of growth factor and cytokine signaling in determining muscle mass. J Appl Physiol 2007; 103:378-387.
75. Creutzberg EC, Casaburi R. Endocrinological disturbances in chronic obstructive pulmonary disease. Eur Respir J Suppl 2003; 46:76s-80s.
76. Kamischke A, Kemper DE, Castel MA, et al. Testosterone levels in men with chronic obstructive pulmonary disease with or without glucocorticoid therapy. Eur Respir J 1998; 11:41-45.
77. Debigare R, Marquis K, Cote CH, et al. Catabolic/anabolic balance and muscle wasting in patients with COPD. Chest 2003; 124:83-89.
78. Crul T, Spruit MA, Gayan-Ramirez G, et al. Markers of inflammation and disuse in vastus lateralis of chronic obstructive pulmonary disease patients. Eur J Clin Invest 2007; 37:897-904.
79. Doucet M, Russell AP, Leger B, et al. Muscle atrophy and hypertrophy signaling in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2007; 176:261-269.
80. Plant PJ, Brooks D, Faughnan M, et al. Cellular markers of muscle atrophy in chronic obstructive pulmonary disease (COPD). Am J Respir Cell Mol Biol 2009; 11 June [Epub ahead of print].
81. Engelen MP, Wouters EF, Deutz NE, et al. Effects of exercise on amino acid metabolism in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2001; 163:859-864.
82. Schols AM, Wouters EF. Nutritional abnormalities and supplementation in chronic obstructive pulmonary disease. Clin Chest Med 2000; 21:753-762.
83. Schols AMWJ, Soeters PB, Mostert R, et al. Energy balance in chronic obstructive pulmonary disease. Am Rev Respir Dis 1991; 143:1248-1252.
84. Wilson DO, Donahoe M, Rogers RM, et al. Metabolic rate and weight loss in chronic obstructive lung disease. J Parenter Enteral Nutr 1990; 14:7-11.
85. Baarends EM, Schols AMWJ, Slebos DJ, et al. Metabolic and ventilatory response pattern to arm elevation in patients with COPD and healthy agematched subjects. Eur Respir J 1995; 8:1345-1351.
86. Baarends EM, Schols AMWJ, Pannemans DLE, et al. Total free living energy expenditure in patients with severe COPD. Eur Respir J 1997; 155:549-554.
87. Hugli O, Schutz Y, Fitting JW. The daily energy expenditure in stable chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1996; 153:294-300.
88. Pitta F, Troosters T, Spruit MA, et al. Characteristics of physical activities in daily life in chronic obstructive pulmonary disease. Am J Respir Crit CareMed 2005; 171:972-977.
89. Singh S, Morgan MD. Activity monitors can detect brisk walking in patients with chronic obstructive pulmonary disease. J Cardiopulm Rehabil 2001; 21:143-148.
90. Schonhofer B, Ardes P, GeibelM, et al. Evaluation of a movement detector to measure daily activity in patients with chronic lung disease. Eur Respir J 1997; 10:2814-2819.
91. Walker PP, Burnett A, Flavahan PW, et al. Lower limb activity and its determinants in COPD. Thorax 2008; 63:683-689.
92. Pitta F, Troosters T, Probst VS, et al. Physical activity and hospitalization for exacerbation of COPD. Chest 2006; 129:536-544.
93. Roca J, Weisman IM, Palange P, et al. Clinical exercise testing. In: Roca J, Whipp B, editors. Lausanne, Switzerland: European Respiratory Society; 1997. pp. 88-114.
94. Jaspers SR, Tischler ME. Atrophy and growth failure of rat hindlimb muscles in tail-cast suspension. J Appl Physiol 1984; 57:1472-1479.
95. Ferrando AA, Lane HW, Stuart CA, et al. Prolonged bed rest decreases skeletal muscle and whole body protein synthesis. Am J Physiol 1996; 270 (4 Pt 1):E627-E633.
96. Gibson JN, Halliday D, Morrison WL, et al. Decrease in human quadriceps muscle protein turnover consequent upon leg immobilization. Clin Sci (Lond) 1987; 72:503-509.
97. Maltais F, Leblanc P, Simard C, et al. Skeletal muscle adaptation to endurance training in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1996; 154:442-447. (Pubitemid 26269117)
98. Maltais F, Leblanc P, Jobin J, et al. Intensity of training and physiologic adaptation in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1997; 155:555-561. (Pubitemid 27085801)
99. Franssen FM, Wouters EF, Schols AM. The contribution of starvation, deconditioning and ageing to the observed alterations in peripheral skeletal muscle in chronic organ diseases. Clin Nutr 2002; 21:1-14.
100. Decramer M, De Bock V, Dom R. Functional and histologic picture of steroidinduced myopathy in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1996; 153:1958-1964.
101. Decramer M, Lacquet LM, Fagard R, et al. Corticosteroids contribute to muscle weakness in chronic airflow obstruction. Am J Respir Crit Care Med 1994; 150:11-16.
102. Hopkinson NS, Man WD, Dayer MJ, et al. Acute effect of oral steroids on muscle function in chronic obstructive pulmonary disease. Eur Respir J 2004; 24:137-142.
103. Preedy VR, Smith DM, Sugden PH. The effects of 6 h of hypoxia on protein synthesis in rat tissues in vivo and in vitro. Biochem J 1985; 228:179-185.
104. Green HJ, Sutton JR, Cymerman A, et al. Operation Everest II: adaptations in human skeletal muscle. J Appl Physiol 1989; 66:2454-2461.
105. Bigard AX, Brunet A, Guezennec CY, et al. Skeletal muscle changes after endurance training at high altitude. J Appl Physiol 1991; 71:2114-2121.
106. Howald H, Pette D, Simoneau JA, et al. Effects of chronic hypoxia on muscle enzyme activities. Int J Sports Med 1990; 11:S10-S14.
107. Pastoris O, Dossena M, Foppa P, et al. Modifications by chronic intermittent hypoxia and drug treatment on skeletal muscle metabolism. Neurochem Res 1995; 20:143-150.
108. Kwast KE, Hand SC. Acute depression of mitochondrial protein synthesis during anoxia: contributions of oxygen sensing, matrix acidification, and redox state. J Biol Chem 1996; 271:7313-7319.
109. Bigard AX, Sanchez H, Birot O, et al. Myosin heavy chain composition of skeletal muscles in young rats growing under hypobaric hypoxia conditions. J Appl Physiol 2000; 88:479-486.
110. Rennie MJ, Edwards RH, Emery PW, et al. Depressed protein synthesis is the dominant characteristic of muscle wasting and cachexia. Clin Physiol 1983; 3:387-398.
111. Takabatake M, Nakamura H, Abe H, et al. The relationship between chronic hypoxemia and activation of the tumor necrosis factor: a system in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2000; 161:1179-1184.
112. Heunks LM, Viñ a J, van Herwaarden CL, et al. Xanthine oxidase is involved in exercise-induced oxidative stress in chronic obstructive pulmonary disease. Am J Physiol 1999; 277 (6 Pt 2):R1697-R1704.
113. Semple PD, Beastall GH, Watson WS, et al. Serum testosterone depression associated with hypoxia in respiratory failure. Clin Sci (Lond) 1980; 58:105-106.
114. Rabinovich RA, Bastos R, Ardite E, et al. Mitochondrial dysfunction in COPD patients with low body mass index. Eur Respir J 2007; 29:643-650.
115. Cechetto D, Mainwood GW. Carbon dioxide and acid base balance in the isolated rat diaphragm. Pflugers Arch 1978; 376:251-258.
116. Trivedi B, Danforth WH. Effect of pH on the kinetics of frog muscle phosphofructokinase. J Biol Chem 1966; 241:4110-4112.
117. Mitch WE. Robert H Herman Memorial Award in Clinical Nutrition Lecture, 1997. Mechanisms causing loss of lean body mass in kidney disease. Am J Clin Nutr 1998; 67:359-366.
118. Sahlin K, Edstrom L, Sjoholm H. Fatigue and phosphocreatine depletion during carbon dioxide-induced acidosis in rat muscle. Am J Physiol 1983; 245:C15-C20.
119. Gertz I, Hedenstierna G, Hellers G, et al. Muscle metabolism in patients with chronic obstructive lung disease and acute respiratory failure. Clin Sci 1977; 52:395-403.
120. Mauro A. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 1961; 9:493-495.
121. Rudnicki MA, Le GF, McKinnell I, et al. The molecular regulation of muscle stem cell function. Cold Spring Harb Symp Quant Biol 2008; 73:323-331.
122. Sabourin LA, Rudnicki MA. The molecular regulation of myogenesis. Clin Genet 2000; 57:16-25.
123. Vogiatzis I, Stratakos G, Simoes DC, et al. Effects of rehabilitative exercise on peripheral muscle TNFalpha, IL-6, IGF-I and MyoD expression in patients with COPD. Thorax 2007; 62:950-956.
124. Lewis MI, Fournier M, Storer TW, et al. Skeletal muscle adaptations to testosterone and resistance training in men with COPD. J Appl Physiol 2007; 103:1299-1310.
125. Burnett D, Chamba A, Hill SL, et al. Neutrophils from subjects with chronic obstructive lung disease show enhanced chemotaxis and extracellular proteolysis. Lancet 1987; 2:1043-1046.
126. Noguera A, Busquets X, Sauleda J, et al. Expression of adhesion molecules and G proteins in circulating neutrophils in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1998; 158 (5 Pt 1):1664-1668.
127. Di Francia M, Barbier D, Mege J, et al. Tumor necrosis factor-alpha and weight loss in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1994; 150:1453-1455.
128. Piehl-Aulin K, Jones I, Lindvall B, et al. Increased serum inflammatory markers in the absence of clinical and skeletal muscle inflammation in patients with chronic obstructive pulmonary disease. Respiration 2009; 78:191-196.
129. Schols AM, Buurman WA, Staal van den Brekel AJ, et al. 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; 51:819-824.
130. Creutzberg EC, Schols AM, Weling-Scheepers CA, et al. Characterization of nonresponse to high caloric oral nutritional therapy in depleted patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2000; 161:745-752.
131. Rabinovich RA, Figueras M, Ardite E, et al. Increased tumour necrosis factoralpha plasma levels during moderate-intensity exercise in COPD patients. Eur Respir J 2003; 21:789-794.
132. Montes de OM, Torres SH, De SJ, et al. Skeletal muscle inflammation and nitric oxide in patients with COPD. Eur Respir J 2005; 26:390-397.
133. Barreiro E, Schols AM, Polkey MI, et al. Cytokine profile in quadriceps muscles of patients with severe COPD. Thorax 2008; 63:100-107.
134. Li YP, Schwartz RJ, Waddell IA, et al. Skeletal muscle myocytes undergo protein loss and reactive oxygen-mediated NF-kB activation in response to TNF-a. FASEB J 1998; 12:871-880.
135. Li YP, Atkins CM, Sweatt JD, et al. Mitochondria mediate tumor necrosis factor-alpha/NF-kappaB signaling in skeletal muscle myotubes. Antioxid Redox Signal 1999; 1:97-104.
136. Chandel NS, Trzyna WX, McClintock DS, et al. Role of oxidants in NF-kappa B activation and TNF-alpha gene transcription induced by hypoxia and endotoxin. J Immunol 2000; 165:1013-1021.
137. Agusti A, Morla M, Sauleda J, et al. NF-kappaB activation and iNOS upregulation in skeletal muscle of patients with COPD and low body weight. Thorax 2004; 59:483-487.
138. Nowak D, Antczak A, Krol M, et al. Increased content of hydrogen peroxide in the expired breath of cigarette smokers. Eur Respir J 1996; 9:652-657.
139. MacNee W, Rahman I. Oxidants and antioxidants as therapeutic targets in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1999; 160 (5 Pt 2):S58-S65.
140. Dekhuijzen PN, Aben KK, Dekker I, et al. Increased exhalation of hydrogen peroxide in patients with stable and unstable chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1996; 154 (3 Pt 1):813-816.
141. Thompson AB, Bohling T, Heires A, et al. Lower respiratory tract iron burden is increased in association with cigarette smoking. J Lab Clin Med 1991; 117:493-499.
142. Pratico D, Basili S, Vieri M, et al. Chronic obstructive pulmonary disease is associated with an increase in urinary levels of isoprostane F2alpha-III, an index of oxidant stress. Am J Respir Crit Care Med 1998; 158:1709-1714.
143. Rahman I, Skwarska E, MacNee W. Attenuation of oxidant/antioxidant imbalance during treatment of exacerbations of chronic obstructive pulmonary disease. Thorax 1997; 52:565-568.
144. Couillard A, Maltais F, Saey D, et al. Exercise-induced quadriceps oxidative stress and peripheral muscle dysfunction in COPD patients. Am J Respir Crit Care Med 2003; 167:1664-1669.
145. Allaire J, Maltais F, Leblanc P, et al. Lipofuscin accumulation in the vastus lateralis muscle in patients with chronic obstructive pulmonary disease. Muscle Nerve 2002; 25:383-389.
146. Couillard A, Koechlin C, Cristol JP, et al. Evidence of local exercise-induced systemic oxidative stress in chronic obstructive pulmonary disease patients. Eur Respir J 2002; 20:1123-1129.
147. van Helvoort HA, Heijdra YF, Heunks LM, et al. Supplemental oxygen prevents exercise-induced oxidative stress in muscle-wasted patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2006; 173:1122-1129.
148. Barreiro E, Rabinovich R, Marin-Corral J, et al. Chronic endurance exercise induces quadriceps nitrosative stress in patients with severe COPD. Thorax 2009; 64:13-19.
149. Reid MB. Plasticity in skeletal, cardiac, and smooth muscle. Invited review: redox modulation of skeletal muscle contraction: what we know and what we don't. J Appl Physiol 2001; 90:724-731.
150. Koechlin C, Couillard A, Simar D, et al. Does oxidative stress alter quadriceps endurance in chronic obstructive pulmonary disease? Am J Respir Crit Care Med 2004; 169:1022-1027.
151. Mitch WE, Goldberg AL. Mechanisms of muscle wasting. The role of the ubiquitin-proteasome pathway. N Engl J Med 1996; 335:1897-1905.
152. Buck M, Chojkier M. Muscle wasting and dedifferentiation induced by oxidative stress in a murine model of cachexia is prevented by inhibitors of nitric oxide synthesis and antioxidants. EMBO J 1996; 15:1753-1765.
153. Stadtman ER. Metal ion-catalyzed oxidation of proteins: biochemical mechanism and biological consequences. Free Radic Biol Med 1990; 9:315-325.
154. Barreiro E, Gea J, Corominas JM, et al. Nitric oxide synthases and protein oxidation in the quadriceps femoris of patients with chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol 2003; 29:771-778.
155. Barreiro E, Gea J, Matar G, et al. 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; 33:636-642.
156. Gosker HR, Schrauwen P, Hesselink MK, et al. Uncoupling protein-3 content is decreased in peripheral skeletal muscle of patients with COPD. Eur Respir J 2003; 22:88-93.
157. Russell AP, Somm E, Debigare R, et al. COPD results in a reduction in UCP3 long mRNA and UCP3 protein content in types I and IIa skeletal muscle fibers. J Cardiopulm Rehabil 2004; 24:332-339.
158. Gosker HR, Hesselink MK, Duimel H, et al. Reduced mitochondrial density in the vastus lateralis muscle of patients with COPD. Eur Respir J 2007; 30:73-79.
159. Picard M, Godin R, Sinnreich M, et al. The mitochondrial phenotype of peripheral muscle in chronic obstructive pulmonary disease: disuse or dysfunction? Am J Respir Crit Care Med 2008; 178:1040-1047.
160. Puente-Maestu L, Perez-Parra J, Godoy R, et al. Abnormal mitochondrial function in locomotor and respiratory muscles of COPD patients. Eur Respir J 2009; 33:1045-1052.
161. Puente-Maestu L, Perez-Parra J, Godoy R, et al. Abnormal transition pore kinetics and cytochrome C release in muscle mitochondria of patients with chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol 2009; 40:746-750.
162. Agusti AG, Sauleda J, Miralles C, et al. Skeletal muscle apoptosis and weight loss in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2002; 166:485-489. (Pubitemid 34895433)
163. Luquet S, Lopez-Soriano J, Holst D, et al. Peroxisome proliferator-activated receptor delta controls muscle development and oxidative capability. FASEB J 2003; 17:2299-2301.
164. Koves TR, Li P, An J, et al. Peroxisome proliferator-activated receptor-gamma co-activator 1alpha-mediated metabolic remodeling of skeletal myocytes mimics exercise training and reverses lipid-induced mitochondrial inefficiency. J Biol Chem 2005; 280:33588-33598.
165. Puigserver P, Spiegelman BM. Peroxisome proliferator-activated receptorgamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr Rev 2003; 24:78-90.
166. Lin J, Wu H, Tarr PT, et al. Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 2002; 418:797-801.
167. Remels AH, Schrauwen P, Broekhuizen R, et al. Peroxisome proliferatoractivated receptor expression is reduced in skeletal muscle in COPD. Eur Respir J 2007; 30:245-252.
168. Nici L, Donner C, Wouters E, et al. American Thoracic Society/European Respiratory Society statement on pulmonary rehabilitation. Am J Respir Crit Care Med 2006; 173:1390-1413.
169. Ries AL, Bauldoff GS, Carlin BW, et al. Pulmonary rehabilitation: joint ACCP/ AACVPR evidence-based clinical practice guidelines. Chest 2007; 131 (5 Suppl):4S-42S.
170. Lacasse Y, Brosseau L, Milne S, et al. Pulmonary rehabilitation for chronic obstructive pulmonary disease. Cochrane Database Syst Rev 2002: CD003793.
171. Mador MJ, Krawza M, Alhajhusian A, et al. Interval training versus continuous training in patients with chronic obstructive pulmonary disease. J Cardiopulm Rehabil Prev 2009; 29:126-132.
172. Franssen FM, Broekhuizen R, Janssen PP, et al. Effects of whole-body exercise training on body composition and functional capacity in normalweight patients with COPD. Chest 2004; 125:2021-2028.
173. Vogiatzis I, Terzis G, Nanas S, et al. Skeletal muscle adaptations to interval training in patients with advanced COPD. Chest 2005; 128:3838-3845.
174. Global Initiative for ChronicObstructive Lung Disease: updated 2004; 2007.
175. Ferreira IM, Brooks D, Lacasse Y, et al. Nutritional supplementation for stable chronic obstructive pulmonary disease. Cochrane Database Syst Rev 2005:CD000998.
176. Schols AMWJ. Weight loss is a reversible factor in the prognosis of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1998; 157: 1791-1797.
177. Prescott E, Almdal T, Mikkelsen KL, et al. Prognostic value of weight change in chronic obstructive pulmonary disease: results from the Copenhagen City Heart study. Eur Respir J 2002; 20:539-544.
178. Burdet L, de Muralt B, Schutz Y, et al. Administration of growth hormone to underweight patients with chronic obstructive pulmonary disease. A prospective, randomized, controlled study. Am J Respir Crit Care Med 1997; 156:1800-1806.
179. Schols AM, Soeters PB, Mostert R, et al. Physiologic effects of nutritional support and anabolic steroids in patients with chronic obstructive pulmonary disease. A placebo-controlled randomized trial. Am J Respir Crit Care Med 1995; 152:1268-1274.
180. Casaburi R, Bhasin S, Cosentino L, et al. Effects of testosterone and resistance training in men with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2004; 170:870-878.
181. Creutzberg EC, Wouters EF, Mostert R, et al. A role for anabolic steroids in the rehabilitation of patients with COPD? A double-blind, placebocontrolled, randomized trial. Chest 2003; 124:1733-1742.
182. Pape GS, Friedman M, Underwood LE, et al. The effect of growth hormone on weight gain and pulmonary function in patients with chronic obstructive lung disease. Chest 1991; 99:1495-1500.
183. Shapiro J, Christiana J, Frishman WH. Testosterone and other anabolic steroids as cardiovascular drugs. Am J Ther 1999; 6:167-174.