Journal List > Tuberc Respir Dis > v.68(3) > 1001478

Kim, Lee, and Hwang: Skeletal Muscle Dysfunction in Patients with Chronic Obstructive Pulmonary Disease

Abstract

Patients with chronic obstructive pulmonary disease (COPD) frequently complain of dyspnea on exertion and reduced exercise capacity, which has been attributed to an increase in the work of breathing and in impaired of gas exchange. Although COPD primarily affects the pulmonary system, patients with COPD exhibit significant systemic manifestations of disease progression. These manifestations include weight loss, nutritional abnormalities, skeletal muscle dysfunction (SMD), cardiovascular problems, and psychosocial complications. It has been documented that SMD significantly contributes to a reduced exercise capacity in patients with COPD. Ventilatory and limb muscle in these patients show structural and functional alteration, which are influenced by several factors, including physical inactivity, hypoxia, smoking, aging, corticosteroid, malnutrition, systemic inflammation, oxidative stress, apoptosis, and ubiquitin-proteasome pathway activation. This article summarizes briefly the evidence and the clinical consequences of SMD in patients with COPD. In addition, it reviews contributing factors and therapeutic strategies.

Figures and Tables

Figure 1
The strength of the quadriceps, pectoralis major, and latissimus dorsi muscles in normal subjects and in chronic obstructive pulmonary disease (COPD). The strength of each muscle was significantly reduced in COPD patients compared with normal subjects. Values are mean±SD. *p<0.005. Adapted from 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.
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Figure 2
Computed tomography finding of quadriceps muscle found in chronic obstructive pulmonary disease (COPD) patient and in control subject. Adapted from 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.
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Figure 3
Fiber-type composition of the vastus lateralis muscle found in chronic obstructive pulmonary disease (COPD) patients and in normal subjects. When it compared with normal subjects, a significant reduction in the proportion of type I fiber with a corresponding increase in the proportion of type IIb fiber was observed in COPD patients. Values are mean±SD. *p<0.0005, p<0.05. Adapted from Whittom F, Jobin J, Simard PM, Leblanc P, Simard C, Bernard S, et al. Histochemical and morphological characteristics of the vastus lateralis muscle in patients with chronic obstructive pulmonary disease. Med Sci Sports Exerc 1998;30:1467-74.
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Figure 4
Proposed mechanisms of skeletal muscle dysfunction in patients with COPD. COPD: chronic obstructive pulmonary disease; UPP: ubiquitin proteasome pathway.
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Table 1
Structural and functional changes in COPD, which were shown in vastus lateralis muscle biopsies
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COPD: chronic obstructive pulmonary disease.

Table 2
Difference of structural and biochemical changes between diaphragm and limb muscles in COPD patients
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COPD: chronic obstructive pulmonary disease.

Table 3
Effects of oxidative stress in skeletal muscle dysfunction of COPD patients
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COPD: chronic obstructive pulmonary disease.

Table 4
Possible novel therapeutic agents
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References

1. 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.
2. Agustí AG, Noguera A, Sauleda J, Sala E, Pons J, Busquets X. Systemic effects of chronic obstructive pulmonary disease. Eur Respir J. 2003. 21:347–360.
3. Casaburi R, Gosselink R, Decramer M, Dekhuijzen RPN, Fournier M, Lewis MI, et al. 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. Maltais F, LeBlanc P, Jobin J, Casaburi R. Peripheral muscle dysfunction in chronic obstructive pulmonary disease. Clin Chest Med. 2000. 21:665–677.
5. Gosker HR, Wouters EF, van der Vusse GJ, Schols AM. Skeletal muscle dysfunction in chronic obstructive pulmonary disease and chronic heart failure: underlying mechanisms and therapy perspectives. Am J Clin Nutr. 2000. 71:1033–1047.
6. 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.
7. 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. 158:629–634.
8. Man WD, Hopkinson NS, Harraf F, Nikoletou D, Polkey MI, Moxham J. Abdominal muscle and quadriceps strength in chronic obstructive pulmonary disease. Thorax. 2005. 60:718–722.
9. Franssen FM, Broekhuizen R, Janssen PP, Wouters EF, Schols AM. Limb muscle dysfunction in COPD: effects of muscle wasting and exercise training. Med Sci Sports Exerc. 2005. 37:2–9.
10. Engelen MP, Schols AM, Does JD, Wouters EF. 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.
11. Jobin J, Maltais F, Doyon JF, LeBlanc P, Simard PM, Simard AA, et al. Chronic obstructive pulmonary disease: capillarity and fiber-type characteristics of skeletal muscle. J Cardiopulm Rehabil. 1998. 18:432–437.
12. Whittom F, Jobin J, Simard PM, Leblanc P, Simard C, Bernard S, 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.
13. Maltais F, Sullivan MJ, LeBlanc P, Duscha BD, Schachat FH, Simard C, et al. Altered expression of myosin heavy chain in the vastus lateralis muscle in patients with COPD. Eur Respir J. 1999. 13:850–854.
14. Aagaard P, Andersen JL. Correlation between contractile strength and myosin heavy chain isoform composition in human skeletal muscle. Med Sci Sports Exerc. 1998. 30:1217–1222.
15. Maltais F, LeBlanc P, Whittom F, Simard C, Marquis K, Bélanger M, et al. Oxidative enzyme activities of the vastus lateralis muscle and the functional status in patients with COPD. Thorax. 2000. 55:848–853.
16. Saey D, Michaud A, Couillard A, Côté CH, Mador MJ, LeBlanc P, et al. Contractile fatigue, muscle morphometry, and blood lactate in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2005. 171:1109–1115.
17. Wegner RE, Jörres RA, Kirsten DK, Magnussen H. Factor analysis of exercise capacity, dyspnoea ratings and lung function in patients with severe COPD. Eur Respir J. 1994. 7:725–729.
18. Foglio K, Carone M, Pagani M, Bianchi L, Jones PW, Ambrosino N. Physiological and symptom determinants of exercise performance in patients with chronic airway obstruction. Respir Med. 2000. 94:256–263.
19. 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. 146:935–940.
20. O'Donnell DE, Revill SM, Webb KA. Dynamic hyperinflation and exercise intolerance in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2001. 164:770–777.
21. 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. 1997. 10:417–423.
22. Marquis K, Debigaré R, Lacasse Y, LeBlanc P, Jobin J, Carrier G, 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.
23. 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. 62:115–120.
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. 168:706–713.
25. Levine S, Gregory C, Nguyen T, Shrager J, Kaiser L, Rubinstein N, et al. Bioenergetic adaptation of individual human diaphragmatic myofibers to severe COPD. J Appl Physiol. 2002. 92:1205–1213.
26. Levine S, Kaiser L, Leferovich J, Tikunov B. Cellular adaptations in the diaphragm in chronic obstructive pulmonary disease. N Engl J Med. 1997. 337:1799–1806.
27. Orozco-Levi M, Gea J, Lloreta JL, Félez M, Minguella J, Serrano S, et al. Subcellular adaptation of the human diaphragm in chronic obstructive pulmonary disease. Eur Respir J. 1999. 13:371–378.
28. Ottenheijm CA, Heunks LM, Sieck GC, Zhan WZ, Jansen SM, Degens H, et al. Diaphragm dysfunction in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2005. 172:200–205.
29. 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. 164:1734–1739.
30. Levine S, Nguyen T, Friscia M, Zhu J, Szeto W, Kucharczuk JC, et al. Parasternal intercostal muscle remodeling in severe chronic obstructive pulmonary disease. J Appl Physiol. 2006. 101:1297–1302.
31. Bloomfield SA. Changes in musculoskeletal structure and function with prolonged bed rest. Med Sci Sports Exerc. 1997. 29:197–206.
32. Tesch PA, Berg HE, Häggmark T, Ohlsén H, Dudley GA. Muscle strength and endurance following lower limb suspension in man. Physiologist. 1991. 34:S104–S106.
33. Lawler JM, Song W, Demaree SR. Hindlimb unloading increases oxidative stress and disrupts antioxidant capacity in skeletal muscle. Free Radic Biol Med. 2003. 35:9–16.
34. Ries AL, Bauldoff GS, Carlin BW, Casaburi R, Emery CF, Mahler DA, et al. Pulmonary Rehabilitation: Joint ACCP/AACVPR Evidence-Based Clinical Practice Guidelines. Chest. 2007. 131:4S–42S.
35. Paddon-Jones D, Sheffield-Moore M, Cree MG, Hewlings SJ, Aarsland A, Wolfe RR, et al. Atrophy and impaired muscle protein synthesis during prolonged inactivity and stress. J Clin Endocrinol Metab. 2006. 91:4836–4841.
36. Proctor DN, Sinning WE, Walro JM, Sieck GC, Lemon PW. Oxidative capacity of human muscle fiber types: effects of age and training status. J Appl Physiol. 1995. 78:2033–2038.
37. Couillard A, Koechlin C, Cristol JP, Varray A, Prefaut C. Evidence of local exercise-induced systemic oxidative stress in chronic obstructive pulmonary disease patients. Eur Respir J. 2002. 20:1123–1129.
38. 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. 2004. 24:129–136.
39. Gosker HR, Lencer NH, Franssen FM, van der Vusse GJ, Wouters EF, Schols AM. Striking similarities in systemic factors contributing to decreased exercise capacity in patients with severe chronic heart failure or COPD. Chest. 2003. 123:1416–1424.
40. Couillard A, Prefaut C. From muscle disuse to myopathy in COPD: potential contribution of oxidative stress. Eur Respir J. 2005. 26:703–719.
41. Gan WQ, Man SF, Senthilselvan A, Sin DD. Association between chronic obstructive pulmonary disease and systemic inflammation: a systematic review and a meta-analysis. Thorax. 2004. 59:574–580.
42. Li YP, Lecker SH, Chen Y, Waddell ID, Goldberg AL, Reid MB. TNF-alpha increases ubiquitin-conjugating activity in skeletal muscle by up-regulating UbcH2/E220k. FASEB J. 2003. 17:1048–1057.
43. Li YP, Schwartz RJ, Waddell ID, Holloway BR, Reid MB. Skeletal muscle myocytes undergo protein loss and reactive oxygen-mediated NF-kappaB activation in response to tumor necrosis factor alpha. FASEB J. 1998. 12:871–880.
44. Langen RC, Van Der Velden JL, Schols AM, Kelders MC, Wouters EF, Janssen-Heininger YM. Tumor necrosis factor-alpha inhibits myogenic differentiation through MyoD protein destabilization. FASEB J. 2004. 18:227–237.
45. Janssen SP, Gayan-Ramirez G, Van den Bergh A, Herijgers P, Maes K, Verbeken E, et al. Interleukin-6 causes myocardial failure and skeletal muscle atrophy in rats. Circulation. 2005. 111:996–1005.
46. Yende S, Waterer GW, Tolley EA, Newman AB, Bauer DC, Taaffe DR, et al. Inflammatory markers are associated with ventilatory limitation and muscle dysfunction in obstructive lung disease in well functioning elderly subjects. Thorax. 2006. 61:10–16.
47. Pinto-Plata VM, Müllerova H, Toso JF, Feudjo-Tepie M, Soriano JB, Vessey RS, et al. C-reactive protein in patients with COPD, control smokers and non-smokers. Thorax. 2006. 61:23–28.
48. Broekhuizen R, Wouters EF, Creutzberg EC, Schols AM. Raised CRP levels mark metabolic and functional impairment in advanced COPD. Thorax. 2006. 61:17–22.
49. Barreiro E, Schols AM, Polkey MI, Galdiz JB, Gosker HR, Swallow EB, et al. Cytokine profile in quadriceps muscles of patients with severe COPD. Thorax. 2008. 63:100–107.
50. Crul T, Spruit MA, Gayan-Ramirez G, Quarck R, Gosselink R, Troosters T, et al. Markers of inflammation and disuse in vastus lateralis of chronic obstructive pulmonary disease patients. Eur J Clin Invest. 2007. 37:897–904.
51. Petersen AM, Penkowa M, Iversen M, Frydelund-Larsen L, Andersen JL, Mortensen J, et al. Elevated levels of IL-18 in plasma and skeletal muscle in chronic obstructive pulmonary disease. Lung. 2007. 185:161–171.
52. Casadevall C, Coronell C, Ramírez-Sarmiento AL, Martínez-Llorens J, Barreiro E, Orozco-Levi M, et al. Upregulation of pro-inflammatory cytokines in the intercostal muscles of COPD patients. Eur Respir J. 2007. 30:701–707.
53. van der Poll T, Romijn JA, Endert E, Sauerwein HP. Effects of tumor necrosis factor on the hypothalamic-pituitary-testicular axis in healthy men. Metabolism. 1993. 42:303–307.
54. Van Vliet M, Spruit MA, Verleden G, Kasran A, Van Herck E, Pitta F, et al. Hypogonadism, quadriceps weakness, and exercise intolerance in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2005. 172:1105–1111.
55. Repine JE, Bast A, Lankhorst I. Oxidative Stress Study Group. Oxidative stress in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1997. 156:341–357.
56. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol. 2007. 39:44–84.
57. Dean RT, Fu S, Stocker R, Davies MJ. Biochemistry and pathology of radical-mediated protein oxidation. Biochem J. 1997. 324(Pt 1):1–18.
58. 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. 171:1116–1124.
59. Barreiro E, Gea J, Di Falco M, Kriazhev L, James S, Hussain SN. Protein carbonyl formation in the diaphragm. Am J Respir Cell Mol Biol. 2005. 32:9–17.
60. Allaire J, Maltais F, LeBlanc P, Simard PM, Whittom F, Doyon JF, et al. Lipofuscin accumulation in the vastus lateralis muscle in patients with chronic obstructive pulmonary disease. Muscle Nerve. 2002. 25:383–389.
61. Couillard A, Maltais F, Saey D, Debigaré R, Michaud A, Koechlin C, et al. Exercise-induced quadriceps oxidative stress and peripheral muscle dysfunction in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2003. 167:1664–1669.
62. Rabinovich RA, Ardite E, Troosters T, Carbo N, Alonso J, Gonzalez de Suso JM, et al. Reduced muscle redox capacity after endurance training in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2001. 164:1114–1118.
63. Engelen MP, Schols AM, Does JD, Deutz NE, Wouters EF. Altered glutamate metabolism is associated with reduced muscle glutathione levels in patients with emphysema. Am J Respir Crit Care Med. 2000. 161:98–103.
64. Andrade FH, Reid MB, Allen DG, Westerblad H. Effect of hydrogen peroxide and dithiothreitol on contractile function of single skeletal muscle fibres from the mouse. J Physiol. 1998. 509(Pt 2):565–575.
65. Barclay JK, Hansel M. Free radicals may contribute to oxidative skeletal muscle fatigue. Can J Physiol Pharmacol. 1991. 69:279–284.
66. 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.
67. Langen RC, Schols AM, Kelders MC, Van Der Velden JL, Wouters EF, Janssen-Heininger YM. Tumor necrosis factor-alpha inhibits myogenesis through redox-dependent and -independent pathways. Am J Physiol Cell Physiol. 2002. 283:C714–C721.
68. Koechlin C, Couillard A, Simar D, Cristol JP, Bellet H, Hayot M, et al. Does oxidative stress alter quadriceps endurance in chronic obstructive pulmonary disease? Am J Respir Crit Care Med. 2004. 169:1022–1027.
69. Sandri M. Apoptotic signaling in skeletal muscle fibers during atrophy. Curr Opin Clin Nutr Metab Care. 2002. 5:249–253.
70. Degens H, Swisher AK, Heijdra YF, Siu PM, Dekhuijzen PN, Alway SE. Apoptosis and Id2 expression in diaphragm and soleus muscle from the emphysematous hamster. Am J Physiol Regul Integr Comp Physiol. 2007. 293:R135–R144.
71. Agustí AG, Sauleda J, Miralles C, Gomez C, Togores B, Sala E, et al. Skeletal muscle apoptosis and weight loss in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2002. 166:485–489.
72. Cao PR, Kim HJ, Lecker SH. Ubiquitin-protein ligases in muscle wasting. Int J Biochem Cell Biol. 2005. 37:2088–2097.
73. Attaix D, Ventadour S, Codran A, Bechet D, Taillandier D, Combaret L. The ubiquitin-proteasome system and skeletal muscle wasting. Essays Biochem. 2005. 41:173–186.
74. Klaude M, Fredriksson K, Tjäder I, Hammarqvist F, Ahlman B, Rooyackers O, et al. Proteasome proteolytic activity in skeletal muscle is increased in patients with sepsis. Clin Sci (Lond). 2007. 112:499–506.
75. Baracos VE, DeVivo C, Hoyle DH, Goldberg AL. Activation of the ATP-ubiquitin-proteasome pathway in skeletal muscle of cachectic rats bearing a hepatoma. Am J Physiol. 1995. 268:E996–E1006.
76. Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A, et al. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell. 2004. 117:399–412.
77. Ottenheijm CA, Heunks LM, Li YP, Jin B, Minnaard R, van Hees HW, et al. Activation of the ubiquitin-proteasome pathway in the diaphragm in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2006. 174:997–1002.
78. Schols AM, Soeters PB, Dingemans AM, Mostert R, Frantzen PJ, Wouters EF. Prevalence and characteristics of nutritional depletion in patients with stable COPD eligible for pulmonary rehabilitation. Am Rev Respir Dis. 1993. 147:1151–1156.
79. Landbo C, Prescott E, Lange P, Vestbo J, Almdal TP. Prognostic value of nutritional status in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1999. 160:1856–1861.
80. Prescott E, Almdal T, Mikkelsen KL, Tofteng CL, Vestbo J, Lange P. Prognostic value of weight change in chronic obstructive pulmonary disease: results from the Copenhagen City Heart Study. Eur Respir J. 2002. 20:539–544.
81. McLoughlin DM, Spargo E, Wassif WS, Newham DJ, Peters TJ, Lantos PL, et al. Structural and functional changes in skeletal muscle in anorexia nervosa. Acta Neuropathol. 1998. 95:632–640.
82. Vermeeren MA, Schols AM, Wouters EF. Effects of an acute exacerbation on nutritional and metabolic profile of patients with COPD. Eur Respir J. 1997. 10:2264–2269.
83. Baarends EM, Schols AM, Westerterp KR, Wouters EF. Total daily energy expenditure relative to resting energy expenditure in clinically stable patients with COPD. Thorax. 1997. 52:780–785.
84. Ferreira IM, Brooks D, Lacasse Y, Goldstein RS. Nutritional support for individuals with COPD: a meta-analysis. Chest. 2000. 117:672–678.
85. Decramer M, Lacquet LM, Fagard R, Rogiers P. Corticosteroids contribute to muscle weakness in chronic airflow obstruction. Am J Respir Crit Care Med. 1994. 150:11–16.
86. Decramer M, de Bock V, Dom R. Functional and histologic picture of steroid-induced myopathy in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1996. 153:1958–1964.
87. Menconi M, Fareed M, O'Neal P, Poylin V, Wei W, Hasselgren PO. Role of glucocorticoids in the molecular regulation of muscle wasting. Crit Care Med. 2007. 35:S602–S608.
88. Kamischke A, Kemper DE, Castel MA, Lüthke M, Rolf C, Behre HM, et al. Testosterone levels in men with chronic obstructive pulmonary disease with or without glucocorticoid therapy. Eur Respir J. 1998. 11:41–45.
89. Ishihara A, Itoh K, Oishi Y, Itoh M, Hirofuji C, Hayashi H. Effects of hypobaric hypoxia on histochemical fibre-type composition and myosin heavy chain isoform component in the rat soleus muscle. Pflugers Arch. 1995. 429:601–606.
90. Howald H, Pette D, Simoneau JA, Uber A, Hoppeler H, Cerretelli P. Effect of chronic hypoxia on muscle enzyme activities. Int J Sports Med. 1990. 11:Suppl 1. S10–S14.
91. 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.
92. Koechlin C, Maltais F, Saey D, Michaud A, LeBlanc P, Hayot M, et al. Hypoxaemia enhances peripheral muscle oxidative stress in chronic obstructive pulmonary disease. Thorax. 2005. 60:834–841.
93. Takabatake N, Nakamura H, Abe S, Inoue S, Hino T, Saito H, et al. The relationship between chronic hypoxemia and activation of the tumor necrosis factor-alpha system in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2000. 161:1179–1184.
94. Semple PD, Beastall GH, Watson WS, Hume R. Serum testosterone depression associated with hypoxia in respiratory failure. Clin Sci (Lond). 1980. 58:105–106.
95. Montes de Oca M, Loeb E, Torres SH, De Sanctis J, Hernández N, Tálamo C. Peripheral muscle alterations in non-COPD smokers. Chest. 2008. 133:13–18.
96. Petersen AM, Magkos F, Atherton P, Selby A, Smith K, Rennie MJ, et al. Smoking impairs muscle protein synthesis and increases the expression of myostatin and MAFbx in muscle. Am J Physiol Endocrinol Metab. 2007. 293:E843–E848.
97. Hopkinson NS, Tennant RC, Dayer MJ, Swallow EB, Hansel TT, Moxham J, 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.
98. Young A, Stokes M, Crowe M. The size and strength of the quadriceps muscles of old and young men. Clin Physiol. 1985. 5:145–154.
99. Larsson L, Grimby G, Karlsson J. Muscle strength and speed of movement in relation to age and muscle morphology. J Appl Physiol. 1979. 46:451–456.
100. Tolep K, Higgins N, Muza S, Criner G, Kelsen SG. Comparison of diaphragm strength between healthy adult elderly and young men. Am J Respir Crit Care Med. 1995. 152:677–682.
101. Holloszy JO, Coyle EF. Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. J Appl Physiol. 1984. 56:831–838.
102. Hawley JA. Adaptations of skeletal muscle to prolonged, intense endurance training. Clin Exp Pharmacol Physiol. 2002. 29:218–222.
103. Mador MJ, Kufel TJ, Pineda LA, Steinwald A, Aggarwal A, Upadhyay AM, et al. Effect of pulmonary rehabilitation on quadriceps fatiguability during exercise. Am J Respir Crit Care Med. 2001. 163:930–935.
104. 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. 154:442–447.
105. Leggett RJ, Flenley DC. Portable oxygen and exercise tolerance in patients with chronic hypoxic cor pulmonale. Br Med J. 1977. 2:84–86.
106. Payen JF, Wuyam B, Levy P, Reutenauer H, Stieglitz P, Paramelle B, et al. Muscular metabolism during oxygen supplementation in patients with chronic hypoxemia. Am Rev Respir Dis. 1993. 147:592–598.
107. Mannix ET, Boska MD, Galassetti P, Burton G, Manfredi F, Farber MO. Modulation of ATP production by oxygen in obstructive lung disease as assessed by 31P-MRS. J Appl Physiol. 1995. 78:2218–2227.
108. Ferreira IM, Brooks D, Lacasse Y, Goldstein RS, White J. Nutritional supplementation for stable chronic obstructive pulmonary disease. Cochrane Database Syst Rev. 2002. (1):CD000998.
109. Cuneo RC, Salomon F, Wiles CM, Hesp R, Sonksen PH. Growth hormone treatment in growth hormone-deficient adults: II. Effects on exercise performance. J Appl Physiol. 1991. 70:695–700.
110. Pape GS, Friedman M, Underwood LE, Clemmons DR. The effect of growth hormone on weight gain and pulmonary function in patients with chronic obstructive lung disease. Chest. 1991. 99:1495–1500.
111. Burdet L, de Muralt B, Schutz Y, Pichard C, Fitting JW. 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.
112. Urban RJ, Bodenburg YH, Gilkison C, Foxworth J, Coggan AR, Wolfe RR, et al. Testosterone administration to elderly men increases skeletal muscle strength and protein synthesis. Am J Physiol. 1995. 269:E820–E826.
113. Schols AM, Soeters PB, Mostert R, Pluymers RJ, Wouters EF. 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.
114. Creutzberg EC, Wouters EF, Mostert R, Pluymers RJ, Schols AM. A role for anabolic steroids in the rehabilitation of patients with COPD? A double-blind, placebo-controlled, randomized trial. Chest. 2003. 124:1733–1742.
115. Ferreira IM, Verreschi IT, Nery LE, Goldstein RS, Zamel N, Brooks D, et al. The influence of 6 months of oral anabolic steroids on body mass and respiratory muscles in undernourished COPD patients. Chest. 1998. 114:19–28.
116. Ryall JG, Gregorevic P, Plant DR, Sillence MN, Lynch GS. Beta 2-agonist fenoterol has greater effects on contractile function of rat skeletal muscles than clenbuterol. Am J Physiol Regul Integr Comp Physiol. 2002. 283:R1386–R1394.
117. Hinkle RT, Hodge KM, Cody DB, Sheldon RJ, Kobilka BK, Isfort RJ. Skeletal muscle hypertrophy and anti-atrophy effects of clenbuterol are mediated by the beta2-adrenergic receptor. Muscle Nerve. 2002. 25:729–734.
118. Hinkle RT, Dolan E, Cody DB, Bauer MB, Isfort RJ. Phosphodiesterase 4 inhibition reduces skeletal muscle atrophy. Muscle Nerve. 2005. 32:775–781.
119. Sanders PM, Russell ST, Tisdale MJ. Angiotensin II directly induces muscle protein catabolism through the ubiquitin-proteasome proteolytic pathway and may play a role in cancer cachexia. Br J Cancer. 2005. 93:425–434.
120. Brink M, Price SR, Chrast J, Bailey JL, Anwar A, Mitch WE, et al. Angiotensin II induces skeletal muscle wasting through enhanced protein degradation and down-regulates autocrine insulin-like growth factor I. Endocrinology. 2001. 142:1489–1496.
121. Adigun AQ, Ajayi AA. The effects of enalapril-digoxin-diuretic combination therapy on nutritional and anthropometric indices in chronic congestive heart failure: preliminary findings in cardiac cachexia. Eur J Heart Fail. 2001. 3:359–363.
122. Mulligan K, Schambelan M. Anabolic treatment with GH, IGF-I, or anabolic steroids in patients with HIV-associated wasting. Int J Cardiol. 2002. 85:151–159.
123. Engelen MP, Schols AM. Altered amino acid metabolism in chronic obstructive pulmonary disease: new therapeutic perspective? Curr Opin Clin Nutr Metab Care. 2003. 6:73–78.
124. Appell HJ, Duarte JA, Soares JM. Supplementation of vitamin E may attenuate skeletal muscle immobilization atrophy. Int J Sports Med. 1997. 18:157–160.
125. Agacdiken A, Basyigit I, Ozden M, Yildiz F, Ural D, Maral H, et al. The effects of antioxidants on exercise-induced lipid peroxidation in patients with COPD. Respirology. 2004. 9:38–42.
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