Comparative assessment of the quadriceps and the diaphragm in patients with COPD

Journal of Applied Physiology

Volumn 107, Issue 3, 2009, Pages 952-961

  Caron, Marc André ^a   Debigaré, Richard ^a   Dekhuijzen, P N Richard ^b   Maltais, François ^a  

^a LAVAL UNIVERSITY   (Canada)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Cell signaling; Chronic obstructive pulmonary disease; Muscle dysfunction

Indexed keywords

AEROBIC METABOLISM; CHRONIC OBSTRUCTIVE LUNG DISEASE; DIAPHRAGM; DIAPHRAGM DISEASE; HUMAN; MICROENVIRONMENT; MUSCLE ATROPHY; MUSCLE CAPILLARY; MUSCLE CELL; MUSCLE CONTRACTILITY; MUSCLE DISEASE; MUSCLE FATIGUE; MUSCLE HYPERTROPHY; MUSCLE INJURY; MUSCLE METABOLISM; MUSCLE MITOCHONDRION; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; QUADRICEPS FEMORIS MUSCLE; REVIEW;

EID: 67650090288     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00194.2009     Document Type: Review

References (97)

1. Agusti AG, Sauleda J, Miralles C, Gomez C, Togores B, Sala E, Batle S, Busquets X. Skeletal muscle apoptosis and weight loss in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 166: 485-489, 2002. (Pubitemid 34895433)
2. American Thoracic Society/European Respiratory 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: S1-S40, 1999.
3. Arora NS, Rochester DF. COPD and human diaphragm muscle dimensions. Chest 91: 719-724, 1987.
4. Barreiro E, de la Puente B, Minguella J, Corominas JM, Serrano S, Hussain SN, Gea J. Oxidative stress and respiratory muscle dysfunction in severe chronic obstructive pulmonary disease. Am J Respir Crit Care Med 171: 1116-1124, 2005. (Pubitemid 40663723)
5. Barreiro E, Rabinovich R, Marin-Corral J, Barbera JA, Gea J, Roca J. Chronic endurance exercise induces quadriceps nitrosative stress in patients with severe COPD. Thorax 64: 13-19, 2009.
6. Barreiro E, Schols AM, Polkey MI, Galdiz JB, Gosker HR, Swallow EB, Coronell C, Gea J. Cytokine profile in quadriceps muscles of patients with severe COPD. Thorax 63: 100-107, 2008. (Pubitemid 351236469)
7. Begin P, Grassino A. Inspiratory muscle dysfunction and chronic hypercapnia in chronic obstructive pulmonary disease. Am Rev Respir Dis 143: 905-912, 1991.
8. Bernard S, LeBlanc P, Whittom F, Carrier G, Jobin J, Belleau R, Maltais F. Peripheral muscle weakness in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 158: 629-634, 1998. (Pubitemid 28378196)
9. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, Pan ZQ, Valenzuela DM, DeChiara TM, Stitt TN, Yancopoulos GD, Glass DJ. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294: 1704-1708, 2001. (Pubitemid 33104839)
10. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawrence JC, Glass DJ, Yancopoulos GD. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3: 1014-1019, 2001. (Pubitemid 34428747)
11. Breen E, Tang K, Olfert M, Knapp A, Wagner P. Skeletal muscle capillarity during hypoxia: VEGF and its activation. High Alt Med Biol 9: 158-166, 2008. (Pubitemid 351913541)
12. 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 15: 1753-1765, 1996. (Pubitemid 26119211)
13. Burrows B. The bronchial and emphysematous types of chronic obstructive lung disease in London and Chicago. Aspen Emphysema Conf 9: 327-338, 1968.
14. Calnan DR, Brunet A. The FoxO code. Oncogene 27: 2276-2288, 2008.
15. Casaburi R, Bhasin S, Cosentino L, Porszasz J, Somfay A, Lewis MI, Fournier M, Storer TW. Effects of testosterone and resistance training in men with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 170: 870-878, 2004. (Pubitemid 39346482)
16. Chin ER, Olson EN, Richardson JA, Yang Q, Humphries C, Shelton JM, Wu H, Zhu W, Bassel-Duby R, Williams RS. A calcineurin-dependent transcriptional pathway controls skeletal muscle fiber type. Genes Dev 12: 2499-2509, 1998. (Pubitemid 28406953)
17. Clanton TL, Levine S. Respiratory muscle fiber remodeling in chronic hyperinflation: dysfunction or adaptation? J Appl Physiol 107: 324-335, 2009.
18. Close GL, Kayani A, Vasilaki A, McArdle A. Skeletal muscle damage with exercise and aging. Sports Med 35: 413-427, 2005. (Pubitemid 40806941)
19. Coronell C, Orozco-Levi M, Gea J. COPD and body weight in a Mediterranean population. Clin Nutr 21: 437; author reply 437; author reply 438, 2002.
20. Debigare R, Cote CH, Hould FS, LeBlanc P, Maltais F. In vitro and in vivo contractile properties of the vastus lateralis muscle in males with COPD. Eur Respir J 21: 273-278, 2003. (Pubitemid 36204542)
21. Debigare R, Maltais F, Cote CH, Michaud A, Caron MA, Mofarrahi M, Leblanc P, Hussain SN. Profiling of mRNA expression in quadriceps of patients with COPD and muscle wasting. COPD 5: 75-84, 2008. (Pubitemid 351549830)
22. Doucet M, Debigare R, Joanisse DR, Cote C, Leblanc P, Gregoire J, Deslauriers J, Vaillancourt R, Maltais F. Adaptation of the diaphragm and the vastus lateralis in mild-to-moderate COPD. Eur Respir J 24: 971-979, 2004. (Pubitemid 39642288)
23. Doucet M, Joanisse DR, Debigare R, Michaud A, Paré ME, Vaillancourt R, Fréchette E, Maltais F. Activation of the ubiquitin-proteasome pathway in the quadriceps compared to the diaphragm in patients with chronic obstructive pulmonary disease (COPD). Am J Respir Crit Care Med 177: A26, 2008.
24. Doucet M, Russell AP, Leger B, Debigare R, Joanisse DR, Caron MA, LeBlanc P, Maltais F. Muscle atrophy and hypertrophy signaling in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 176: 261-269, 2007. (Pubitemid 47195876)
25. Du J, Wang X, Miereles C, Bailey JL, Debigare R, Zheng B, Price SR, Mitch WE. Activation of caspase-3 is an initial step triggering accelerated muscle proteolysis in catabolic conditions. J Clin Invest 113: 115-123, 2004. (Pubitemid 38541638)
26. Farkas GA, Roussos C. Diaphragm in emphysematous hamsters: sarcomere adaptability. J Appl Physiol 54: 1635-1640, 1983.
27. Gea JG, Pasto M, Carmona MA, Orozco-Levi M, Palomeque J, Broquetas J. Metabolic characteristics of the deltoid muscle in patients with chronic obstructive pulmonary disease. Eur Respir J 17: 939-945, 2001. (Pubitemid 32600343)
28. Gomes-Marcondes MC, Tisdale MJ. Induction of protein catabolism and the ubiquitin-proteasome pathway by mild oxidative stress. Cancer Lett 180: 69-74, 2002. (Pubitemid 34242966)
29. Gomes MD, Lecker SH, Jagoe RT, Navon A, Goldberg AL. Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci USA 98: 14440-14445, 2001. (Pubitemid 33121410)
30. Gosker HR, Hesselink MK, Duimel H, Ward KA, Schols AM. Reduced mitochondrial density in the vastus lateralis muscle of patients with COPD. Eur Respir J 30: 73-79, 2007. (Pubitemid 47074009)
31. Gosker HR, Kubat B, Schaart G, van der Vusse GJ, Wouters EF, Schols AM. Myopathological features in skeletal muscle of patients with chronic obstructive pulmonary disease. Eur Respir J 22: 280-285, 2003. (Pubitemid 36986998)
32. Gosker HR, van Mameren H, van Dijk PJ, Engelen MP, van der Vusse GJ, Wouters EF, Schols AM. Skeletal muscle fibre-type shifting and metabolic profile in patients with chronic obstructive pulmonary disease. Eur Respir J 19: 617-625, 2002. (Pubitemid 34285157)
33. 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 71: 1033-1047, 2000.
34. Gosker HR, Zeegers MP, Wouters EF, Schols AM. Muscle fibre type shifting in the vastus lateralis of patients with COPD is associated with disease severity: a systematic review and meta-analysis. Thorax 62: 944-949, 2007.
35. Gray-Donald K, Gibbons L, Shapiro SH, Macklem PT, Martin JG. Nutritional status and mortality in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 153: 961-966, 1996. (Pubitemid 26081646)
36. Green HJ, Bombardier E, Burnett M, Iqbal S, D'Arsigny CL, O'Donnell DE, Ouyang J, Webb KA. Organization of metabolic pathways in vastus lateralis of patients with chronic obstructive pulmonary disease. Am J Physiol Regul Integr Comp Physiol 295: R935-R941, 2008.
37. 2+-sequestering properties in skeletal muscle in chronic obstructive pulmonary disease. Am J Physiol Cell Physiol 295: C350-C357, 2008.
38. 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 152: 2021-2031, 1995.
39. Howald H, Hoppeler H, Claassen H, Mathieu O, Straub R. Influences of endurance training on the ultrastructural composition of the different muscle fiber types in humans. Pflügers Arch 403: 369-376, 1985.
40. Jatta K, Eliason G, Portela-Gomes GM, Grimelius L, Caro O, Nilholm L, Sirjso A, Piehl-Aulin K, Abdel-Halim SM. Overexpression of von Hippel-Lindau protein in skeletal muscles of patients with chronic obstructive pulmonary disease. J Clin Pathol 62: 70-76, 2009.
41. Jobin J, Maltais F, Doyon JF, LeBlanc P, Simard PM, Simard AA, Simard C. Chronic obstructive pulmonary disease: capillarity and fiber-type characteristics of skeletal muscle. J Cardiopulm Rehabil 18: 432-437, 1998. (Pubitemid 29024891)
42. Kamei Y, Miura S, Suzuki M, Kai Y, Mizukami J, Taniguchi T, Mochida K, Hata T, Matsuda J, Aburatani H, Nishino I, Ezaki O. Skeletal muscle FOXO1 (FKHR) transgenic mice have less skeletal muscle mass, down-regulated Type I (slow twitch/red muscle) fiber genes, and impaired glycemic control. J Biol Chem 279: 41114-41123, 2004. (Pubitemid 39287713)
43. Larsson L. Histochemical characteristics of human skeletal muscle during aging. Acta Physiol Scand 117: 469-471, 1983.
44. Lecker SH, Jagoe RT, Gilbert A, Gomes M, Baracos V, Bailey J, Price SR, Mitch WE, Goldberg AL. Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J 18: 39-51, 2004. (Pubitemid 38076464)
45. Lecker SH, Solomon V, Mitch WE, Goldberg AL. Muscle protein breakdown and the critical role of the ubiquitin-proteasome pathway in normal and disease states. J Nutr 129: 227S-237S, 1999. (Pubitemid 29035981)
46. Levine S, Gregory C, Nguyen T, Shrager J, Kaiser L, Rubinstein N, Dudley G. Bioenergetic adaptation of individual human diaphragmatic myofibers to severe COPD. J Appl Physiol 92: 1205-1213, 2002. (Pubitemid 34670981)
47. Levine S, Kaiser L, Leferovich J, Tikunov B. Cellular adaptations in the diaphragm in chronic obstructive pulmonary disease. N Engl J Med 337: 1799 - 1806, 1997.
48. Lin J, Wu H, Tarr PT, Zhang CY, Wu Z, Boss O, Michael LF, Puigserver P, Isotani E, Olson EN, Lowell BB, Bassel-Duby R, Spiegelman BM. Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 418: 797-801, 2002. (Pubitemid 34894105)
49. Lotters F, van Tol B, Kwakkel G, Gosselink R. Effects of controlled inspiratory muscle training in patients with COPD: a meta-analysis. Eur Respir J 20: 570-576, 2002. (Pubitemid 35050147)
50. Maltais F, LeBlanc P, Whittom F, Simard C, Marquis K, Belanger M, Breton MJ, Jobin J. Oxidative enzyme activities of the vastus lateralis muscle and the functional status in patients with COPD. Thorax 55: 848-853, 2000. (Pubitemid 30744219)
51. Maltais F, Simard AA, Simard C, Jobin J, Desgagnes P, LeBlanc P. Oxidative capacity of the skeletal muscle and lactic acid kinetics during exercise in normal subjects and in patients with COPD. Am J Respir Crit Care Med 153: 288-293, 1996. (Pubitemid 26026864)
52. Marin-Corral J, Minguella J, Ramirez-Sarmiento AL, Hussain SN, Gea J, Barreiro E. Oxidized proteins and superoxide anion production in the diaphragm of severe COPD patients. Eur Respir J 2009.
53. Marquis K, Debigare R, Lacasse Y, LeBlanc P, Jobin J, Carrier G, Maltais F. 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 166: 809-813, 2002.
54. Martinez-Llorens J, Casadevall C, Lloreta J, Orozco-Levi M, Barreiro E, Broquetas J, Gea J. [Activation of satellite cells in the intercostal muscles of patients with chronic obstructive pulmonary disease]. Arch Bronconeumol 44: 239-244, 2008.
55. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, Wykoff CC, Pugh CW, Maher ER, Ratcliffe PJ. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399: 271-275, 1999.
56. McPherron AC, Lawler AM, Lee SJ. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387: 83-90, 1997.
57. Mostert R, Goris A, Weling-Scheepers C, Wouters EF, Schols AM. Tissue depletion and health related quality of life in patients with chronic obstructive pulmonary disease. Respir Med 94: 859-867, 2000. (Pubitemid 30734060)
58. Nguyen T, Shrager J, Kaiser L, Mei L, Daood M, Watchko J, Rubinstein N, Levine S. Developmental myosin heavy chains in the adult human diaphragm: coexpression patterns and effect of COPD. J Appl Physiol 88: 1446-1456, 2000. (Pubitemid 30217448)
59. Orozco-Levi M. Structure and function of the respiratory muscles in patients with COPD: impairment or adaptation? Eur Respir J Suppl 46: 41S-51S, 2003. (Pubitemid 37351736)
60. Orozco-Levi M, Ferrer M, Coronell C, Ramirez-Sarmiento AL, Lioreta J, Barreiro E, Broquetas J, Gea J. Evidence of sarcomere disruption and myofibrillar degeneration in the quadriceps muscle of stable COPD patients. Eur Respir J, 22 Suppl 45: 552S, 2003.
61. Orozco-Levi M, Gea J, Lloreta JL, Felez M, Minguella J, Serrano S, Broquetas JM. Subcellular adaptation of the human diaphragm in chronic obstructive pulmonary disease. Eur Respir J 13: 371-378, 1999. (Pubitemid 29086836)
62. 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 164: 1734-1739, 2001. (Pubitemid 33124167)
63. Ottenheijm CA, Heunks LM, Dekhuijzen PN. Diaphragm muscle fiber dysfunction in chronic obstructive pulmonary disease: toward a pathophysiological concept. Am J Respir Crit Care Med 175: 1233-1240, 2007. (Pubitemid 46905747)
64. Ottenheijm CA, Heunks LM, Dekhuijzen RP. Diaphragm adaptations in patients with COPD. Respir Res 9: 12, 2008.
65. Ottenheijm CA, Heunks LM, Hafmans T, van der Ven PF, Benoist C, Zhou H, Labeit S, Granzier HL, Dekhuijzen PN. Titin and diaphragm dysfunction in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 173: 527-534, 2006.
66. Ottenheijm CA, Heunks LM, Li YP, Jin B, Minnaard R, van Hees HW, Dekhuijzen PN. Activation of the ubiquitin-proteasome pathway in the diaphragm in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 174: 997-1002, 2006. (Pubitemid 44684448)
67. Ottenheijm CA, Heunks LM, Sieck GC, Zhan WZ, Jansen SM, Degens H, de Boo T, Dekhuijzen PN. Diaphragm dysfunction in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 172: 200-205, 2005. (Pubitemid 40981194)
68. Picard M, Godin R, Sinnreich M, Baril J, Bourbeau J, Perrault H, Taivassalo T, Burelle Y. The mitochondrial phenotype of peripheral muscle in chronic obstructive pulmonary disease: disuse or dysfunction? Am J Respir Crit Care Med 178: 1040-1047, 2008.
69. Puente-Maestu L, Perez-Parra J, Godoy R, Moreno N, Tejedor A, Gonzalez-Aragoneses F, Bravo JL, Villar F, Camano S, Agusti A. Abnormal mitochondrial function in locomotor and respiratory muscles of COPD patients. Eur Respir J 33: 1045-1052, 2009.
70. Rabinovich RA, Ardite E, Troosters T, Carbo N, Alonso J, Gonzalez de Suso JM, Vilaro J, Barbera JA, Polo MF, Argiles JM, Fernandez-Checa JC, Roca J. Reduced muscle redox capacity after endurance training in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 164: 1114-1118, 2001. (Pubitemid 33052236)
71. Radom-Aizik S, Kaminski N, Hayek S, Halkin H, Cooper DM, Ben-Dov I. Effects of exercise training on quadriceps muscle gene expression in chronic obstructive pulmonary disease. J Appl Physiol 102: 1976-1984, 2007.
72. Remels AH, Schrauwen P, Broekhuizen R, Willems J, Kersten S, Gosker HR, Schols AM. Peroxisome proliferator-activated receptor expression is reduced in skeletal muscle in COPD. Eur Respir J 30: 245-252, 2007. (Pubitemid 47194177)
73. Ribera F, N'Guessan B, Zoll J, Fortin D, Serrurier B, Mettauer B, Bigard X, Ventura-Clapier R, Lampert E. Mitochondrial electron transport chain function is enhanced in inspiratory muscles of patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 167: 873-879, 2003. (Pubitemid 36801776)
74. Sadoul P. Les cachexies respiratoires. Bull Physiopathol Resp 5: 3-11, 1969.
75. Sandri M. Signaling in muscle atrophy and hypertrophy. Physiology 23: 160-170, 2008.
76. Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A, Walsh K, Schiaffino S, Lecker SH, Goldberg AL. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117: 399-412, 2004. (Pubitemid 38534545)
77. Sauleda J, Garcia-Palmer F, Wiesner RJ, Tarraga S, Harting I, Tomas P, Gomez C, Saus C, Palou A, Agusti AG. Cytochrome oxidase activity and mitochondrial gene expression in skeletal muscle of patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 157: 1413-1417, 1998. (Pubitemid 28242070)
78. Schols AM, Broekhuizen R, Weling-Scheepers CA, Wouters EF. Body composition and mortality in chronic obstructive pulmonary disease. Am J Clin Nutr 82: 53-59, 2005. (Pubitemid 41716377)
79. 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 147: 1151-1156, 1993. (Pubitemid 23149871)
80. Schuelke M, Wagner KR, Stolz LE, Hubner C, Riebel T, Komen W, Braun T, Tobin JF, Lee SJ. Myostatin mutation associated with gross muscle hypertrophy in a child. N Engl J Med 350: 2682-2688, 2004. (Pubitemid 38788003)
81. Scott A, Wang X, Road JD, Reid WD. Increased injury and intramuscular collagen of the diaphragm in COPD: autopsy observations. Eur Respir J 27: 51-59, 2006. (Pubitemid 43092666)
82. Shi H, Scheffler JM, Pleitner JM, Zeng C, Park S, Hannon KM, Grant AL, Gerrard DE. Modulation of skeletal muscle fiber type by mitogen-activated protein kinase signaling. FASEB J 22: 2990-3000, 2008.
83. Similowski T, Yan S, Gauthier AP, Macklem PT, Bellemare F. Contractile properties of the human diaphragm during chronic hyperinflation. N Engl J Med 325: 917-923, 1991.
84. Spruit MA, Gosselink R, Troosters T, Kasran A, Gayan-Ramirez G, Bogaerts P, Bouillon R, Decramer M. Muscle force during an acute exacerbation in hospitalised patients with COPD and its relationship with CXCL8 and IGF-I. Thorax 58: 752-756, 2003. (Pubitemid 37094049)
85. Steuten LM, Creutzberg EC, Vrijhoef HJ, Wouters EF. COPD as a multicomponent disease: inventory of dyspnoea, underweight, obesity and fat free mass depletion in primary care. Prim Care Respir J 15: 84-91, 2006.
86. Stitt TN, Drujan D, Clarke BA, Panaro F, Timofeyva Y, Kline WO, Gonzalez M, Yancopoulos GD, Glass DJ. The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol Cell 14: 395-403, 2004. (Pubitemid 38591410)
87. Stubbings AK, Moore AJ, Dusmet M, Goldstraw P, West TG, Polkey MI, Ferenczi MA. Physiological properties of human diaphragm muscle fibres and the effect of chronic obstructive pulmonary disease. J Physiol 586: 2637-2650, 2008. (Pubitemid 351689817)
88. Tisdale MJ. Biology of cachexia. J Natl Cancer Inst 89: 1763-1773, 1997.
89. van Hees HW, Dekhuijzen PN, Heunks LM. Levosimendan enhances force generation of diaphragm muscle from patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 179: 41-47, 2009.
90. Vestbo J, Prescott E, Almdal T, Dahl M, Nordestgaard BG, Andersen T, Sorensen TI, Lange P. Body mass, fat-free body mass, and prognosis in patients with chronic obstructive pulmonary disease from a random population sample: findings from the Copenhagen City Heart Study. Am J Respir Crit Care Med 173: 79-83, 2006. (Pubitemid 43069791)
91. Vogiatzis I, Stratakos G, Simoes DC, Terzis G, Georgiadou O, Roussos C, Zakynthinos S. Effects of rehabilitative exercise on peripheral muscle TNFalpha, IL-6, IGF-I and MyoD expression in patients with COPD. Thorax 62: 950-956, 2007. (Pubitemid 350084492)
92. Wagner PD. Possible mechanisms underlying the development of cachexia in COPD. Eur Respir J 31: 492-501, 2008.
93. Whittom F, Jobin J, Simard PM, Leblanc P, Simard C, Bernard S, Belleau R, Maltais F. Histochemical and morphological characteristics of the vastus lateralis muscle in patients with chronic obstructive pulmonary disease. Med Sci Sports Exerc 30: 1467-1474, 1998. (Pubitemid 28465510)
94. Wijnhoven HJ, Heunks LM, Geraedts MC, Hafmans T, Vina JR, Dekhuijzen PN. Oxidative and nitrosative stress in the diaphragm of patients with COPD. Int J Chron Obstruct Pulmon Dis 1: 173-179, 2006.
95. Wijnhoven JH, Janssen AJ, van Kuppevelt TH, Rodenburg RJ, Dekhuijzen PN. Metabolic capacity of the diaphragm in patients with COPD. Respir Med 100: 1064-1071, 2006.
96. Wray CJ, Mammen JM, Hershko DD, Hasselgren PO. Sepsis upregulates the gene expression of multiple ubiquitin ligases in skeletal muscle. Int J Biochem Cell Biol 35: 698-705, 2003.
97. Wu AL, Kim JH, Zhang C, Unterman TG, Chen J. Forkhead box protein O1 negatively regulates skeletal myocyte differentiation through degradation of mammalian target of rapamycin pathway components. Endocrinology 149: 1407-1414, 2008.