Mechanisms of striated muscle dysfunction during acute exacerbations of COPD

Journal of Applied Physiology

Volumn 114, Issue 9, 2013, Pages 1291-1299

  Gayan Ramirez, Ghislaine ^a   Decramer, Marc ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Limb muscles; Mitochondria; Oxidative stress; Proteolysis; Respiratory muscles; Striated muscles

Indexed keywords

AUTACOID; CORTICOSTEROID;

ACUTE DISEASE; ANIMAL; BREATHING MUSCLE; CHRONIC OBSTRUCTIVE LUNG DISEASE; HUMAN; LIMB; LIMB MUSCLES; LUNG GAS EXCHANGE; METABOLISM; MITOCHONDRION; MUSCLE STRENGTH; MUSCLE WEAKNESS; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PROTEIN DEGRADATION; REVIEW; SKELETAL MUSCLE; STRIATED MUSCLES;

LIMB MUSCLES; MITOCHONDRIA; OXIDATIVE STRESS; PROTEOLYSIS; RESPIRATORY MUSCLES; STRIATED MUSCLES;

ACUTE DISEASE; ADRENAL CORTEX HORMONES; ANIMALS; EXTREMITIES; HUMANS; INFLAMMATION MEDIATORS; MUSCLE STRENGTH; MUSCLE WEAKNESS; MUSCLE, SKELETAL; OXIDATIVE STRESS; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; PULMONARY GAS EXCHANGE; RESPIRATORY MUSCLES;

EID: 84878580388     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00847.2012     Document Type: Review

References (85)

1. Abdellaoui A, Préfaut C, Gouzi F, Couillard A, Coisy-Quivy M, Hugon G, Molinari N, Lafontaine T, Jonquet O, Laoudj-Chenivesse D, Hayot M. Skeletal muscle effects of electrostimulation after COPD exacerbation: a pilot study. Eur Respir J 38:781-788, 2011.
2. Allen DL, Linderman JK, Roy RR, Bigbee AJ, Grindeland RE, Mukku V, Edgerton VR. Apoptosis: a mechanism contributing to remodeling of skeletal muscle in response to hindlimb unweighting. Am J Physiol Cell Physiol 273:C579-C587, 1997.
3. Almagro P, Calbo E, Ochoa De Echagüen A, Barreiro B, Quintana S, Heredia JL, Garau J. Mortality after hospitalization for COPD. Chest 121:1441-1448, 2002. (Pubitemid 34499653)
4. Ansari K, Keaney N, Taylor I, Burns G, Farrow M. Muscle weakness, health status and frequency of exacerbations in chronic obstructive pulmonary disease. Postgrad Med J 88:372-376, 2012.
5. Argilés JM, Alvarez B, Carbó N, Busquets S, Van RM, López-Soriano FJ. The divergent effects of tumour necrosis factor-alpha on skeletal muscle: implications in wasting. Eur Cytokine Netw 11:552-559, 2000. (Pubitemid 32044238)
6. Awede B, Thissen J, Gailly P, Lebacq J. Regulation of IGF-I, IGFBP-4 and IGFBP-5 gene expression by loading in mouse skeletal muscle. FEBS Lett 461:263-267, 1999. (Pubitemid 29533344)
7. Barberà JA, Roca J, Ferrer A, Félez MA, Diaz O, Roger N, Rodriguez-Roisin R. Mechanisms of worsening gas exchange during acute exacerbations of chronic obstructive pulmonary disease. Eur Respir J 10:1285-1291, 1997. (Pubitemid 27278247)
8. Bellemare F, Grassino A. Force reserve of the diaphragm in patients with chronic obstructive pulmonary disease. J Appl Physiol 55:8-15, 1983. (Pubitemid 13075315)
9. Burge S, Wedzicha JA. COPD exacerbations: definitions and classifications. Eur Respir J Suppl 41:46s-53s, 2003. (Pubitemid 36648154)
10. Celli BR, Barnes PJ. Exacerbations of chronic obstructive pulmonary disease. Eur Respir J 29:1224-1238, 2007. (Pubitemid 46895385)
11. Chaplin EJ, Houchen L, Greening NJ, Harvey-Dunstan T, Morgan MD, Steiner MC, Singh SJ. Neuromuscular stimulation of quadriceps in patients hospitalised during an exacerbation of COPD: a comparison of low (35 Hz) and high (50 Hz) frequencies. Physiother Res Int In press.
12. Connors AF Jr, Dawson NV, Thomas C, Harrell FE Jr, Desbiens N, Fulkerson WJ, Kussin P, Bellamy P, Goldman L, Knaus WA. Outcomes following acute exacerbation of severe chronic obstructive lung disease. The SUPPORT investigators (Study to Understand Prognoses and Preferences for Outcomes and Risks of Treatments). Am J Respir Crit Care Med 154:959-967, 1996.
13. Cote CG, Dordelly LJ, Celli BR. Impact of COPD exacerbations on patient-centered outcomes. Chest 131:696-704, 2007. (Pubitemid 46446859)
14. Couillard A, Prefaut C. From muscle disuse to myopathy in COPD: potential contribution of oxidative stress. Eur Respir J 26:703-719, 2005. (Pubitemid 41448671)
15. 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 162:1239-1245, 2000.
16. Crul T, Spruit MA, Gayan-Ramirez G, Quarck R, Gosselink R, Troosters T, Pitta F, Decramer M. Markers of inflammation and disuse in vastus lateralis of chronic obstructive pulmonary disease patients. Eur J Clin Invest 37:897-904, 2007. (Pubitemid 350029204)
17. Crul T, Testelmans D, Spruit MA, Troosters T, Gosselink R, Geeraerts I, Decramer M, Gayan-Ramirez G. Gene expression profiling in vastus lateralis muscle during an acute exacerbation of COPD. Cell Physiol Biochem 25:491-500, 2010.
18. Curtis JR, Hudson LD. Emergent assessment and management of acute respiratory failure in COPD. Clin Chest Med 15:481-500, 1994. (Pubitemid 24289403)
19. De Troyer A, Wilson TA. Effect of acute inflation on the mechanics of the inspiratory muscles. J Appl Physiol 107:315-323, 2009.
20. 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 153:1958-1964, 1996. (Pubitemid 26187926)
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 10:417-423, 1997. (Pubitemid 27063862)
22. Dekhuijzen PNR, Decramer M. Steroid-induced myopathy and its significance to respiratory disease: a known disease rediscovered. Eur Respir J 5:997-1003, 1992.
23. Dentener MA, Creutzberg EC, Schols AM, Mantovani A, Van't Veer C, Buurman WA, Wouters EF. Systemic anti-inflammatory mediators in COPD: increase in soluble interleukin 1 receptor II during treatment of exacerbations. Thorax 56:721-726, 2001. (Pubitemid 32831700)
24. Dirks-Naylor AJ, Griffiths CL. Glucocorticoid-induced apoptosis and cellular mechanisms of myopathy. J Steroid Biochem Mol Biol 117:1-7, 2009.
25. Donaldson GC, Seemungal TA, Bhowmik A, Wedzicha JA. Relationship between exacerbation frequency and lung function decline in chronic obstructive pulmonary disease. Thorax 57:847-852, 2002. (Pubitemid 35178607)
26. Donaldson GC, Wilkinson TM, Hurst JR, Perera WR, Wedzicha JA. Exacerbations and time spent outdoors in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 171:446-452, 2005. (Pubitemid 40444244)
27. Favier FB, Benoit H, Freyssenet D. Cellular and molecular events controlling skeletal muscle mass in response to altered use. Pflugers Arch 456:587-600, 2008.
28. Ferrando AA, Lane HW, Stuart CA, Davis-Street J, Wolfe RR. Prolonged bed rest decreases skeletal muscle and whole body protein synthesis. Am J Physiol Endocrinol Metab 270:E627-E633, 1996.
29. Fiaccadori E, Del Canale S, Arduini U, Antonucci C, Coffrini E, Vitali P, Meley R, Guariglia A. Intracellular acid-base and electrolyte metabolism in skeletal muscle of patients with chronic obstructive lung disease and acute respiratory failure. Clin Sci (Lond) 71:703-712, 1986. (Pubitemid 17176169)
30. Fulco CS, Cymerman A, Muza SR, Rock PB, Pandolf KB, Lewis SF. Adductor pollicis muscle fatigue during acute and chronic altitude exposure and return to sea level. J Appl Physiol 77:179-183, 1994. (Pubitemid 24226132)
31. Gayan-Ramirez G, Vanderhoydonc F, Verhoeven G, Decramer M. Acute treatment with corticosteroids decreases IGF-I and IGF-II expression in the rat diaphragm and gastrocnemius. Am J Respir Crit Care Med 159:283-289, 1999. (Pubitemid 29036536)
32. Gertz I, Hedenstierna G, Hellers G, Wahren J. Muscle metabolism in patients with chronic obstructive lung disease and acute respiratory failure. Clin Sci Mol Med 52:396-403, 1977.
33. Girón R, Matesanz C, Garcia-Rio F, De Santiago E, Mancha A, Rodriguez-Salvanés F, Ancochea J. Nutritional state during COPD exacerbation: clinical and prognostic implications. Ann Nutr Metab 54:52-58, 2009.
34. Glover EI, Yasuda N, Tarnopolsky MA, Abadi A, Phillips SM. Little change in markers of protein breakdown and oxidative stress in humans in immobilization-induced skeletal muscle atrophy. Appl Physiol Nutr Metab 35:125-133, 2010.
35. Hopkinson NS, Tennant RC, Dayer MJ, Swallow EB, Hansel TT, Moxham J, Polkey MI. A prospective study of decline in fat free mass and skeletal muscle strength in chronic obstructive pulmonary disease. Respir Res 8:25, 2007.
36. Hurst JR, Vestbo J, Anzueto A, Locantore N, Müllerova H, Tal-Singer R, Miller B, Lomas DA, Agusti A, Macnee W, Calverley P, Rennard S, Wouters EF, Wedzicha JA. Susceptibility to exacerbation in chronic obstructive pulmonary disease. N Engl J Med 363:1128-1138, 2010.
37. Jagoe RT, Engelen MP. Muscle wasting and changes in muscle protein metabolism in chronic obstructive pulmonary disease. Eur Respir J Suppl 46:52s-63s, 2003. (Pubitemid 37351737)
38. Janssen S, Gayan-Ramirez G, Decramer M. IL-8 administration does not result in skeletal muscle wasting in rats (Abstract). Proc Am Thorac Soc 3:A256, 2006.
39. Janssen SP, Gayan-Ramirez G, Van Den Bergh A, Herijgers P, Maes K, Verbeken E, Decramer M. Interleukin-6 causes myocardial failure and skeletal muscle atrophy in rats. Circulation 111:996-1005, 2005. (Pubitemid 40354517)
40. Juan G, Calverley P, Talamo C, Schnader J, Roussos C. Effect of carbon dioxide on diaphragmatic function in human beings. N Engl J Med 310:874-879, 1984. (Pubitemid 14173179)
41. Kanner RE, Anthonisen NR, Connett JE. Lower respiratory illnesses promote FEV (1) decline in current smokers but not ex-smokers with mild chronic obstructive pulmonary disease: results from the lung health study. Am J Respir Crit Care Med 164:358-364, 2001. (Pubitemid 32778199)
42. Kent BD, Mitchell PD, McNicholas WT. Hypoxemia in patients with COPD: cause, effects, and disease progression. Int J Chron Obstruct Pulmon Dis 6:199-208, 2011.
43. Lewis MI. Apoptosis as a potential mechanism of muscle cachexia in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 166:434-436, 2002.
44. Lundby C, Calbet JA, Robach P. The response of human skeletal muscle tissue to hypoxia. Cell Mol Life Sci 66:3615-3623, 2009.
45. Lundby C, Pilegaard H, Van Hall G, Sander M, Calbet J, Loft S, Møller P. Oxidative DNA damage and repair in skeletal muscle of humans exposed to high-altitude hypoxia. Toxicology 192:229-236, 2003. (Pubitemid 37311413)
46. Mador MJ, Mogri M, Lewis M, Fournier M, Ray AD, Michlin C, Farkas G. Exercise capacity in hamsters with elastase-induced emphysema compared to normal controls. Respir Physiol Neurobiol 173:16-22, 2010.
47. Mador MJ, Wendel T, Kufel TJ. Effect of acute hypercapnia on diaphragmatic and limb muscle contractility. Am J Respir Crit Care Med 155:1590-1595, 1997. (Pubitemid 27216663)
48. Mattson JP, Delp MD, Poole DC. Differential effects of emphysema on skeletal muscle fibre atrophy in hamsters. Eur Respir J 23:703-707, 2004. (Pubitemid 38618139)
49. Mozdziak PE, Greaser ML, Schultz E. Myogenin, MyoD, and myosin heavy chain isoform expression following hindlimb suspension. Aviat Space Environ Med 70:511-516, 1999. (Pubitemid 29205468)
50. Murphy N, Bell C, Costello RW. Extending a home from hospital care programme for COPD exacerbations to include pulmonary rehabilitation. Respir Med 99:1297-1302, 2005. (Pubitemid 41245317)
51. Newell SZ, McKenzie DK, Gandevia SC. Inspiratory and skeletal muscle strength and endurance and diaphragmatic activation in patients with chronic airflow limitation. Thorax 44:903-912, 1989. (Pubitemid 19281531)
52. O'Donnell DE, Parker CM. COPD exacerbations. 3: Pathophysiology. Thorax 61:354-361, 2006.
53. 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)
54. Phillips SM, Glover EI, Rennie MJ. Alterations of protein turnover underlying disuse atrophy in human skeletal muscle. J Appl Physiol 107:645-654, 2009.
55. Pitta F, Troosters T, Probst V, Spruit MA, Decramer M, Gosselink R. Physical activity and hospitalization for exacerbation of COPD. Chest 129:536-544, 2006.
56. Plant PK, Owen JL, Elliott MW. Non-invasive ventilation in acute exacerbations of chronic obstructive pulmonary disease: long term survival and predictors of in-hospital outcome. Thorax 56:708-712, 2001. (Pubitemid 32831698)
57. Powers SK, Smuder AJ, Criswell DS. Mechanistic links between oxidative stress and disuse muscle atrophy. Antioxid Redox Signal 15:2519-2528, 2011.
58. Powers SK, Wiggs MP, Duarte J, Zergeroglu AM, Demirel HA. Mitochondrial signaling contributes to disuse muscle atrophy. Am J Physiol Endocrinol Metab 303:E31-E39, 2012.
59. Probst VS, Troosters T, Coosemans I, Spruit MA, Pitta FO, Decramer M, Gosselink R. Mechanisms of improvement in exercise capacity using a rollator in patients with COPD. Chest 126:1102-1107, 2004. (Pubitemid 39391238)
60. Puente-Maestu L, Pérez-Parra J, Godoy R, Moreno N, Tejedor A, González-Aragoneses F, Bravo JL, Alvarez FV, Camaño S, Agusti A. Abnormal mitochondrial function in locomotor and respiratory muscles of COPD patients. Eur Respir J 33:1045-1052, 2009.
61. Puhan M, Scharplatz M, Troosters T, Walters EH, Steurer J. Pulmonary rehabilitation following exacerbations of chronic obstructive pulmonary disease. Cochrane Database Syst Rev CD005305, 2009.
62. Purro A, Appendini L, Polillo C, Musso G, Taliano C, Mecca F, Colombo R, Carbone G. Mechanical determinants of early acute ventilatory failure in COPD patients: a physiologic study. Intensive Care Med 35:639-647, 2009.
63. Rabinovich RA, Bastos R, Ardite E, Llinàs L, Orozco-Levi M, Gea J, Vilaró J, Barberá JA, Rodriguez-Roisin R, Fernández-Checa JC, Roca J. Mitochondrial dysfunction in COPD patients with low body mass index. Eur Respir J 29:643-650, 2007. (Pubitemid 46554612)
64. Rahman I, Morrison D, Donaldson K, Macnee W. Systemic oxidative stress in asthma, COPD, and smokers. Am J Respir Crit Care Med 154:1055-1060, 1996.
65. Rahman I, Skwarska E, Macnee W. Attenuation of oxidant/antioxidant imbalance during treatment of exacerbations of chronic obstructive pulmonary disease. Thorax 52:565-568, 1997. (Pubitemid 27298512)
66. Reid MB. Response of the ubiquitin-proteasome pathway to changes in muscle activity. Am J Physiol Regul Integr Comp Physiol 288:R1423-R1431, 2005. (Pubitemid 40720691)
67. Rodriguez-Roisin R. Toward a consensus definition for COPD exacerbations. Chest 117:398S-401S, 2000. (Pubitemid 30314474)
68. Saudny-Unterberger H, Martin JG, Gray-Donald K. Impact of nutritional support on functional status during an acute exacerbation of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 156:794-799, 1997. (Pubitemid 27396417)
69. Schakman O, Gilson H, Kalista S, Thissen JP. Mechanisms of muscle atrophy induced by glucocorticoids. Horm Res 72 Suppl 1:36-41, 2009.
70. 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)
71. Seemungal TA, Donaldson GC, Paul EA, Bestall JC, Jeffries DJ, Wedzicha JA. Effect of exacerbation on quality of life in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 157:1418-1422, 1998.
72. Seymour JM, Moore L, Jolley CJ, Ward K, Creasey J, Steier JS, Yung B, Man WD, Hart N, Polkey MI, Moxham J. Outpatient pulmonary rehabilitation following acute exacerbations of COPD. Thorax 65:423-428, 2010.
73. Soler-Cataluna JJ, Martinez-Garcia MA, Roman SP, Salcedo E, Navarro M, Ochando R. Severe acute exacerbations and mortality in patients with chronic obstructive pulmonary disease. Thorax 60:925-931, 2005. (Pubitemid 41598207)
74. 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)
75. Tesch PA, Von Walden F, Gustafsson T, Linnehan RM, Trappe TA. Skeletal muscle proteolysis in response to short-term unloading in humans. J Appl Physiol 105:902-906, 2008.
76. Troosters T, Probst VS, Crul T, Pitta F, Gayan-Ramirez G, Decramer M, Gosselink R. Resistance training prevents deterioration in quadriceps muscle function during acute exacerbations of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 181:1072-1077, 2010.
77. Vermeeren MA, Schols AM, Wouters EF. Effects of an acute exacerbation on nutritional and metabolic profile of patients with COPD. Eur Respir J 10:2264-2269, 1997. (Pubitemid 27479547)
78. Vermeeren MA, Wouters EF, Geraerts-Keeris AJ, Schols AM. Nutritional support in patients with chronic obstructive pulmonary disease during hospitalization for an acute exacerbation; a randomized controlled feasibility trial. Clin Nutr 23:1184-1192, 2004. (Pubitemid 39243036)
79. Vescovo G, Volterrani M, Zennaro R, Sandri M, Ceconi C, Lorusso R, Ferrari R, Ambrosio GB, Dalla LL. Apoptosis in the skeletal muscle of patients with heart failure: investigation of clinical and biochemical changes. Heart 84:431-437, 2000.
80. Vianna LG, Koulouris N, Lanigan C, Moxham J. Effect of acute hypercapnia on limb muscle contractility in humans. J Appl Physiol 69:1486-1493, 1990. (Pubitemid 20361272)
81. Vilaró J, Ramirez-Sarmiento A, Martinez-Llorens JM, Mendoza T, Alvarez M, Sánchez-Cayado N, Vega A, Gimeno E, Coronell C, Gea J, Roca J, Orozco-Levi M. Global muscle dysfunction as a risk factor of readmission to hospital due to COPD exacerbations. Respir Med 104:1896-1902, 2010.
82. Vitacca M, Bianchi L, Barbano L, Ambrosino N. Lung and respiratory muscle function at discharge from a respiratory intensive care unit. Monaldi Arch Chest Dis 63:142-148, 2005. (Pubitemid 41700741)
83. Wedzicha JA, Seemungal TA, MacCallum PK, Paul EA, Donaldson GC, Bhowmik A, Jeffries DJ, Meade TW. Acute exacerbations of chronic obstructive pulmonary disease are accompanied by elevations of plasma fibrinogen and serum IL-6 levels. Thromb Haemost 84:210-215, 2000. (Pubitemid 30601465)
84. World Health Organization. Obesity: preventing and managing the global epidemic. Report of a WHO consultation. World Health Organ Tech Rep Ser 894:5-15, 2000.
85. Zanotti E, Felicetti G, Maini M, Fracchia C. Peripheral muscle strength training in bed-bound patients with COPD receiving mechanical ventilation: effect of electrical stimulation. Chest 124:292-296, 2003. (Pubitemid 36851365)