Skeletal muscle dysfunction in chronic obstructive pulmonary disease

Respiratory Research

Erkan Bozkanat¹  M Jeffery Mador² 

[1] GATA Camlica Hospital of Chest Diseases, Istanbul, Turkey;Division of Pulmonary, Critical Care & Sleep Medicine, State University of New York at Buffalo, Veterans Administration Medical Center, Buffalo, New York, USA

关键词: skeletal;    rehabilitation;    obstructive;    nutrition disorder;    muscle;    lung diseases;    exercise;   

Others  :  1227444
DOI  :  10.1186/rr60

 received in 2001-02-06, accepted in 2001-04-05,  发布年份 2001

【 摘 要 】

It has become increasingly recognized that skeletal muscle dysfunction is common in patients with chronic obstructive pulmonary disease (COPD). Muscle strength and endurance are decreased, whereas muscle fatigability is increased. There is a reduced proportion of type I fibers and an increase in type II fibers. Muscle atrophy occurs with a reduction in fiber cross-sectional area. Oxidative enzyme activity is decreased, and measurement of muscle bioenergetics during exercise reveals a reduced aerobic capacity. Deconditioning is probably very important mechanistically. Other mechanisms that may be of varying importance in individual patients include chronic hypercapnia and/or hypoxia, nutritional depletion, steroid usage, and oxidative stress. Potential therapies include exercise training, oxygen supplementation, nutritional repletion, and administration of anabolic hormones.

【 授权许可】

   
2001 BioMed Central Ltd

【 参考文献 】

• [1]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 1998, 158:629-634.
• [2]Hamilton AL, Killian KJ, Summers E, Jones NL: Muscle strength, symptom intensity, and exercise capacity in patients with car-diorespiratory disorders. Am J Respir Crit Care Med 1995, 152:2021-2031.
• [3]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.
• [4]Serres I, Gautier V, Varray A, Prefaut C: Impaired skeletal muscle endurance related to physical inactivity and altered lung function in COPD patients. Chest 1998, 113:900-905.
• [5]Zattara-Hartmann MC, Badier M, Guillot C, Tomei C, Jammes Y: Maximal force and endurance to fatigue of respiratory and skeletal muscles in chronic hypoxemic patients: the effects of oxygen breathing. Muscle Nerve 1995, 18:495-502.
• [6]Newell SZ, McKenzie DK, Gandevia SC: Inspiratory and skeletal muscle strength and endurance and diaphragmatic activation in patients with chronic airflow limitation. Thorax 1989, 44:903-912.
• [7]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.
• [8]Kufel TJ, Pineda LA, Mador MJ: Comparison of potentiated and unpotentiated twitches as an index of contractile fatigue [abstract]. Am J Respir Crit Care Med 1998, 157:A215.
• [9]Mador MJ, Kufel TJ, Pineda LA, Steinwald A, Aggarwal A, Upadhyay AM, Khan MA: Effect of pulmonary rehabilitation on quadriceps fatigability during exercise. Am J Respir Crit Care Med 2001, 163:930-935.
• [10]Mador MJ, Kufel TJ, Pineda LA: Quadriceps and diaphragmatic function after exhaustive cycle exercise in the healthy elderly. Am J Respir Crit Care Med 2000, 162:1760-1766.
• [11]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 1998, 30:1467-1474.
• [12]Maltais F, Sullivan MJ, LeBlanc P, Duscha BD, Schachat FH, Simard C, Blank JM, Jobin J: Altered expression of myosin heavy chain in the vastus lateralis muscle in patients with COPD. Eur Respir J 1999, 13:850-854.
• [13]Satta A, Migliori GB, Spanevello A, Neri M, Bottinelli R, Canepari M, Pellegrino MA, Reggiani C: Fiber types in skeletal muscles of chronic obstructive pulmonary disease patients related to respiratory function and exercise tolerance. Eur Respir J 1997, 10:2853-2860.
• [14]Jobin J, Maltais F, Doyon JF, LeBlanc P, Simard PM, Simard AA, Simard : Chronic obstructive pulmonary disease capillarity and fiber-type characteristics of skeletal muscle. J Cardiopulm Rehab 1998, 18:432-437.
• [15]Jakobsson P, Jorfeldt L, Brundin A: Skeletal muscle metabolites and fiber types in patients with advanced chronic obstructive pulmonary disease (COPD), with and without chronic respiratory failure. Eur Respir J 1990, 3:192-196.
• [16]Jakobsson P, Jorfeldt L, Henriksson J: Metabolic enzyme activity in the quadriceps femoris muscle in patients with severe chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1995, 151:374-377.
• [17]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 1996, 153:288-293.
• [18]Maltais F, LeBlanc P, Whittom F, Simard C, Marquis K, Belanger M, Breton M-J, Jobin J: Oxidative enzyme activities of the vastus lateralis muscle and the functional status in patients with COPD. Thorax 2000, 55:848-853.
• [19]Sauleda J, Garcia-Palmer F, Wiesner RJ, Tarraga S, Harting I, Tomas P, Gomez C, Saus C, Palou A, Agusti AGN: 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.
• [20]Sala E, Roca J, Marrades RM, Alonso J, Gonzalez de Suso JM, Moreno A, Barbera JA, Nadal J, de Jover L, Rodriguez-Roisin R, Wagner PD: Effects of endurance training on skeletal muscle bioenergetics in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1999, 159:1726-1734.
• [21]Kutsuzawa T, Shioya S, Kurita D, Haida M, Ohta Y, Yamabayashi H: Muscle energy metabolism and nutritional status in patients with chronic obstructive pulmonary disease. A 31P magnetic resonance study. Am J Respir Crit Care Med 1995, 152:647-652.
• [22]Tada H, Kato H, Misawa T, Sasaki F, Hayashi S, Takahashi Y, Kutsumi Y, Ishizaki T, Nakai T, Miyabo S: 31P-nuclear magnetic resonance evidence of abnormal skeletal muscle metabolism in patients with chronic lung disease and congestive heart failure. Eur Respir J 1992, 5:163-169.
• [23]Thompson CH, Davies RJO, Kemp GJ, Taylor DJ, Radda GK, Rajagopalan B: Skeletal muscle metabolism during exercise and recovery in patients with respiratory failure. Thorax 1993, 48:486-490.
• [24]Payen JF, Wuyam B, Levy P, Reutenauer H, Stieglitz P, Paramelle B, Le Bas J-F: Muscular metabolism during oxygen supplementation in patients with chronic hypoxemia. Am Rev Respir Dis 1993, 147:592-598.
• [25]Wuyam B, Payen JF, Levy P, Bensaidane H, Reutenauer H, LeBas JF, Benabid AL: Metabolism and aerobic capacity of skeletal muscle in chronic respiratory failure related to chronic obstructive pulmonary disease. Eur Respir J 1992, 5:157-162.
• [26]Casaburi R, Patessio A, Ioli F, Zanaboni S, Donner CF, Wasserman K: 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.
• [27]Maltais F, Jobin J, Sullivan MJ, Bernard S, Whittom F, Killian KJ, Desmeules M, Belanger M, LeBlanc P: Metabolic and hemodynamic responses of lower limb during exercise in patients with COPD. J Appl Physiol 1998, 84:1573-1580.
• [28]Saltin B, Gollnick PD: Skeletal muscle adaptability: significance for metabolism and performance. In: Handbook of Physiology: Skeletal Muscle. Edited by Peachey LD. Washington, DC: American Physiological Society, 1986, :555-631.
• [29]Casaburi R: Deconditioning. In: Pulmonary Rehabilitation. Edited by Fishman AP. New York: Marcel Dekker, 1996, :213-230.
• [30]Coyle EF, Martin WH, Bloomfield SA, Lowry DH, Holloszy JO: Effects of detraining on responses to submaximal exercise. J Appl Physiol 1985, 59:853-859.
• [31]Larsson L, Ansved T: Effects of long-term physical training and detraining on enzyme histochemical and functional skeletal muscle characteristic in man. Muscle Nerve 1985, 8:714-722.
• [32]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.
• [33]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.
• [34]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, 11:510-514.
• [35]Corbucci GG, Menichetti A, Cogliati A, Ruvolo C: Metabolic aspects of cardiac and skeletal muscle tissues in the condition of hypoxia, ischaemia and reperfusion induced by extra-corporeal circulation. Int J Tissue React 1995, 17:219-225.
• [36]Bigard AX, Brunet A, Guezennec CY, Monod H: Effects of chronic hypoxia and endurance training on muscle capillarity in rats. Pflugers Arch 1991, 419:225-229.
• [37]Hoppeler H, Kleinert E, Schlegel C, Claassen H, Howald H, Kayar SR, Cerretelli P: Morphological adaptations of human skeletal muscle to chronic hypoxia. Int J Sports Med 1990, 11(suppl 1):S3-S9.
• [38]Mador MJ, Wendel T, Kufel TJ: Effect of acute hypercapnia on diaphragmatic and limb muscle contractility. Am J Respir Crit Care Med 1997, 155:1590-1595.
• [39]Vianna LG, Koulouris N, Lanigan C, Moxham J: Effect of acute hypercapnia on limb muscle contractility in humans. J Appl Physiol 1990, 69:1486-1493.
• [40]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 1977, 52:396-403.
• [41]Fiaccadori E, Del Canale S, Vitali P, Coffrini E, Ronda N, Guariglia A: Skeletal muscle energetics, acid-base equilibrium and lactate metabolism in patients with severe hypercapnia and hypoxemia. Chest 1987, 92:883-887.
• [42]Schols AMWJ, Soeters PB, Dingemans AMC, Mostert R, Frantzen PJ, Wouters EFM: Prevalence and characteristics of nutritional depletion in patients with stable COPD eligible for pulmonary rehabilitation. Am Rev Respir Dis 1993, 147:1151-1156.
• [43]McLoughlin DM, Spargo E, Wassif WS, Newham DJ, Peters TJ, Lantos PL, Russell GF: Structural and functional changes in skeletal muscle in anorexia nervosa. Acta Neuropathol 1998, 95:632-640.
• [44]Engelen MAM, Schols AMWJ, Baken WC, Wesseling GJ, Wouters EFM: Nutritional depletion in relation to respiratory and peripheral skeletal muscle function in an outpatient population with chronic obstructive pulmonary disease. Eur Respir J 1994, 7:1793-1797.
• [45]Lopes J, Russell DM, Whitwell J, Jeejeebhoy KN: Skeletal muscle function in malnutrition. Am J Clin Nutr 1982, 36:602-610.
• [46]Essen B, Fohlin L, Thoren C, Saltin B: Skeletal muscle fiber types and sizes in anorexia nervosa patients. Clin Physiol 1981, 1:395-403.
• [47]Mijan de la Torre A, Madapallimattam A, Cross A, Armstrong RL, Jeejeebhoy KN: Effect of fasting, hypocaloric feeding, and refeeding on the energetics of stimulated rat muscle as assessed by nuclear magnetic resonance spectroscopy. J Clin Invest 1993, 92:114-121.
• [48]Russell DM, Atwood HL, Whittaker JS, Itakura T, Walker PM, Mickle DA, Jeejeebhoy KN: The effect of fasting and hypocaloric diets on the functional and metabolic characteristics of rat gastrocnemius muscle. Clin Sci 1984, 67:185-194.
• [49]Rahman I, Morrison D, Donaldson K, Macnee W: Systemic oxidative stress in asthma, COPD, and smokers. Am J Respir Crit Care Med 1996, 154:1055-1060.
• [50]Ji LL: Exercise, oxidative stress, and antioxidants. Am J Sports Med 1996, 24:520-524.
• [51]Giuliani A, Cestaro B: Exercise, free radical generation and vitamins. Eur J Cancer Prev 1997, 6:555-567.
• [52]Di Francia M, Barbier D, Mege JL, Orehek J: Tumor necrosis factor-a levels and weight loss in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1994, 150:1453-1455.
• [53]de Godoy I, Donahoe M, Calhoun WJ, Mancino J, Rogers RM: Elevated TNF-alpha production by peripheral blood monocytes of weight-losing COPD patients. Am J Respir Crit Care Med 1996, 153:633-637.
• [54]Howard H, Hoppeler H, Claassen H, Mathieu O, Stroub R: Influences of endurance training on the ultrastructural composition of the different muscle fiber types in humans. Pflugers Arch 1985, 403:369-376.
• [55]American College of Sports Medicine: The recommended quantity and quality of exercise for developing and maintaining cardiorespiratory and muscular fitness in healthy adults. Med Sci Sports Exerc 1990, 22:265-274.
• [56]Belman MJ, Kendregan BA: Exercise training fails to increase skeletal muscle enzymes in patients with chronic obstructive pulmonary disease. Am Rev Respir Dis 1981, 123:256-261.
• [57]Maltais F, LeBlanc P, Simard C, Jobin J, Berube C, Bruneau J, Carrier L, Belleau R: Skeletal muscle adaptation to endurance training in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1996, 154:442-447.
• [58]Serres I, Varray A, Vallet G, Micallef JP, Prefaut C: Improved skeletal muscle performance after individualized exercise training in patients with chronic obstructive pulmonary disease. J Cardiopulm Rehab 1997, 17:232-238.
• [59]Ries AL, Kaplan RM, Limberg TM, Prewit LM: Effect of pulmonary rehabilitation on physiologic and psychological outcomes in patients with chronic obstructive pulmonary disease. Ann Intern Med 1995, 122:823-832.
• [60]Goldstein RS, Gort ED, Stubbing D, Avendano MA, Guyatt GH: Randomized controlled trial of respiratory rehabilitation. Lancet 1994, 344:1394-1397.
• [61]Casaburi R, Porszasz J, Burns MR, Carithers E, Chang RSY, Cooper CB: Physiologic benefits of exercise training in rehabilitation of patients with severe chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1997, 155:1541-1551.
• [62]Casaburi R, Storer TW, Sullivan CS, Wasserman K: Evaluation of blood lactate elevation as an intensity criterion for exercise training. Med Sci Sports Exerc 1995, 27:852-862.
• [63]Lacasse Y, Guyatt GH, Goldstein RS: The components of a respiratory rehabilitation program. A systematic overview. Chest 1997, 111:1077-1088.
• [64]Bernard S, Whittom F, LeBlanc P, Jobin J, Belleau R, Berube C, Carrier G, Maltais F: Aerobic and strength training in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1999, 159:896-901.
• [65]Cotes JE, Gilson JC: Effect of oxygen on exercise ability in chronic respiratory insufficiency. Lancet 1956, 1:872-876.
• [66]Stein DA, Bradley BL, Miller WC: Mechanisms of oxygen effects on exercise in patients with chronic obstructive pulmonary disease. Chest 1982, 81:6-10.
• [67]Jakobsson P, Jorfeldt L: Long-term oxygen therapy may improve skeletal muscle metabolism in advanced chronic obstructive pulmonary disease patients with chronic hypoxemia. Respir Med 1995, 89:471-476.
• [68]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.
• [69]Rooyackers JM, Dekhuijzen PN, Van Herwaarden CL, Folgering HT: Training with supplemental oxygen in patients with COPD and hypoxemia at peak exercise. Eur Respir J 1997, 10:1278-1284.
• [70]Callahan CM, Dittus RS, Katz BP: Oral corticosteriod therapy for patients with stable chronic obstructive pulmonary disease. A meta-analysis. Ann Intern Med 1991, 114:216-223.
• [71]Niewoehner DE, Erbland ML, Deupree RH, Collins D, Gross NJ, Light RW, Anderson P, Morgan NA: Effect of systemic glucocorticoids on exacerbations of chronic obstructive pulmonary disease. Department of Veterans Affairs Cooperative Study Group. N Engl J Med 1999, 340:1941-1947.
• [72]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 1996, 153:961-966.
• [73]Shoup R, Dalsky G, Warner S, Davies M, Connors M, Khan M, Khan F, ZuWallack R: Body composition and health-related quality of life in patients with obstructive airways disease. Eur Respir J 1997, 10:1576-1580.
• [74]Ferreira IM, Brooks D, Lacasse Y, Goldstein RS: Nutritional support for individuals with COPD. A meta-analysis. Chest 2000, 117:672-678.
• [75]Donahoe M, Mancino J, Costantino J, Lebow H, Rogers RM: The effect of an aggressive nutritional support regimen on body composition in patients with severe COPD and weight loss [abstract]. Am J Respir Crit Care Med 1994, 149:A313.
• [76]Schols AMWJ, Soeters PB, Mostert R, Pluymers RJ, Wouters EFM: 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.
• [77]Cuneo RC, Salomon F, Wiles CM, Hesp R, Sonksen PH: Growth hormone treatment in growth hormone-deficient adults. I. Effects on muscle mass and strength. J Appl Physiol 1991, 70:688-694.
• [78]Cuneo RC, Salomon F, Wiles CM, Hesp R, Sonksen PH: Growth hormone treatment in growth hormone-deficient adults. Il. Effects on exercise performance. J Appl Physiol 1991, 70:695-700.
• [79]Taaffe DR, Pruitt L, Reim J, Hintz RL, Butterfield G, Hoffman AR, Marcus R: Effect of recombinant human growth hormone on the muscle strength response to resistance exercise in elderly men. J Clin Endocrinol Metab 1994, 79:1361-1366.
• [80]Papadakis MA, Grady D, Black D, Tierney MJ, Gooding GA, Schambelan M, Grunfeld C: Growth hormone replacement in healthy older men improves body composition but not functional ability. Ann Intern Med 1996, 124:708-716.
• [81]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.
• [82]Casaburi R, Carithers E, Tosolini J, Phillips J, Bhasin S: Randomized placebo controlled trial of growth hormone in severe COPD patients undergoing endurance exercise training [abstract]. Am J Respir Crit Care Med 1997, 155:A498.
• [83]Bhasin S, Storer TW, Berman N, Yarasheski KE, Clevenger B, Phillips J, Lee WP, Bunnell TJ, Casaburi R: Testosterone replacement increases fat-free mass and muscle size in hypogonadal men. J Clin Endocrinol Metab 1997, 82:407-413.
• [84]Sih R, Morley JE, Kaiser FE, Perry HM, Patrick P, Ross C: Testosterone replacement in older hypogonadal men: a 12-month randomized controlled trial. J Clin Endocrinol Metab 1997, 82:1661-1667.
• [85]Bhasin S, Storer TW, Berman N, Callegari C, Clevenger B, Phillips J, Bunnell TJ, Tricker R, Shirazi A, Casaburi R: The effects of supraphysiologic doses of testosterone on muscle size and strength in normal men. N Engl J Med 1996, 335:1-7.
• [86]Urban RJ, Bodenburg YH, Gilkison C, Foxworth J, Coggan AR, Wolfe RR, Ferrando A: Testosterone administration to elderly men increases skeletal muscle strength and protein synthesis. Am J Physiol 1995, 269:E820-E826.
• [87]Segal JM, Laghi F, Choe W, Desai K, Jubran A, Tobin MJ: Prevalence of hypogonadism in patients with chronic obstructive pulmonary disease [abstract]. Am J Respir Crit Care Med 2000, 161:A232.
• [88]Ferreira IM, Verreschi IT, Nery LE, Goldstein RS, Zamel N, Brooks D, Jardim JR: The influence of 6 months of oral anabolic steroids on body mass and respiratory muscles in undernourished COPD patients. Chest 1998, 114:19-28.