Assessment of Limb Muscle Function

  • Roberto A. Rabinovich
  • Kim-Ly Bui
  • André Nyberg
  • Didier Saey
  • François MaltaisEmail author


Limb muscle dysfunction is frequent in COPD and contributes to its morbidity and mortality. Limb muscle dysfunction encompasses several manifestations including muscle atrophy and weakness, susceptibility to muscle fatigue and reduced oxidative capacity and mitochondrial function. Depending on the criteria used, up to a third of patients with COPD expresses some form of muscle dysfunction, including atrophy and weakness [1]. Although the extent of muscle atrophy and weakness is greater in more advanced disease, it is important to recognize that muscle dysfunction may also occur in early disease [1, 2]. The typical patients with COPD entering a pulmonary rehabilitation program have already lost about 30% of muscle mass and strength [3]. One important aspect of limb muscle dysfunction is that it is amenable to therapy, the most effective for this problem being exercise training [4–7]. Arguably, the most perverse consequence of muscle dysfunction is its negative effect on life expectancy. Parameters such as reduced mid-thigh cross-sectional area [8], fat-free mass [9], lower quadriceps strength [10] and vastus lateralis fibre-type shift [11] are predictors of mortality in subjects with COPD. Beyond its negative impact on survival, limb muscle dysfunction also contributes to exercise intolerance in COPD and poor quality of life in this disease. For example, quadriceps strength is a strong determinant of exercise capacity [12]. Premature leg fatigue reduces the ability of bronchodilators to enhance exercise tolerance [13, 14]. The links that exist between limb muscle function and relevant clinical outcomes in COPD stress out the importance for clinicians to carefully monitor body composition and muscle function when evaluating a patient with COPD, particularly before pulmonary rehabilitation where one goal of the intervention is to improve limb muscle function.


  1. 1.
    Seymour JM, Spruit MA, Hopkinson NS, Natanek SA, Man WD, Jackson A, Gosker HR, Schols AM, Moxham J, Polkey MI, Wouters EF. The prevalence of quadriceps weakness in COPD and the relationship with disease severity. Eur Respir J. 2010;36:81–8.PubMedCrossRefGoogle Scholar
  2. 2.
    Shrikrishna D, Patel M, Tanner RJ, Seymour JM, Connolly BA, Puthucheary ZA, Walsh SL, Bloch SA, Sidhu PS, Hart N, et al. Quadriceps wasting and physical inactivity in patients with COPD. Eur Respir J. 2012;40:1115–22.PubMedCrossRefGoogle Scholar
  3. 3.
    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;158:629–34.PubMedCrossRefGoogle Scholar
  4. 4.
    Bernard S, Whittom F, Leblanc P, Jobin J, Belleau R, Bérubé C, Carrier G, Maltais F. Aerobic and strength training in patients with COPD. Am J Respir Crit Care Med. 1999;159:896–901.PubMedCrossRefGoogle Scholar
  5. 5.
    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;159:1726–34.PubMedCrossRefGoogle Scholar
  6. 6.
    Ortega F, Toral J, Cejudo P, Villagomez R, Sánchez H, Castillo J, Montemayor T. Comparison of effects of strength and endurance training in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2002;166:669–74.PubMedCrossRefGoogle Scholar
  7. 7.
    Vogiatzis I, Terzis G, Nanas S, Stratakos G, Simoes DC, Georgiadou O, Zakynthinos S, Roussos C. Skeletal muscle adaptations to interval training in patients with advanced COPD. Chest. 2005;128:3838–45.PubMedCrossRefGoogle Scholar
  8. 8.
    Marquis K, Debigaré R, LeBlanc P, Lacasse Y, Jobin J, Carrier G, Maltais F. Mid-thigh muscle cross-sectional area is a better predictor of mortality than body mass index in patients with COPD. Am J Respir Crit Care Med. 2002;166:809–13.PubMedCrossRefGoogle Scholar
  9. 9.
    Schols AM, Broekhuizen R, Weling-Scheepers CA, Wouters EF. Body composition and mortality in chronic obstructive pulmonary disease. Am J Clin Nutr. 2005;82:53–9.PubMedCrossRefGoogle Scholar
  10. 10.
    Swallow EB, Reyes D, Hopkinson NS, Man WD, Porcher R, Cetti EJ, Moore AJ, Moxham J, Polkey MI. Quadriceps strength predicts mortality in patients with moderate to severe chronic obstructive pulmonary disease. Thorax. 2007;62:115–20.PubMedCrossRefGoogle Scholar
  11. 11.
    Patel MS, Natanek SA, Stratakos G, Pascual S, Martinez-Llorens J, Disano L, Terzis G, Hopkinson NS, Gea J, Vogiatzis I, et al. Vastus lateralis fiber shift is an independent predictor of mortality in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2014;190:350–2.PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    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. 1995;152:2021–31.PubMedCrossRefGoogle Scholar
  13. 13.
    Saey D, Debigaré R, LeBlanc P, Mador MJ, Côté C, Jobin J, Maltais F. Contractile leg fatigue after cycle exercise: a factor limiting exercise in patients with COPD. Am J Respir Crit Care Med. 2003;168:425–30.PubMedCrossRefGoogle Scholar
  14. 14.
    Deschênes D, Pepin V, Saey D, LeBlanc P, Maltais F. Locus of symptom limitation and exercise response to bronchodilation in chronic obstructive pulmonary disease. J Cardiopulm Rehabil Prev. 2008;28:208–14.PubMedCrossRefGoogle Scholar
  15. 15.
    Engelen MPKJ, Schols AMWJ, Baken WC, Wesseling GJ, Wouters EFM. Nutritional depletion in relation to respiratory and peripheral skeletal muscle function in out-patients with COPD. Eur Respir J. 1994;7:1793–7.PubMedCrossRefGoogle Scholar
  16. 16.
    Schols AMWJ, Soeters PB, Dingemans MC, 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;147:1151–6.PubMedCrossRefGoogle Scholar
  17. 17.
    Eid AA, Ionescu AA, Nixon LS, Lewis-Jenkins V, Mathews SB, Griffiths TL, Shale DJ. The inflammatory response and body composition in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2001;164:1414–8.PubMedCrossRefGoogle Scholar
  18. 18.
    Braun SR, Keim NL, Dixon RM, Clagnaz P, Anderegg A, Shrago ES. The prevalence and determinants of nutritional changes in chronic obstructive pulmonary disease. Chest. 1984;86:558–63.PubMedCrossRefGoogle Scholar
  19. 19.
    Gray-Donald K, Gibbons L, Shapiro SH, Martin JG. Effect of nutritional status on exercise with chronic obstructive pulmonary disease. Am Rev Respir Dis. 1989;140:1544–8.PubMedCrossRefGoogle Scholar
  20. 20.
    Schols AMWJ, Slangen J, Volovics L, Wouters EFM. Weight loss is a reversible factor in the prognosis of chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1998;157:1791–7.PubMedCrossRefGoogle Scholar
  21. 21.
    Gosselink R, Troosters T, Decramer M. Peripheral muscle weakness contributes to exercise limitation in COPD. Am J Respir Crit Care Med. 1996;153:976–80.PubMedCrossRefGoogle Scholar
  22. 22.
    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;71:733–8.PubMedCrossRefGoogle Scholar
  23. 23.
    Baarends EM, Schols AM, Mostert R, Wouters EF. Peak exercise response in relation to tissue depletion in patients with chronic obstructive pulmonary disease. Eur Respir J. 1997;10:2807–13.PubMedCrossRefGoogle Scholar
  24. 24.
    Kobayashi A, Yoneda T, Yoshikawa M, Ikuno M, Takenaka H, Fukuoka A, Narita N, Nezu K. The relation of fat-free mass to maximum exercise performance in patients with chronic obstructive pulmonary disease. Lung. 2000;178:119–27.PubMedCrossRefGoogle Scholar
  25. 25.
    Schols AMWJ, Mostert R, Soeters PB, Wouters EFM. Body composition and exercise performance in patients with chronic obstructive pulmonary disease. Thorax. 1991;46:695–9.PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Mostert R, Goris A, Weling-Scheepers C, Wouters EFM, Schols AMW. Tissue depletion and health related quality of life in patients with chronic obstructive pulmonary disease. Respir Med. 2000;94:859–67.PubMedCrossRefGoogle Scholar
  27. 27.
    Collins PF, Elia M, Stratton RJ. Nutritional support and functional capacity in chronic obstructive pulmonary disease: a systematic review and meta-analysis. Respirology. 2013;18:616–29.PubMedCrossRefGoogle Scholar
  28. 28.
    van Wetering CR, Hoogendoorn M, Broekhuizen R, Geraerts-Keeris GJ, De Munck DR, Rutten-van Molken MP, Schols AM. Efficacy and costs of nutritional rehabilitation in muscle-wasted patients with chronic obstructive pulmonary disease in a community-based setting: a prespecified subgroup analysis of the INTERCOM trial. J Am Med Dir Assoc. 2010;11:179–87.PubMedCrossRefGoogle Scholar
  29. 29.
    Steiner MC, Barton RL, Singh SJ, Morgan MD. Bedside methods versus dual energy X-ray absorptiometry for body composition measurement in COPD. Eur Respir J. 2002;19:626–31.PubMedCrossRefGoogle Scholar
  30. 30.
    Lerario MC, Sachs A, Lazaretti-Castro M, Saraiva LG, Jardim JR. Body composition in patients with chronic obstructive pulmonary disease: which method to use in clinical practice? Br J Nutr. 2006;96:86–92.PubMedCrossRefGoogle Scholar
  31. 31.
    Siri WE. Body composition from fluid spaces and density: analysis of methods. 1961. Nutrition. 1993;9:480–91; discussion 480, 492.PubMedGoogle Scholar
  32. 32.
    Lukaski HC, Johnson PE, Bolonchuk WW, Lykken GI. Assessment of fat-free mass using bioelectrical impedance measurements of the human body. Am J Clin Nutr. 1985;41:810–7.PubMedCrossRefGoogle Scholar
  33. 33.
    Schols AMWJ, Wouters EFM, Soeters PB, Westerterp KR. Body composition by bioelectrical-impedance analysis compared with deuterium dilution and skinfold anthropometry in patients with chronic obstructive pulmonary disease. Am J Clin Nutr. 1991;53:421–4.PubMedCrossRefGoogle Scholar
  34. 34.
    Rutten EP, Spruit MA, Wouters EF. Critical view on diagnosing muscle wasting by single-frequency bio-electrical impedance in COPD. Respir Med. 2010;104:91–8.PubMedCrossRefGoogle Scholar
  35. 35.
    Maltais F, Decramer M, Casaburi R, Barreiro E, Burelle Y, Debigare R, Dekhuijzen PN, Franssen F, Gayan-Ramirez G, Gea J, et al. An official American Thoracic Society/European Respiratory Society statement: update on limb muscle dysfunction in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2014;189:e15–62.PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Engelen MP, Schols AM, Heidendal GA, Wouters EF. Dual-energy X-ray absorptiometry in the clinical evaluation of body composition and bone mineral density in patients with chronic obstructive pulmonary disease. Am J Clin Nutr. 1998;68:1298–303.PubMedCrossRefGoogle Scholar
  37. 37.
    Mathur S, Takai KP, Macintyre DL, Reid D. Estimation of thigh muscle mass with magnetic resonance imaging in older adults and people with chronic obstructive pulmonary disease. Phys Ther. 2008;88:219–30.PubMedCrossRefGoogle Scholar
  38. 38.
    Seymour JM, Ward K, Sidhu PS, Puthucheary Z, Steier J, Jolley CJ, Rafferty G, Polkey MI, Moxham J. Ultrasound measurement of rectus femoris cross-sectional area and the relationship with quadriceps strength in COPD. Thorax. 2009;64:418–23.PubMedCrossRefGoogle Scholar
  39. 39.
    Maddocks M, Shrikrishna D, Vitoriano S, Natanek SA, Tanner RJ, Hart N, Kemp PR, Moxham J, Polkey MI, Hopkinson NS. Skeletal muscle adiposity is associated with physical activity, exercise capacity and fibre shift in COPD. Eur Respir J. 2014;44:1188–98.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Robles PG, Sussman MS, Naraghi A, Brooks D, Goldstein RS, White LM, Mathur S. Intramuscular fat infiltration contributes to impaired muscle function in COPD. Med Sci Sports Exerc. 2015;47:1334–41.PubMedCrossRefGoogle Scholar
  41. 41.
    Roig M, Eng JJ, MacIntyre DL, Road JD, Reid WD. Deficits in muscle strength, mass, quality, and mobility in people with chronic obstructive pulmonary disease. J Cardiopulm Rehabil Prev. 2011;31:120–4.PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Robles PG, Mathur S, Janaudis-Fereira T, Dolmage TE, Goldstein RS, Brooks D. Measurement of peripheral muscle strength in individuals with chronic obstructive pulmonary disease: a systematic review. J Cardiopulm Rehabil Prev. 2011;31:11–24.PubMedCrossRefGoogle Scholar
  43. 43.
    WDc M, Moxham J, Polkey MI. Magnetic stimulation for the measurement of respiratory and skeletal muscle function. Eur Respir J. 2004;24:846–60.CrossRefGoogle Scholar
  44. 44.
    Nyberg A, Saey D, Maltais F. Why and how limb muscle mass and function should be measured in patients with COPD. Ann Am Thorac Soc. 2015;12(9):1269–77.PubMedCrossRefGoogle Scholar
  45. 45.
    Saey D, Troosters T. Measuring skeletal muscle strength and endurance, from bench to bedside. Clin Invest Med. 2008;31:307–11.CrossRefGoogle Scholar
  46. 46.
    Meldrum D, Cahalane E, Conroy R, Fitzgerald D, Hardiman O. Maximum voluntary isometric contraction: reference values and clinical application. Amyotroph Lateral Scler. 2007;8:47–55.PubMedCrossRefGoogle Scholar
  47. 47.
    Andrews AW, Thomas MW, Bohannon RW. Normative values for isometric muscle force measurements obtained with hand-held dynamometers. Phys Ther. 1996;76:248–59.PubMedCrossRefGoogle Scholar
  48. 48.
    Danneskiold-Samsøe B, Bartels EM, Bülow PM, Lund H, Stockmarr A, Holm CC, Wätjen I, Appleyard M, Bliddal H. Isokinetic and isometric muscle strength in a healthy population with special reference to age and gender. Acta Physiol. 2009;197:1–68.CrossRefGoogle Scholar
  49. 49.
    Thompson WR, Gordon NF, Pescatello LS, et al. ACSM’s guidelines for exercise testing and prescription. Philadelphia: Wolters Kluwer/Lippincott Williams & Wilkins; 2010.Google Scholar
  50. 50.
    Levinger I, Goodman C, Hare DL, Jerums G, Toia D, Selig S. The reliability of the 1RM strength test for untrained middle-aged individuals. J Sci Med Sport. 2009;12:310–6.PubMedCrossRefGoogle Scholar
  51. 51.
    Wallerstein LF, Barroso R, Tricoli V, Mello MT, Ugrinowitsch C. The influence of familiarization sessions on the stability of ramp and ballistic isometric torque in older adults. J Aging Phys Act. 2010;18:390–400.PubMedCrossRefGoogle Scholar
  52. 52.
    Andreacci JL, LeMura LM, Cohen SL, Ea U, Sa C, Von Duvillard SP. The effects of frequency of encouragement on performance during maximal exercise testing. J Sports Sci. 2002;20:345–52.PubMedCrossRefGoogle Scholar
  53. 53.
    Peacock B, Westers T, Walsh S, Nicholson K. Feedback and maximum voluntary contraction. Ergonomics. 1981;24:223–8.PubMedCrossRefGoogle Scholar
  54. 54.
    Kellis E. Resistive eccentric exercise: effects of visual feedback on maximum moment of knee extensors and flexors. J Orthop Sports Phys Ther. 1996;23(2):120–4.PubMedCrossRefGoogle Scholar
  55. 55.
    Hald RD, Bottjen EJ. Effect of visual feedback on maximal and submaximal lsokinetic test measurements of normal quadricem—and hamstrings. J Orthop Sports Phys Ther. 1987;9:86–93.PubMedCrossRefGoogle Scholar
  56. 56.
    Jung MC, Hallbeck MS. Quantification of the effects of instruction type, verbal encouragement, and visual feedback on static and peak handgrip strength. Int J Ind Ergon. 2004;34:367–74.CrossRefGoogle Scholar
  57. 57.
    Amagliani RM, Peterella JK, Jung AP. Type of encouragement influences peak muscle force in college-age women. Int J Exerc Sci. 2015;3(4):165–73.Google Scholar
  58. 58.
    Campenella B, Mattacola CG, Kimura IF. Effect of visual feedback and verbal encouragement on concentric quadriceps and hamstrings peak torque of males and females. Isokinet Exerc Sci. 2000;8:1–6.Google Scholar
  59. 59.
    Man WDC, Soliman MGG, Nikoletou D, Harris ML, Rafferty GF, Mustfa N, Polkey MI, Moxham J. Non-volitional assessment of skeletal muscle strength in patients with chronic obstructive pulmonary disease. Thorax. 2003;58:665–9.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Han T-R, Shin H-I, Kim I-S. Magnetic stimulation of the quadriceps femoris muscle: comparison of pain with electrical stimulation. Am J Phys Med Rehabil. 2006;85:593–9.PubMedCrossRefGoogle Scholar
  61. 61.
    Polkey MI, Kyroussis D, Hamnegard CH, Mills GH, Green M, Moxham J. Quadriceps strength and fatigue assessed by magnetic stimulation of the femoral nerve in man. Muscle Nerve. 1996;19:549–55.PubMedCrossRefGoogle Scholar
  62. 62.
    CR J, Chen RC. Quadriceps strength assessed by magnetic stimulation of femoral nerve in patients with chronic obstructive pulmonary disease. Chin Med J. 2011;124:2309–15.Google Scholar
  63. 63.
    Wright W. Muscle training in the treatment of infantile paralysis. Boston Med Surgery. 1912;167:567.CrossRefGoogle Scholar
  64. 64.
    Hermans G, Clerckx B, Vanhullebusch T, Segers J, Vanpee G, Robbeets C, Casaer MP, Wouters P, Gosselink R, Van Den Berghe G. Interobserver agreement of Medical Research Council sum-score and handgrip strength in the intensive care unit. Muscle Nerve. 2012;45:18–25.PubMedCrossRefGoogle Scholar
  65. 65.
    Hough CL, Lieu BK, Caldwell ES. Manual muscle strength testing of critically ill patients: feasibility and interobserver agreement. Crit Care. 2011;15:R43.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Frese E, Brown M, Norton BJ. Clinical reliability of manual muscle testing. Phys Ther. 1987;67:1072–6.PubMedCrossRefGoogle Scholar
  67. 67.
    Bohannon RW. Measuring knee extensor muscle strength. Am J Phys Med Rehabil. 2001;80:13–8.PubMedCrossRefGoogle Scholar
  68. 68.
    Brown L, Weir JP. ASEP procedures recommendation I: accurate assessment of muscular strength and power. J Exerc Physiol Online. 2001;4:1–21.Google Scholar
  69. 69.
    O'Shea SD, Taylor NF, Paratz JD. Measuring muscle strength for people with chronic obstructive pulmonary disease: retest reliability of hand-held dynamometry. Arch Phys Med Rehabil. 2007;88:32–6.PubMedCrossRefGoogle Scholar
  70. 70.
    Bachasson D, Villiot-Danger E, Verges S, Hayot M, Perez T, Chambellan A, Wuyam B. Maximal isometric voluntary quadriceps strength assessment in COPD. Rev Mal Respir. 2014;31:765–70.PubMedCrossRefGoogle Scholar
  71. 71.
    Visser J, Mans E, De Visser M, Van Den Berg-Vos RM, Franssen H, JMBV DJ, Van Den Berg LH, JHJ W, De Haan RJ. Comparison of maximal voluntary isometric contraction and hand-held dynamometry in measuring muscle strength of patients with progressive lower motor neuron syndrome. Neuromuscul Disord. 2003;13:744–50.PubMedCrossRefGoogle Scholar
  72. 72.
    Vieira L, Bottaro M, Celes R, Viegas CA, Silva C. Isokinetic muscle evaluation of quadriceps in patients with chronic obstructive pulmonary disease. Rev Port Pneumol. 2010;16:717–36.PubMedCrossRefGoogle Scholar
  73. 73.
    Mathur S, Makrides L, Hernandez P. Test-retest reliability of isomeric and isokinetic torque in patients with chronic obstructive pulmonary disease. Physiother Can. 2004;56:94–101.CrossRefGoogle Scholar
  74. 74.
    Butcher SJ, Pikaluk BJ, Chura RL, Walkner MJ, Farthing JP, Marciniuk DD. Associations between isokinetic muscle strength, high-level functional performance, and physiological parameters in patients with chronic obstructive pulmonary disease. Int J Chron Obstruct Pulmon Dis. 2012;7:537–42.PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Zanini A, Aiello M, Cherubino F, Zampogna E, Azzola A, Chetta A, Spanevello A. The one repetition maximum test and the sit-to-stand test in the assessment of a specific pulmonary rehabilitation program on peripheral muscle strength in COPD patients. Int J COPD. 2015;10:2423–30.CrossRefGoogle Scholar
  76. 76.
    Kealin ME, Swank AM, Adams KJ, Barnard KL, Berning JM, Green A. Cardiopulmonary responses, muscle soreness, and injury during the one repetition maximum assessment in pulmonary rehabilitation patients. J Cardpulm Rehabil. 1999;19:366–72.CrossRefGoogle Scholar
  77. 77.
    Ra E, Kaplovitch E, Beauchamp MK, Dolmage TE, Goldstein RS, Gillies CL, Brooks D, Mathur S. Is quadriceps endurance reduced in COPD? Chest. 2015;147:673.CrossRefGoogle Scholar
  78. 78.
    Allaire J, Maltais F, Doyon JF, Noel M, Leblanc P, Carrier G, Simard C, Jobin J. Peripheral muscle endurance and the oxidative profile of the quadriceps in patients with COPD. Thorax. 2004;59:673–8.PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Coronell C, Orozco-Levi M, Mendez R, Ramirez-Sarmiento A, Galdiz JB, Gea J. Relevance of assessing quadriceps endurance in patients with COPD. Eur Respir J. 2004;24:129–36.PubMedCrossRefGoogle Scholar
  80. 80.
    Enoka RM, Duchateau J. Muscle fatigue: what, why and how it influences muscle function. J Physiol. 2008;1:11–23.CrossRefGoogle Scholar
  81. 81.
    Bigland-Ritchie B, Furbush F, Woods JJ. Fatigue of intermittent submaximal voluntary contractions: central and peripheral factors. J Appl Physiol. 1986;61:421–9.PubMedCrossRefGoogle Scholar
  82. 82.
    Swallow EB, Gosker HR, Ward KA, Moore AJ, Dayer MJ, Hopkinson NS, Schols AM, Moxham J, Polkey MI. A novel technique for nonvolitional assessment of quadriceps muscle endurance in humans. J Appl Physiol. 2007;103:739–46.PubMedCrossRefGoogle Scholar
  83. 83.
    Man WD, Natanek SA, Riddoch-Contreras J, Lewis A, Marsh GS, Kemp PR, Polkey MI. Quadriceps myostatin expression in COPD. Eur Respir J. 2010;36:686–8.PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Natanek SA, Gosker HR, Slot IG, Marsh GS, Hopkinson NS, Moxham J, Kemp PR, Schols AM, Polkey MI. Pathways associated with reduced quadriceps oxidative fibres and endurance in COPD. Eur Respir J. 2013;41:1275–83.PubMedCrossRefGoogle Scholar
  85. 85.
    Rossman MJ, Venturelli M, McDaniel J, Amann M, Richardson RS. Muscle mass and peripheral fatigue: a potential role for afferent feedback? Acta Physiol (Oxford). 2012;206:242–50.CrossRefGoogle Scholar
  86. 86.
    Burtin C, Saey D, Saglam M, Langer D, Gosselink R, Janssens W, Decramer M, Maltais F, Troosters T. Effectiveness of exercise training in patients with COPD: the role of muscle fatigue. Eur Respir J. 2012;40(2):338–44.PubMedCrossRefGoogle Scholar
  87. 87.
    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.PubMedCrossRefGoogle Scholar
  88. 88.
    Shah S, Nahar P, Vaidya S, Salvi S. Upper limb muscle strength & endurance in chronic obstructive pulmonary disease. Indian J Med Res. 2013;138:492–6.PubMedPubMedCentralGoogle Scholar
  89. 89.
    Clark CJ, Cochrane LM, Mackay E, Paton B. Skeletal muscle strength and endurance in patients with mild COPD and the effects of weight training. Eur Respir J. 2000;15:92–7.PubMedCrossRefGoogle Scholar
  90. 90.
    Nyberg A, Lindstrom B, Rickenlund A, Wadell K. Low-load/high-repetition elastic band resistance training in patients with COPD: a randomized, controlled, multicenter trial. Clin Respir J. 2015;9(3):278–88.PubMedCrossRefGoogle Scholar
  91. 91.
    Ribeiro F, Lepine PA, Garceau-Bolduc C, Coats V, Allard E, Maltais F, Saey D. Test-retest reliability of lower limb isokinetic endurance in COPD: a comparison of angular velocities. Int J Chron Obs Pulmon Dis. 2015;10:1163–72.Google Scholar
  92. 92.
    Malaguti C, Nery LE, Dal Corso S, Napolis L, De Fuccio MB, Castro M, Neder JA. Scaling skeletal muscle function to mass in patients with moderate-to-severe COPD. Eur J Appl Physiol. 2006;98:482–8.PubMedCrossRefGoogle Scholar
  93. 93.
    Janaudis-Ferreira T, Wadell K, Sundelin G, Lindstrom B. Thigh muscle strength and endurance in patients with COPD compared with healthy controls. Respir Med. 2006;100:1451–7.PubMedCrossRefGoogle Scholar
  94. 94.
    Pincivero DM, Lephart SM, Karunakara RA. Reliability and precision of isokinetic strength and muscular endurance for the quadriceps and hamstrings. Int J Sports Med. 1997;18:113–7.PubMedCrossRefGoogle Scholar
  95. 95.
    Pincivero DM, Gear WS, Sterner RL. Assessment of the reliability of high-intensity quadriceps femoris muscle fatigue. Med Sci Sports Exerc. 2001;33:334–8.PubMedCrossRefGoogle Scholar
  96. 96.
    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;20:1123–9.PubMedCrossRefGoogle Scholar
  97. 97.
    Couillard A, Maltais F, Saey D, Debigaré R, Michaud A, Koechlin C, LeBlanc P, Préfaut C. Exercise-induced quadriceps oxidative stress and peripheral muscle dysfunction in patients with COPD. Am J Respir Crit Care Med. 2003;167:1664–9.PubMedCrossRefGoogle Scholar
  98. 98.
    Nyberg A, Saey D, Martin M, Maltais F. Acute effects of low-load/high-repetition single-limb resistance training in COPD. Med Sci Sports Exerc. 2016;48:2353–61.PubMedCrossRefGoogle Scholar
  99. 99.
    Clark CJ, Cochrane L, Mackay E. Low intensity peripheral muscle conditioning improves exercise tolerance and breathlessness in COPD. Eur Respir J. 1996;9:2590–6.PubMedCrossRefGoogle Scholar
  100. 100.
    Nyberg A, Saey D, Martin M, Maltais F. Muscular and functional effects of partitioning exercising muscle mass in patients with chronic obstructive pulmonary disease - a study protocol for a randomized controlled trial. Trials. 2015;16:194.PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Clark AL, Poole-Wilson PA, Coats AJ. Exercise limitation in chronic heart failure: central role of the periphery. J Am Coll Cardiol. 1996;28:1092–102.PubMedCrossRefGoogle Scholar
  102. 102.
    Spruit MA, Singh SJ, Garvey C, ZuWallack R, Nici L, Rochester C, Hill K, Holland AE, Lareau SC, Man WD, et al. An official American Thoracic Society/European Respiratory Society statement: key concepts and advances in pulmonary rehabilitation. Am J Respir Crit Care Med. 2013;188:e13–64.PubMedCrossRefPubMedCentralGoogle Scholar
  103. 103.
    McCarthy B, Casey D, Devane D, Murphy K, Murphy E, Lacasse Y. Pulmonary rehabilitation for chronic obstructive pulmonary disease. Cochrane Database Syst Rev. 2015;2:CD003793.Google Scholar
  104. 104.
    Troosters T, Gosselink R, Janssens W, Decramer M. Exercise training and pulmonary rehabilitation: new insights and remaining challenges. Eur Respir Rev. 2010;19:24–9.PubMedCrossRefGoogle Scholar
  105. 105.
    Spruit MA, Gosselink R, Troosters T, De Paepe K, Decramer M. Resistance versus endurance training in patients with COPD and peripheral muscle weakness. Eur Respir J. 2002;19:1072–8.PubMedCrossRefGoogle Scholar
  106. 106.
    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.PubMedCrossRefGoogle Scholar
  107. 107.
    Puente-Maestu L, Sanz ML, Sanz P, Cubillo JM, Mayol J, Casaburi R. Comparison of effects of supervised versus self-monitored training programmes in patients with chronic obstructive pulmonary disease. Eur Respir J. 2000;15:517–25.PubMedCrossRefGoogle Scholar
  108. 108.
    Maltais F, Leblanc P, Jobin J, BÇrubÇ C, Bruneau J, Carrier L, Breton MJ, Falardeau G, Belleau R. Intensity of training and physiologic adaptation in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1997;155:555–61.PubMedCrossRefGoogle Scholar
  109. 109.
    Coppoolse R, Schols AMWJ, Baarends EM, Mostert R, Akkermans MA, Janssen PP, Wouters EFM. Interval versus continuous training in patients with severe COPD: a randomized clinical trial. Eur Respir J. 1999;14:258–63.PubMedCrossRefGoogle Scholar
  110. 110.
    Vogiatzis I, Nanas S, Roussos C. Interval training as an alternative modality to continuous exercise in patients with COPD. Eur Respir J. 2002;20:12–9.PubMedCrossRefGoogle Scholar
  111. 111.
    O'Donnell DE, McGuire M, Samis L, Webb KA. General exercise training improves ventilatory and peripheral muscle strength and endurance in chronic airflow limitation. Am J Respir Crit Care Med. 1998;157:1489–97.PubMedCrossRefGoogle Scholar
  112. 112.
    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 COPD patients. Comparison with normal subjects and effects of exercise training. Med Sci Sports Exerc. 1998;30:1467–74.PubMedCrossRefGoogle Scholar
  113. 113.
    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. 2007;62:950–6.PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Vogiatzis I, Terzis G, Stratakos G, Cherouveim E, Athanasopoulos D, Spetsioti S, Nasis I, Manta P, Roussos C, Zakynthinos S. Effect of pulmonary rehabilitation on peripheral muscle fiber remodeling in patients with COPD in GOLD stages II to IV. Chest. 2011;140:744–52.PubMedCrossRefGoogle Scholar
  115. 115.
    Troosters T, Gosselink R, Decramer M. Short- and long-term effects of outpatient rehabilitation in patients with chronic obstructive pulmonary disease: a randomized trial. Am J Med. 2000;109:207–12.PubMedCrossRefGoogle Scholar
  116. 116.
    Mador MJ, Kufel TJ, Pineda LA, Steinwald A, Aggarwal A, Upadhyay AM, Khan MA. Effect of pulmonary rehabilitation on quadriceps fatiguability during exercise. Am J Respir Crit Care Med. 2001;163:930–5.PubMedCrossRefGoogle Scholar
  117. 117.
    Skumlien S, Aure Skogedal E, Skrede Ryg M, Bjortuft O. Endurance or resistance training in primary care after in-patient rehabilitation for COPD? Respir Med. 2008;102:422–9.PubMedCrossRefGoogle Scholar
  118. 118.
    Man WD, Kemp P, Moxham J, Polkey MI. Exercise and muscle dysfunction in COPD: implications for pulmonary rehabilitation. Clin Sci (Lond). 2009;117:281–91.CrossRefGoogle Scholar
  119. 119.
    Vonbank K, Strasser B, Mondrzyk J, Marzluf BA, Richter B, Losch S, Nell H, Petkov V, Haber P. Strength training increases maximum working capacity in patients with COPD--randomized clinical trial comparing three training modalities. Respir Med. 2012;106:557–63.PubMedCrossRefGoogle Scholar
  120. 120.
    Spruit MA, Troosters T, Trappenburg JC, Decramer M, Gosselink R. Exercise training during rehabilitation of patients with COPD: a current perspective. Patient Educ Couns. 2004;52:243–8.PubMedCrossRefGoogle Scholar
  121. 121.
    Nici L, Donner C, Wouters E, Zuwallack R, Ambrosino N, Bourbeau J, Carone M, Celli B, Engelen M, Fahy B, et al. American Thoracic Society/European Respiratory Society statement on pulmonary rehabilitation. Am J Respir Crit Care Med. 2006;173:1390–413.PubMedCrossRefGoogle Scholar
  122. 122.
    O'Shea SD, Taylor NF, Paratz J. Peripheral muscle strength training in COPD: a systematic review. Chest. 2004;126:903–14.PubMedCrossRefGoogle Scholar
  123. 123.
    O'Shea SD, Taylor NF, Paratz JD. Progressive resistance exercise improves muscle strength and may improve elements of performance of daily activities for people with COPD: a systematic review. Chest. 2009;136:1269–83.PubMedCrossRefGoogle Scholar
  124. 124.
    Kraemer WJ, Adams K, Cafarelli E, Dudley GA, Dooly C, Feigenbaum MS, Fleck SJ, Franklin B, Fry AC, Hoffman JR, et al. American College of Sports Medicine position stand. Progression models in resistance training for healthy adults. Med Sci Sports Exerc. 2002;34:364–80.PubMedCrossRefGoogle Scholar
  125. 125.
    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. 2010;181:1072–7.PubMedCrossRefGoogle Scholar
  126. 126.
    Lewis MI, Fournier M, Storer TW, Bhasin S, Porszasz J, Ren SG, Da X, Casaburi R. Skeletal muscle adaptations to testosterone and resistance training in men with COPD. J Appl Physiol. 2007;103:1299–310.PubMedCrossRefGoogle Scholar
  127. 127.
    Menon MK, Houchen L, Singh SJ, Morgan MD, Bradding P, Steiner MC. Inflammatory and satellite cells in the quadriceps of patients with COPD and response to resistance training. Chest. 2012;142:1134–42.PubMedCrossRefGoogle Scholar
  128. 128.
    Puhan MA, Schunemann HJ, Frey M, Scharplatz M, Bachmann LM. How should COPD patients exercise during respiratory rehabilitation? Comparison of exercise modalities and intensities to treat skeletal muscle dysfunction. Thorax. 2005;60:367–75.PubMedPubMedCentralCrossRefGoogle Scholar
  129. 129.
    Lepsen UW, Jorgensen KJ, Ringbaek T, Hansen H, Skrubbeltrang C, Lange P. A systematic review of resistance training versus endurance training in COPD. J Cardiopulm Rehabil Prev. 2015;35:163–72.CrossRefGoogle Scholar
  130. 130.
    Puente-Maestu L, Sanz ML, Sanz P, Ruiz de Ona JM, Rodriguez-Hermosa JL, Whipp BJ. Effects of two types of training on pulmonary and cardiac responses to moderate exercise in patients with COPD. Eur Respir J. 2000;15:1026–32.PubMedCrossRefGoogle Scholar
  131. 131.
    Mador MJ, Bozkanat E, Aggarwal A, Shaffer M, Kufel TJ. Endurance and Strength Training in Patients With COPD. Chest. 2004;125:2036–45.PubMedCrossRefGoogle Scholar
  132. 132.
    Lepsen UWJK, Ringbaek T, Hansen H, Skrubbeltrang C, Lange PA. Combination of resistance and endurance training increases leg muscle strength in COPD: an evidence-based recommendation based on systematic review with meta-analyses. Chron Respir Dis. 2015;12:13.Google Scholar
  133. 133.
    Normandin EA, McCusker C, Connors M, Vale F, Gerardi D, ZuWallack RL. An evaluation of two approaches to exercise conditioning in pulmonary rehabilitation. Chest. 2002;121:1085–91.PubMedCrossRefGoogle Scholar
  134. 134.
    Houchen L, Steiner MC, Singh SJ. How sustainable is strength training in chronic obstructive pulmonary disease? Physiotherapy. 2009;95:1–7.PubMedCrossRefGoogle Scholar
  135. 135.
    Vivodtzev I, Lacasse Y, Maltais F. Neuromuscular electrical stimulation of the lower limbs in patients with chronic obstructive pulmonary disease. J Cardiopulm Rehabil Prev. 2008;28:79–91.PubMedCrossRefGoogle Scholar
  136. 136.
    Sillen MJ, Speksnijder CM, Eterman RM, Janssen PP, Wagers SS, Wouters EF, Uszko-Lencer NH, Spruit MA. Effects of neuromuscular electrical stimulation of muscles of ambulation in patients with chronic heart failure or COPD: a systematic review of the English-language literature. Chest. 2009;136:44–61.PubMedCrossRefGoogle Scholar
  137. 137.
    Vivodtzev I, Debigare R, Gagnon P, Mainguy V, Saey D, Dube A, Pare ME, Belanger M, Maltais F. Functional and muscular effects of neuromuscular electrical stimulation in patients with severe COPD: a randomized clinical trial. Chest. 2012;141(3):716–25.PubMedCrossRefGoogle Scholar
  138. 138.
    Dal Corso S, Napolis L, Malaguti C, Gimenes AC, Albuquerque A, Nogueira CR, De Fuccio MB, Pereira RD, Bulle A, McFarlane N, et al. Skeletal muscle structure and function in response to electrical stimulation in moderately impaired COPD patients. Respir Med. 2006;101(6):1236–43.PubMedCrossRefGoogle Scholar
  139. 139.
    Abdellaoui A, Prefaut 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. 2011;38:781–8.PubMedCrossRefGoogle Scholar
  140. 140.
    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. 2003;124:292–6.PubMedCrossRefGoogle Scholar
  141. 141.
    Neder JA, Sword D, Ward SA, Mackay E, Cochrane LM, Clark CJ. Home based neuromuscular electrical stimulation as a new rehabilitative strategy for severely disabled patients with chronic obstructive pulmonary disease (COPD). Thorax. 2002;57:333–7.PubMedPubMedCentralCrossRefGoogle Scholar
  142. 142.
    Maddocks M, Nolan CM, Man WD, Polkey MI, Hart N, Gao W, Rafferty GF, Moxham J, Higginson IJ. Neuromuscular electrical stimulation to improve exercise capacity in patients with severe COPD: a randomised double-blind, placebo-controlled trial. Lancet Respir Med. 2016;4:27–36.PubMedCrossRefGoogle Scholar
  143. 143.
    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. 2006;173:79–83.PubMedGoogle Scholar
  144. 144.
    Coin A, Sergi G, Minicuci N, Giannini S, Barbiero E, Manzato E, Pedrazzoni M, Minisola S, Rossini M, Del Puente A, et al. Fat-free mass and fat mass reference values by dual-energy X-ray absorptiometry (DEXA) in a 20-80 year-old Italian population. Clin Nutr. 2008;27:87–94.PubMedCrossRefGoogle Scholar
  145. 145.
    Bachasson D, Wuyam B, Pepin JL, Tamisier R, Levy P, Verges S. Quadriceps and respiratory muscle fatigue following high-intensity cycling in COPD patients. PLoS One. 2013;8:e83432.PubMedPubMedCentralCrossRefGoogle Scholar
  146. 146.
    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.PubMedCrossRefGoogle Scholar
  147. 147.
    Stark T, Walker B, Phillips JK, Fejer R, Beck R. Hand-held dynamometry correlation with the gold standard isokinetic dynamometry: a systematic review. PM R. 2011;3:472–9.PubMedCrossRefGoogle Scholar
  148. 148.
    Hartmann A, Knols R, Murer K, De Bruin ED. Reproducibility of an isokinetic strength-testing protocol of the knee and ankle in older adults. Gerontology. 2009;55:259–68.PubMedCrossRefGoogle Scholar
  149. 149.
    Dourado VZ, Antunes LC, Tanni SE, de Paiva SA, Padovani CR, Godoy I. Relationship of upper-limb and thoracic muscle strength to 6-min walk distance in COPD patients. Chest. 2006;129(3):551–7.PubMedCrossRefGoogle Scholar
  150. 150.
    Burns SP, Spanier DE. Break-technique handheld dynamometry: relation between angular velocity and strength measurements. Arch Phys Med Rehabil. 2005;86:1420–6.PubMedCrossRefGoogle Scholar
  151. 151.
    Burns SP, Breuninger A, Kaplan C, Marin H. Hand-held dynamometry in persons with tetraplegia: comparison of make- versus break-testing techniques. Am J Phys Med Rehabil. 2005;84:22–9.PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2018

Authors and Affiliations

  • Roberto A. Rabinovich
    • 1
  • Kim-Ly Bui
    • 2
  • André Nyberg
    • 2
  • Didier Saey
    • 2
  • François Maltais
    • 2
    Email author
  1. 1.ELEGI Colt Laboratory, Centre for Inflammation Research, The Queen’s Medical Research Institute, University of EdinburghEdinburghUK
  2. 2.Institut Universitaire de Cardiologie et de Pneumologie de Québec, Université LavalQuébecCanada

Personalised recommendations