Exercise-training-based pulmonary rehabilitation has been confirmed to be effective in improving the activities of daily living (ADL) and relieving the dyspnea of chronic obstructive pulmonary disease (COPD) patients. Exercise training increases the antioxidant capacity of COPD patients, but since strenuous exercise and acute exercise loading have the opposite effect and increase oxidative stress, it is important to establish exercise training conditions that efficiently raise antioxidant capacity without increasing oxidative stress. Research on oxidative stress during exercise training by COPD patients has been pursued from that standpoint, but in recent years the targets of research on respirator diseases other than COPD have been expanding. In this article we will therefore review the results of research that has been conducted thus far on the effect of pulmonary rehabilitation on oxidative stress, including the results obtained at our own institution.
Nici, L., Donner, C., Wouters, E., Zuwallack, R., Ambrosino, N. and Borbeau, J. (2006) AmericanThoracic Society/European Respiratory Society statement on pulmonary rehabilitation. American Journal of Respiratory and Critical Care Medicine, 173, 1390-1413. doi:10.1164/rccm.200508-1211ST
Ohishi, S., Kizaki, T., Ookawara, T., Sakurai, T., Izawa, T. and Nagata, N. (1997) Endueance training improves the resistance of rat diaphragm to exercise induced oxidative stress. European Respiratory Journal, 156, 1579-1585.
Rahman, I. and Adcock, I.M. (2006) Oxidative stress and redox regulation of lung inflammation in COPD. European Respiratory Journal, 28, 219-242. doi:10.1183/09031936.06.00053805
Caron, M., Debigaré, R., Dekhuijzen, P.N.R. and Maltais, F. (2009) Comparative assessment of the quadriceps and the diaphragm in patients with COPD. Journal of Applied Physiology, 107, 952-961. doi:10.1152/japplphysiol.00194.2009
Whittom, F., Jobin, J., Simard, P.M., Leblanc, P., Simard, C. and Bernard, S. (1998) Histochemical and morphological characteristics of the vastus lateralis muscle in patients with chronic obstructive pulmonary disease. Medicine and Science in Sports and Exercise, 30, 1467-1474. doi:10.1097/00005768-199810000-00001
Gosker, H.R., Zeegers, M.P., Wouters, E.F. and Schols, A.M. (2007) Muscle fiber 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. doi:10.1136/thx.2007.078980
Jobin, J., Maltais, F., Doyon, J.F., LeBlanc, P., Simard, P.M. and Simard, A.A. (1998) Chronic obstructive pulmonary disease: Capillarity and fiber type characteristics of skeletal muscle. Journal of Cardiopulmonary Rehabilitation, 18, 432-437. doi:10.1097/00008483-199811000-00005
Gosker, H.R., Hesselink, M.K., Duimel, H., Ward, K.A. and Schols, A.M. (2007) Reduced mitochondrial density in the vastus lateralis muscle of patients with COPD. European Respiratory Journal, 30, 73-79. doi:10.1183/09031936.00146906
Picard, M., Godin, R., Sinnreich, M., Baril, J., Bourbeau, J. and Perrault, H. (2008) The mitochondrial phenotype of peripheral muscle in chronic obstructive pulmonary disease: disuse or dysfunction? American Journal of Respiratory and Critical Care Medicine, 178, 1040-1047. doi:10.1164/rccm.200807-1005OC
Puente-Maestu, L., Pérez-Parra, J., Godoy, R., Moreno, N., Tejedor, A. and González-Aragoneses, F. (2009) Abnormal mitochondrial function in locomotor and respiratory muscle of COPD patients. European Respiratory Journal, 33, 1045-1052. doi:10.1183/09031936.00112408
Green, H.J., Bombardier, E. Burnett, M., Iqbal, S., D’Arsigny, C.L. and O’Donnell, D.E. (2008) Organization of metabolic pathways in vastus lateralis of patients with chronic obstructive pulmonary disease. American Journal of Physiology—Regulatory, Integrative and Comparative Physiology, 295, R935-R941. doi:10.1152/ajpregu.00167.2008
Maltais, F., Le Blane, P., Whittom, F., Simard, C., Marquis, K. and Bélanger, M. (2000) Oxidative enzyme activities of the vastus lateralis muscle and the functional status in patients with COPD. Thorax, 55, 848-853. doi:10.1136/thorax.55.10.848
Maltais, F., Simard, A.A., Simard, C., Jobin, J., Desgagnés, P. and LeBlanc, P. (1996) Oxidative capacity of the skeletal muscle and lactic acid kinetics during exercise in normal subjects and in patients with COPD. American Journal of Respiratory and Critical Care Medicine, 153, 288-293.
Radom-Aizik, S., Kaminski, N. Hayek, S., Halkin, H., Cooper, D.M. and Ben-Dov, I. (2007) Effects of exercise training on quadriceps muscle gene expression in chronic obstructive pulmonary disease. Journal of Applied Physiology, 102, 1976-1984. doi:10.1152/japplphysiol.00577.2006
Fermoselle, C., Rabinovich, R. Ausín, P., Puig-Vilanova, E., Coronell, C. and Sanchez, F. (2012) Does oxidative stress modulate limb muscle atrophy in severe COPD patients? European Respiratory Journal, 40, 851-862.
Rodriguez, D.A., Kalko, S., Puig-Vilanova, E., Perez- Olabarría, M., Falciani, F. and Gea, J. (2012) Muscle and blood redox status after exercise training in severe COPD patients. Free Radical Biology & Medicine, 52, 88-94. doi:10.1016/j.freeradbiomed.2011.09.022
Macnee, W. (2001) Oxidative stress and lung inflamemation in airways disease. European Journal of Pharmacology, 429, 195-207. doi:10.1016/S0014-2999(01)01320-6
Couillard, A., Koechlin, C. Cristol, J.P., Varray, A. and Prefaut, C. (2002) Evidence of local exercise-induced systemic oxidative stress in chronic obstructive pulmonary disease patients. European Respiratory Journal, 20, 1123-1129. doi:10.1183/09031936.02.00014302
van Helvoort, H.A., Heijdra, Y.F., de Boer, R.C., Swinkels, A., Thijs, H.M. and Dekhuijzen, P.N. (2007) Six-minutes walking-induced systemic inflammation and oxidative stress in muscle-wasted COPD patient. Chest, 131, 439-445. doi:10.1378/chest.06-1655
Vina, J., Servera, E., Asensi, M., Sastre, J., Pallardó, F.V. and Ferrero, J.A. (1996) Exercise causes blood glutathione oxidation in chronic obstructive pulmonary disease: prevention by O2 therapy. Journal of Applied Physiology, 81, 2198-2202.
Heunks, L.M., Vina, J. van Herwaarden, C.L., Folgering, H.T., Gimeno, A. and Dekhuijzen, P.N. (1999) Xanthine oxidase is involved in exercise-induced oxidative stress in chronic obstructive pulmonary disease. American Journal of Physiology, 277, R1697-R1704.
Couillard, A., Maltais, F., Saey, D., Debigaré, R., Michaud, A. and Koechlin, C. (2003) Exercise-induced quadriceps oxidative stress and peripheral muscle dysfunction in patients with chronic obstructive pulmonary disease. American Journal of Respiratory and Critical Care Medicine, 167, 1664-1669. doi:10.1164/rccm.200209-1028OC
Agacdiken, A., Basyigit, I., Ozden, M., Yildiz, F., Ural, D. and Maral, H. (2004) The effects of antioxidants on exercise-induced lipid peroxidation in patients with COPD. Respirology, 9, 38-42. doi:10.1111/j.1440-1843.2003.00526.x
Koechlin, C., Couillard, A., Cristol, J.P., Chanez, P., Hayot, M. and Le Gallais, D. (2004) Does systemic inflamemation trigger local exercise-induced oxidative stress in COPD? European Respiratory Journal, 23, 538-544. doi:10.1183/09031936.04.00069004
Koechlin, C., Couillard, A., Simar, D., Cristol, J.P., Bellet, H. and Hayot, M. (2004) Does oxidative stress alter quadricceps endurance in chronic obstructive pulmonary disease? American Journal of Respiratory and Critical Care Medicine, 169, 1022-1027. doi:10.1164/rccm.200310-1465OC
Mercken, E.M., Hageman, G.J., Schols, A.M., Akkermans, M.A., Bast, A. and Wouters, E.F. (2005) Rehabilitation decreases exercise-induced oxidative stress in chronic obstructive pulmonary disease. American Journal of Respiratory and Critical Care Medicine, 172, 994-1001. doi:10.1164/rccm.200411-1580OC
van Helvoort, H.A., Heijdra, Y.F., Thijs, H.M., Vina, J., Wanten, G.J. and Dekhuijzen, P.N. (2006) Exercise-induced systemic effects in muscle-wasted patients with COPD. Medicine and Science in Sports and Exercise, 38, 1543-1552. doi:10.1249/01.mss.0000228331.13123.53
Jammes, Y., Steinberg, J.G., Ba, A., Delliaux, S. and Brégeon, F. (2008) Enhanced exercise-induced plasma cytokine response and oxidative stress in COPD patients depend on blood oxygenation. Clinical Physiology and Functional Imaging, 28, 182-188. doi:10.1111/j.1475-097X.2008.00795.x
Mercken, E.M., Gosker, H.R., Rutten, E.P., Wouters, E.F., Bast, A. and Hageman, G.J. (2009) Systemic and pulmonary oxidative stress after single-leg exercise in COPD. Chest, 136, 1291-1300. doi:10.1378/chest.08-2767
Pinho, R.A., Chiesa, D., Mezzomo, K.M., Andrades, M.E., Bonatto, F. and Gelain, D. (2007) Oxidative stress in chronic obstructive pulmonary disease patients submitted to a rehabilitation program. Respiratory Medicine, 101, 1830-1835. doi:10.1016/j.rmed.2007.02.004
Mercken, E.M., Calvert, L.D., Singh, S.J., Hageman, G.J., Schols, A.M. and Steiner, M.C. (2009) Dichloroacetate modulates the oxidative stress and inflammatory response to exercise in COPD. Chest, 136, 744-751. doi:10.1378/chest.08-2890
Mercken, E.M., Hageman, G.J., Langen, R.C., Wouters, E.F. and Schols, A.M. (2011) Decreased exercise-induced expression of nuclear factor-κB-regulated genes in muscle of patients with COPD. Chest, 139, 337-346. doi:10.1378/chest.10-0275
Puente-Maestu, L., Lázaro, A., Tejedor, A., Camano, S., Fuentes, M. and Cuervo, M. (2011) Effects of exercise on mitochondrial DNA content in skeletal muscle of patients with COPD. Thorax, 66, 121-127. doi:10.1136/thx.2010.153031
Graham, T.E., Bangsbo, J., Gollnick, P.D., Juel, C. and Saltin, B. (1990) Ammonia metabolism during intense dynamic exercise and recovery in humans. American Journal of Physiology, 259, E170-E176.
Calvert, L.D., Singh, S.J., Morgan, M.D. and Steiner, M.C. (2011) Exercise induced skeletal muscle metabolic stress is reduced after pulmonary rehabilitation in COPD. Respiratory Medicine, 105, 363-370. doi:10.1016/j.rmed.2010.10.012
Bernard, S., Whittom, F., Leblanc, P., Jobin, J., Belleau, R. and Bérubé, C. (1999) Aerobic and strength training in patients with chronic obstructive pulmonary disease. American Journal of Respiratory and Critical Care Medicine, 159, 896-901.
Maltais, F., Le Blanc, P., Simard, C., Jobin, J., Bérubé, C. and Bruneau, J. (1996) Skeletal muscle adaptation to endurance training in patients with chronic obstructive pulmonary disease. American Journal of Respiratory and Critical Care Medicine, 154, 442-447
Rochester, C.L. (2003) Exercise training in chronic obstructive pulmonary disease. Journal of Rehabilitation Research and Develop, 40, 59-80. doi:10.1682/JRRD.2003.10.0059
Terrados, N., Jansson, E., Sylvén, C. and Kaijser, L. (1990) Is hypoxia a stimulus for synthesis of oxidative enzymes and myoglobin? Journal of Applied Physiology, 68, 2369-2372.
Garcia-Aymerich, J., Lange, P., Benet, M., Schnohr, P. and Antó, J.M. (2007) Regular physical activity modifies smoking-related lung function decline and reduces risk of chronic obstructive pulmonary disease: A population-based cohort study. American Journal of Respiratory and Critical Care Medicine, 175, 458-463. doi:10.1164/rccm.200607-896OC
Toledo, A.C., Magalhaes, R.M., Hizume, D.C., Vieira, R.P., Biselli, P.J. and Moriya, H.T. (2012) Aerobic exercise attenuates pulmonary injury induced by exposure to cigarette smoke. European Respiratory Journal, 39, 254-264. doi:10.1183/09031936.00003411
Barreiro, B., Rabinovich, R., Marin-Corral, J., Barberà, J.A., Gea, J. and Roca, J. (2009) Chronic endurance exercise induces quadriceps nitrosative stress in patients with severe COPD. Thorax, 64, 13-19. doi:10.1136/thx.2008.105163
Silva, L.A., Pinho, C.A., Scarabelot, K.S., Fraga, D.B., Volpato, A.M. and Boeck, C.R. (2009) Physical exercise increases mitochondrial function and reduces oxidative damage in skeletal muscle. European Journal of Applied Physiology, 105, 861-867. doi:10.1007/s00421-008-0971-8
Casaburi, M., Patessio, A., Ioli, F., Zanaboni, S., Donner, C.F. and Wasserman, K. (1991) Reductions in exercise lactic acidosis and ventilation as a result of exercise training in patients with obstructive lung disease. The American Review of Respiratory Disease, 143, 9-18.
Rabinovich, R.A., Ardite, E., Mayer, A.M., Polo, M.F., Vilaró, J. and Argilés, J.M. (2006) Training depletes muscle glutathione in patients with chronic obstructive pulmonary disease and low body mass index. Respiration, 73, 757-761. doi:10.1159/000094395
Flück, M. (2005) Hypoxaemia enhanced peripheral muscle oxidative stress in COPD. Thorax, 60, 797-798. doi:10.1136/thx.2005.047738
van Helvoort, H.A., Heijdra, Y.F., Heunks, L.M., Meijer, P.L., Ruitenbeek, W. and Thijs, H.M. (2006) Supplemental oxygen prevents exercise-induced oxidative stress in muscle-wasted patients with chronic obstructive pulmonary disease. American Journal of Respiratory and Critical Care Medicine, 173, 1122-1129. doi:10.1164/rccm.200512-1957OC
Tsan, M.F. (2001) Superoxide dismutase and pulmonary oxygen toxicity: Lessons from transgenic and knockout mice. International Journal of Molecular Medicine, 7, 13-19.
Itoh, M., OhIshi, S., Sudo, A., Hatao, H., Komiyama, M. and Kishi, K. (2005) Effect of pulmonary rehabilitation on endurance capacity and oxidative stress in patients with COPD. Proceedings of the 100th American Thoracic Society, San Diego, 20-25 May 2005, A53.
Nemoto, K., Itoh, M., Nakamura, H. and OhIshi, S. (2012) Effect of exercise therapy on reactive oxygen species and reactive nitrogen species in COPD patients. Journal of Tokyo Medical University, 70, 34-41.
Onur, E., Kabaroglu, C., Günay, O., Var, A., Yilmaz, O. and Dündar, P. (2011) The beneficial effects of physical exercise on antioxidant status in asthmatic children. Allergol Immunopathol (Madr), 39, 90-95. doi:10.1016/j.aller.2010.04.006
Rammaert, B., Leroy, S., Cavestri, B., Wallaert, B. and Grosbois, J.M. (2011) Home-based pulmonary rehabilitation in idiopathic pulmonary fibrosis. Revue des Maladies Respiratoires, 28, 52-57. doi:10.1016/j.rmr.2011.06.006
Holland, A.E., Hill, C.J., Conron, M., Munro, P. and McDonald, C.F. (2008) Short term improvement in exercise capacity and symptoms following exercise training in interstitial lung disease. Thorax, 63, 549-554. doi:10.1136/thx.2007.088070
Jackson, R., Ramos, C., Gupta, C. and Gomez-Marin, O. (2010) Exercise decreases plasma antioxidant capacity and increases urinary isoprostanes of IPF patients. Respiratory Medicine, 104, 1919-1928. doi:10.1016/j.rmed.2010.07.021