Effect of pulmonary rehabilitation on oxidative stress in patients with pulmonary diseases

Abstract

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.

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Itoh, M. , Nemoto, K. , Tsuji, T. , Nakamura, H. and Aoshiba, K. (2012) Effect of pulmonary rehabilitation on oxidative stress in patients with pulmonary diseases. Advances in Bioscience and Biotechnology, 3, 1028-1036. doi: 10.4236/abb.2012.327125.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] 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
[2] 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.
[3] 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
[4] 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
[5] 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
[6] 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
[7] 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
[8] 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
[9] 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
[10] 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
[11] 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
[12] 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
[13] 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.
[14] 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
[15] 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.
[16] 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
[17] 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
[18] 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
[19] 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
[20] 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.
[21] 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.
[22] 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
[23] 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
[24] 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
[25] 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
[26] 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
[27] 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
[28] 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
[29] 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
[30] 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
[31] 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
[32] 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
[33] 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
[34] 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.
[35] 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
[36] 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.
[37] 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
[38] 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
[39] 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.
[40] 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
[41] 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
[42] 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
[43] 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
[44] 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.
[45] 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
[46] Flück, M. (2005) Hypoxaemia enhanced peripheral muscle oxidative stress in COPD. Thorax, 60, 797-798. doi:10.1136/thx.2005.047738
[47] 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
[48] Tsan, M.F. (2001) Superoxide dismutase and pulmonary oxygen toxicity: Lessons from transgenic and knockout mice. International Journal of Molecular Medicine, 7, 13-19.
[49] 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.
[50] 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.
[51] 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
[52] 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
[53] 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
[54] 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

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