Does impaired O2 delivery during exercise accentuate central and peripheral fatigue in patients with coexistent COPD-CHF?

Frontiers in Physiology

Volumn 6, Issue JAN, 2015, Pages

  Oliveira, Mayron F ^a   Zelt, Joel T J ^b   Jones, Joshua H ^b   Hirai, Daniel M ^a,b   O'Donnell, Denis E ^b   Verges, Samuel ^c   Alberto Neder, J ^a,b  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b QUEEN S UNIVERSITY   (Canada)

^c UNIV GRENOBLE ALPES   (France)

Author keywords

Chronic heart failure; Chronic obstructive pulmonary disease; Oxygenation; Respiratory muscle; Skeletal muscle

Indexed keywords

HELIOX;

ARTICLE; BREATHING; BREATHING MUSCLE; CARDIOPULMONARY FUNCTION; CARDIOPULMONARY HEMODYNAMICS; CENTRAL FATIGUE; CHRONIC OBSTRUCTIVE LUNG DISEASE; COMORBIDITY; CYCLING; EXCITATION CONTRACTION COUPLING; EXERCISE; HEART EJECTION FRACTION; HEART FAILURE; HEART OUTPUT; HUMAN; HYPERINFLATION; HYPOXIA; MUSCLE BLOOD FLOW; MUSCLE FATIGUE; MUSCLE ISOMETRIC CONTRACTION; MUSCLE TWITCH; MUSCLE WEAKNESS; OXYGEN TRANSPORT; PERIPHERAL FATIGUE; POSITIVE END EXPIRATORY PRESSURE; SKELETAL MUSCLE; TISSUE OXYGENATION; TRANSCRANIAL MAGNETIC STIMULATION; VASOCONSTRICTION;

EID: 84926434815     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2014.00514     Document Type: Article

References (66)

1. Agostoni, P., Bussotti, M., Cattadori, G., Margutti, E., Contini, M., Muratori, M., et al. (2006). Gas diffusion and alveolar-capillary unit in chronic heart failure. Eur. Heart J. 27, 2538-2543. doi: 10.1093/eurheartj/ehl302
2. Agostoni, P. G., Bussotti, M., Palermo, P., and Guazzi, M. (2002). Does lung diffusion impairment affect exercise capacity in patients with heart failure? Heart 88, 453-459. doi: 10.1136/heart.88.5.453
3. Aliverti, A., Dellacà, R. L., Lotti, P., Bertini, S., Duranti, R., Scano, G., et al. (2005). Influence of expiratory flow-limitation during exercise on systemic oxygen delivery in humans. Eur. J. Appl. Physiol. 95, 229-242. doi: 10.1007/s00421-005-1386-4
4. Amann, M. (2011). Central and peripheral fatigue: interaction during cycling exercise in humans. Med. Sci. Sports Exerc. 43, 2039-2045. doi: 10.1249/MSS.0b013e31821f59ab
5. Amann, M., and Calbet, J. A. L. (2008). Convective oxygen transport and fatigue. J. Appl. Physiol. 104, 861-870. doi: 10.1152/japplphysiol.01008.2007
6. Amann, M., and Dempsey, J. A. (2008). Locomotor muscle fatigue modifies central motor drive in healthy humans and imposes a limitation to exercise performance. J. Physiol. 586, 161-173. doi: 10.1113/jphysiol.2007.141838
7. Amann, M., Eldridge, M. W., Lovering, A. T., Stickland, M. K., Pegelow, D. F., and Dempsey, J. A. (2006b). Arterial oxygenation influences central motor output and exercise performance via effects on peripheral locomotor muscle fatigue in humans. J. Physiol. 575(Pt 3), 937-952. doi: 10.1113/jphysiol.2006.113936
8. Amann, M., Pegelow, D. F., Jacques, A. J., and Dempsey, J. A. (2007). Inspiratory muscle work in acute hypoxia influences locomotor muscle fatigue and exercise performance of healthy humans. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R2036-R2045. doi: 10.1152/ajpregu.00442.2007
9. Amann, M., Regan, M. S., Kobitary, M., Eldridge, M. W., Boutellier, U., Pegelow, D. F., et al. (2010). Impact of pulmonary system limitations on locomotor muscle fatigue in patients with COPD. Am. J. Physiol. Regul. Integr. Comp. Physiol. 299, R314-R324. doi: 10.1152/ajpregu.00183.2010
10. Amann, M., Romer, L. M., Pegelow, D. F., Jacques, A. J., Hess, C. J., and Dempsey, J. A. (2006a). Effects of arterial oxygen content on peripheral locomotor muscle fatigue. J. Appl. Physiol. 101, 119-127. doi: 10.1152/japplphysiol.01596.2005
11. Belardinelli, R., Barstow, T. J., Nguyen, P., and Wasserman, K. (1997). Skeletal muscle oxygenation and oxygen uptake kinetics following constant work rate exercise in chronic congestive heart failure. Am. J. Cardiol. 80, 1319-1324. doi: 10.1016/S0002-9149(97)00672-3
12. 2 delivery and utilisation during exercise in COPD. Thorax 65, 588-593. doi: 10.1136/thx.2009.120857
13. Borghi-Silva, A., Carrascosa, C., Oliveira, C. C., Barroco, A. C., Berton, D. C., Vilaça, D., et al. (2008b). Effects of respiratory muscle unloading on leg muscle oxygenation and blood volume during high-intensity exercise in chronic heart failure. Am. J. Physiol. Heart Circ. Physiol. 294, H2465-H2472. doi: 10.1152/ajpheart.91520.2007
14. Borghi-Silva, A., Oliveira, C. C., Carrascosa, C., Maia, J., Berton, D. C., Queiroga, F., et al. (2008a). Respiratory muscle unloading improves leg muscle oxygenation during exercise in patients with COPD. Thorax 63, 910-915. doi: 10.1136/thx.2007.090167
15. Boudestein, L. C. M., Rutten, F. H., Cramer, M. J., Lammers, J. W. J., and Hoes, A. W. (2009). The impact of concurrent heart failure on prognosis in patients with chronic obstructive pulmonary disease. Eur. J. Heart Fail. 11, 1182-1188. doi: 10.1093/eurjhf/hfp148
16. Bowen, T. S., Cannon, D. T., Murgatroyd, S. R., Birch, K. M., Witte, K. K., and Rossiter, H. B. (2012). The intramuscular contribution to the slow oxygen uptake kinetics during exercise in chronic heart failure is related to the severity of the condition. J. Appl. Physiol. 112, 378-387. doi: 10.1152/japplphysiol.00779.2011
17. Calverley, P. M. A. (2006). Dynamic hyperinflation: is it worth measuring? Proc. Am. Thorac. Soc. 3, 239-244. doi: 10.1513/pats.200508-084SF
18. Cassidy, S. S., and Mitchell, J. H. (1981). Effects of positive pressure breathing on right and left ventricular preload and afterload. Fed. Proc. 40, 2178-2181.
19. Chiappa, G. R., Borghi-Silva, A., Ferreira, L. F., Carrascosa, C., Oliveira, C. C., Maia, J., et al. (2008). Kinetics of muscle deoxygenation are accelerated at the onset of heavy-intensity exercise in patients with COPD: relationship to central cardiovascular dynamics. J. Appl. Physiol. 104, 1341-1350. doi: 10.1152/japplphysiol.01364.2007
20. Chiappa, G. R., Queiroga, F., Meda, E., Ferreira, L. F., Diefenthaeler, F., Nunes, M., et al. (2009). Heliox improves oxygen delivery and utilization during dynamic exercise in patients with chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care. Med. 179, 1004-1010. doi: 10.1164/rccm.200811-1793OC
21. 2 pressures after contractions in the rat spinotrapezius muscle. Am. J. Physiol. Heart Circ. Physiol. 299, H1755-H1761. doi: 10.1152/ajpheart.00590.2010
22. Dempsey, J. A., Romer, L., Rodman, J., Miller, J., and Smith, C. (2006). Consequences of exercise-induced respiratory muscle work. Respir. Physiol. Neurobiol. 151, 242-250. doi: 10.1016/j.resp.2005.12.015
23. Diederich, E. R., Behnke, B. J., McDonough, P., Kindig, C. A., Barstow, T. J., Poole, D. C., et al. (2002). Dynamics of microvascular oxygen partial pressure in contracting skeletal muscle of rats with chronic heart failure. Cardiovasc. Res. 56, 479-486. doi: 10.1016/S0008-6363(02)00545-X
24. Edwards, R. H., Hill, D. K., Jones, D. A., and Merton, P. A. (1977). Fatigue of long duration in human skeletal muscle after exercise. J. Physiol. 272, 769-778.
25. Gagnon, P., Bussières, J. S., Ribeiro, F., Gagnon, S. L., Saey, D., Gagné, N., et al. (2012). Influences of spinal anesthesia on exercise tolerance in patients with chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care. Med. 186, 606-615. doi: 10.1164/rccm.201203-0404OC
26. Gandevia, S. C. (2001). Spinal and supraspinal factors in human muscle fatigue. Physiol Rev. 81, 1725-1789.
27. Goodall, S., González-Alonso, J., Ali, L., Ross, E. Z., and Romer, L. M. (2012). Supraspinal fatigue after normoxic and hypoxic exercise in humans. J. Physiol. 590(Pt 11), 2767-2782. doi: 10.1113/jphysiol.2012.228890
28. Guazzi, M., Reina, G., Tumminello, G., and Guazzi, M. D. (2005). Alveolar-capillary membrane conductance is the best pulmonary function correlate of exercise ventilation efficiency in heart failure patients. Eur. J. Heart Fail. 7, 1017-1022. doi: 10.1016/j.ejheart.2004.10.009
29. Harms, C. A., Babcock, M. A., McClaran, S. R., Pegelow, D. F., Nickele, G. A., Nelson, W. B., et al. (1997). Respiratory muscle work compromises leg blood flow during maximal exercise. J. Appl. Physiol. 82, 1573-1583.
30. Hirai, T., Zelis, R., and Musch, T. I. (1995). Effects of nitric oxide synthase inhibition on the muscle blood flow response to exercise in rats with heart failure. Cardiovasc. Res. 30, 469-476. doi: 10.1016/S0008-6363(95)00068-2
31. Iandelli, I., Aliverti, A., Kayser, B., Dellacà, R., Cala, S. J., Duranti, R., et al. (2002). Determinants of exercise performance in normal men with externally imposed expiratory flow limitation. J. Appl. Physiol. 92, 1943-1952. doi: 10.1152/japplphysiol.00393.2000
32. Johnson, B. D., Weisman, I. M., Zeballos, R. J., and Beck, K. C. (1999). Emerging concepts in the evaluation of ventilatory limitation during exercise: the exercise tidal flow-volume loop. Chest 116, 488-503. doi: 10.1378/chest.116.2.488
33. Katayama, K., Amann, M., Pegelow, D. F., Jacques, A. J., and Dempsey, J. A. (2007). Effect of arterial oxygenation on quadriceps fatigability during isolated muscle exercise. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292, R1279-R1286. doi: 10.1152/ajpregu.00554.2006
34. Kindig, C. A., Musch, T. I., Basaraba, R. J., and Poole, D. C. (1999). Impaired capillary hemodynamics in skeletal muscle of rats in chronic heart failure. J. Appl. Physiol. 87, 652-660.
35. Langer, D., Ciavaglia, C. E., Neder, J. A., Webb, K. A., and O'Donnell, D. E. (2014). Lung hyperinflation in chronic obstructive pulmonary disease: mechanisms, clinical implications and treatment. Expert Rev. Respir. Med. 27, 1-19. doi: 10.1586/17476348.2014.949676
36. Mador, M. J., Deniz, O., Aggarwal, A., and Kufel, T. J. (2003). Quadriceps fatigability after single muscle exercise in patients with chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care. Med. 168, 102-108. doi: 10.1164/rccm.200202-080OC
37. Mador, M. J., Deniz, O., Deniz, O., Aggarwal, A., Shaffer, M., Kufel, T. J., et al. (2005). Effect of respiratory muscle endurance training in patients with COPD undergoing pulmonary rehabilitation. Chest 128, 1216-1224. doi: 10.1378/chest.128.3.1216
38. Merton, P. A. (1954). Voluntary strength and fatigue. J. Physiol. 123, 553-564.
39. Miller, J. D., Hemauer, S. J., Smith, C. A., Stickland, M. K., and Dempsey, J. A. (2006). Expiratory threshold loading impairs cardiovascular function in health and chronic heart failure during submaximal exercise. J. Appl. Physiol. 101, 213-227. doi: 10.1152/japplphysiol.00862.2005
40. Miller, J. D., Pegelow, D. F., Jacques, A. J., and Dempsey, J. A. (2005). Effects of augmented respiratory muscle pressure production on locomotor limb venous return during calf contraction exercise. J. Appl. Physiol. 99, 1802-1815. doi: 10.1152/japplphysiol.00278.2005
41. Millet, G. Y., and Lepers, R. (2004). Alterations of neuromuscular function after prolonged running, cycling and skiing exercises. Sports Med. 34, 105-116. doi: 10.2165/00007256-200434020-00004
42. Millet, G. Y., Martin, V., Martin, A., and Vergès, S. (2011). Electrical stimulation for testing neuromuscular function: from sport to pathology. Eur. J. Appl. Physiol. 111, 2489-2500. doi: 10.1007/s00421-011-1996-y
43. Narkiewicz, K., Pesek, C. A., van de Borne, P. J., Kato, M., and Somers, V. K. (1999). Enhanced sympathetic and ventilatory responses to central chemoreflex activation in heart failure. Circulation 100, 262-267. doi: 10.1161/01.CIR.100.3.262
44. Nóbrega, A. C., Williamson, J. W., Araújo, C. G., and Friedman, D. B. (1994). Heart rate and blood pressure responses at the onset of dynamic exercise: effect of Valsalva manoeuvre. Eur. J. Appl. Physiol. 68, 336-340. doi: 10.1007/BF00571453
45. O'Donnell, D. E., Laveneziana, P., Webb, K., and Neder, J. A. (2014). Chronic obstructive pulmonary disease: clinical integrative physiology. Clin. Chest Med. 35, 51-69. doi: 10.1016/j.ccm.2013.09.008
46. O'Donnell, D. E., Revill, S. M., and Webb, K. A. (2001). Dynamic hyperinflation and exercise intolerance in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care. Med. 164, 770-777. doi: 10.1164/ajrccm.164.5.2012122
47. Oliveira, M. F., Rodrigues, M. K., Treptow, E., Cunha, T. M., Ferreira, E. M. V., and Neder, J. A. (2012). Effects of oxygen supplementation on cerebral oxygenation during exercise in chronic obstructive pulmonary disease patients not entitled to long-term oxygen therapy. Clin. Physiol. Funct. Imaging 32, 52-58. doi: 10.1111/j.1475-097X.2011.01054.x
48. Piepoli, M., Clark, A. L., Volterrani, M., Adamopoulos, S., Sleight, P., and Coats, A. J. (1996). Contribution of muscle afferents to the hemodynamic, autonomic, and ventilatory responses to exercise in patients with chronic heart failure: effects of physical training. Circulation 93, 940-952. doi: 10.1161/01.CIR.93.5.940
49. Ponikowski, P., Chua, T. P., Anker, S. D., Francis, D. P., Doehner, W., Banasiak, W., et al. (2001). Peripheral chemoreceptor hypersensitivity: an ominous sign in patients with chronic heart failure. Circulation 104, 544-549. doi: 10.1161/hc3101.093699
50. Poole, D. C., Hirai, D. M., Copp, S. W., and Musch, T. I. (2012). Muscle oxygen transport and utilization in heart failure: implications for exercise (in)tolerance. Am. J. Physiol. Heart Circ. Physiol. 302, H1050-H1063. doi: 10.1152/ajpheart.00943.2011
51. Potter, W. A., Olafsson, S., and Hyatt, R. E. (1971). Ventilatory mechanics and expiratory flow limitation during exercise in patients with obstructive lung disease. J. Clin. Invest. 50, 910-919. doi: 10.1172/JCI106563
52. Ranieri, V. M., Dambrosio, M., and Brienza, N. (1996). Intrinsic PEEP and cardiopulmonary interaction in patients with COPD and acute ventilatory failure. Eur. Respir. J. 9, 1283-1292. doi: 10.1183/09031936.96.09061283
53. Ribeiro, J. P., Chiappa, G. R., Neder, J. A., and Frankenstein, L. (2009). Respiratory muscle function and exercise intolerance in heart failure. Curr. Heart Fail. Rep. 6, 95-101. doi: 10.1007/s11897-009-0015-7
54. Robotham, J. L., Lixfeld, W., Holland, L., MacGregor, D., Bryan, A. C., and Rabson, J. (1978). Effects of respiration on cardiac performance. J. Appl. Physiol. 44, 703-709.
55. 2 desaturation. Clin. Physiol. Funct. Imaging 33, 274-281. doi: 10.1111/cpf.12024
56. Romer, L. M., Lovering, A. T., Haverkamp, H. C., Pegelow, D. F., and Dempsey, J. A. (2006). Effect of inspiratory muscle work on peripheral fatigue of locomotor muscles in healthy humans. J. Physiol. 571(Pt 2), 425-439. doi: 10.1113/jphysiol.2005.099697
57. Rutten, F. H., Cramer, M.-J. M., Grobbee, D. E., Sachs, A. P. E., Kirkels, J. H., Lammers, J.-W. J., et al. (2005). Unrecognized heart failure in elderly patients with stable chronic obstructive pulmonary disease. Eur. Heart J. 26, 1887-1894. doi: 10.1093/eurheartj/ehi291
58. Saito, S., Miyamoto, K., Nishimura, M., Aida, A., Saito, H., Tsujino, I., et al. (1999). Effects of inhaled bronchodilators on pulmonary hemodynamics at rest and during exercise in patients with COPD. Chest 115, 376-382. doi: 10.1378/chest.115.2.376
59. Scharf, S. M. (1991). Cardiovascular effects of airways obstruction. Lung 169, 1-23. doi: 10.1007/BF02714137
60. Sheel, A. W., Derchak, P. A., Morgan, B. J., Pegelow, D. F., Jacques, A. J., and Dempsey, J. A. (2001). Fatiguing inspiratory muscle work causes reflex reduction in resting leg blood flow in humans. J. Physiol. 537(Pt 1), 277-289. doi: 10.1111/j.1469-7793.2001.0277k.x
61. Stark-Leyva, K. N., Beck, K. C., and Johnson, B. D. (2004). Influence of expiratory loading and hyperinflation on cardiac output during exercise. J. Appl. Physiol. 96, 1920-1927. doi: 10.1152/japplphysiol.00756.2003
62. St Croix, C. M., Morgan, B. J., Wetter, T. J., and Dempsey, J. A. (2000). Fatiguing inspiratory muscle work causes reflex sympathetic activation in humans. J. Physiol. 529(Pt 2), 493-504. doi: 10.1111/j.1469-7793.2000.00493.x
63. Stubbing, D. G., Pengelly, L. D., Morse, J. L., and Jones, N. L. (1980). Pulmonary mechanics during exercise in subjects with chronic airflow obstruction. J. Appl. Physiol. 49, 511-515.
64. Todd, G., Taylor, J. L., and Gandevia, S. C. (2003). Measurement of voluntary activation of fresh and fatigued human muscles using transcranial magnetic stimulation. J. Physiol. 551(Pt 2), 661-671. doi: 10.1113/jphysiol.2003.044099
65. Verges, S., Bachasson, D., and Wuyam, B. (2010). Effect of acute hypoxia on respiratory muscle fatigue in healthy humans. Respir. Res. 11:109. doi: 10.1186/1465-9921-11-109
66. Verges, S., Rupp, T., Jubeau, M., Wuyam, B., Esteve, F., Levy, P., et al. (2012). Cerebral perturbations during exercise in hypoxia. Am. J. Physiol. Regul. Integr. Comp. Physiol. 302, R903-R916. doi: 10.1152/ajpregu.00555.2011