Respiratory and limb muscle dysfunction in pulmonary arterial hypertension: A role for exercise training?

Pulmonary Circulation

Volumn 5, Issue 3, 2015, Pages 424-434

  Panagiotou, Marios ^a   Peacock, Andrew J ^a   Johnson, Martin K ^a  

^a GOLDEN JUBILEE NATIONAL HOSPITAL   (United Kingdom)

Author keywords

Pulmonary arterial hypertension; Rehabilitation; Respiratory muscles; Skeletal muscle

Indexed keywords

EID: 85026336774     PISSN: 20458932     EISSN: 20458940     Source Type: Journal    
DOI: 10.1086/682431     Document Type: Review

References (78)

1. Galiè N, Hoeper MM, Humbert M, Torbicki A, Vachiéry JL, Barberà JA, Beghetti M, et al. Guidelines for the diagnosis and treatment of pulmonary hypertension: the Task Force for the Diagnosis and Treatment of Pulmonary Hypertension of the European Society of Cardiology (ESC) and the European Respiratory Society (ERS), endorsed by the International Society of Heart and Lung Transplantation (ISHLT). Eur Heart J 2009;30(20):2493-2537.
2. Naeije R. Breathing more with weaker respiratory muscles in pulmonary arterial hypertension. Eur Respir J 2005;25(1):6-8.
3. Garcia-Aymerich J, Serra I, Gómez FP, Farrero E, Balcells E, Rodriguez DA, de Batlle J, et al. Physical activity and clinical and functional status in COPD. Chest 2009;136(1):62-70.
4. Agustí A. Systemic effects of chronic obstructive pulmonary disease: what we know and what we don’t know (but should). Proc Am Thorac Soc 2007;4(7):522-525.
5. Yndestad A, Damås JK, Øie E, Ueland T, Gullestad L, Aukrust P. Systemic inflammation in heart failure—the whys and wherefores. Heart Fail Rev 2006;11(1):83-92.
6. Huertas A, Palange P. COPD: a multifactorial systemic disease. Ther Adv Respir Dis 2011;5(3):217-224.
7. Barnes PJ, Celli BR. Systemic manifestations and comorbidities of COPD. Eur Respir J 2009;33(5):1165-1185.
8. Vijayan VK. Morbidities associated with obstructive sleep apnea. Expert Rev Respir Med 2012;6(5):557-566.
9. Sprunger DB, Olson AL, Huie TJ, Fernandez-Perez ER, Fischer A, Solomon JJ, Brown KK, Swigris JJ. Pulmonary fibrosis is associated with an elevated risk of thromboembolic disease. Eur Respir J 2012;39 (1):125-132.
10. Fowler RM, Gain KR, Gabbay E. Exercise intolerance in pulmonary arterial hypertension. Pulm Med 2012;2012:359204. doi:10.1155/2012/359204.
11. Di Carlo A, De Mori R, Martelli F, Pompilio G, Capogrossi MC, Germani A. Hypoxia inhibits myogenic differentiation through accelerated MyoD degradation. J Biol Chem 2004;279(16):16332-16338.
12. Groth A, Vrugt B, Brock M, Speich R, Ulrich S, Huber LC. Inflammatory cytokines in pulmonary hypertension. Respir Res 2014;15:47. doi:10.1186/1465-9921-15-47.
13. Janssen SP, Gayan-Ramirez G, Van den Bergh A, Herijgers P, Maes K, Verbeken E, Decramer M. Interleukin-6 causes myocardial failure and skeletal muscle atrophy in rats. Circulation 2005;111(8):996-1005.
14. Reid MB, Lännergren J, Westerblad H. Respiratory and limb muscle weakness induced by tumor necrosis factor-α: involvement of muscle myofilaments. Am J Respir Crit Care Med 2002;166(4):479-484.
15. Li YP, Chen Y, John J, Moylan J, Jin B, Mann DL, Reid MB. TNF-α acts via p38 MAPK to stimulate expression of the ubiquitin ligase atrogin1/MAFbx in skeletal muscle. FASEB J 2005;19(3):362-370.
16. Adams V, Mangner N, Gasch A, Krohne C, Gielen S, Hirner S, Thierse HJ, et al. Induction of MuRF1 is essential for TNF-α-induced loss of muscle function in mice. J Mol Biol 2008;384(1):48-59.
17. Remels A, Gosker H, Verhees K, Langen R, Schols A. TNF-α-induced NF-κB activation stimulates skeletal muscle glycolytic metabolism through activation of HIF-1α. Endocrinology 2015;156(5):1770-1781.
18. Velez-Roa S, Ciarka A, Najem B, Vachiéry JL, Naeije R, van de Borne P. Increased sympathetic nerve activity in pulmonary artery hypertension. Circulation 2004;110(10):1308-1312.
19. Zamanian RT, Hansmann G, Snook S, Lilienfeld D, Rappaport KM, Reaven GM, Rabinovitch M, Doyle RL. Insulin resistance in pulmonary arterial hypertension. Eur Respir J 2009;33(2):318-324.
20. Naderi N, Boobejame P, Bakhshandeh H, Amin A, Taghavi S, Maleki M. Insulin resistance in pulmonary arterial hypertension, is it a novel disease modifier? Res Cardiovasc Med 2014;3(3):e19710. doi:10.5812/cardiovascmed.19710.
21. Wei Y, Chen K, Whaley-Connell AT, Stump CS, Ibdah JA, Sowers JR. Skeletal muscle insulin resistance: role of inflammatory cytokines and reactive oxygen species. Am J Physiol Regul Integr Comp Physiol 2008; 294(3):R673-R680.
22. Pugh ME, Buchowski MS, Robbins IM, Newman JH, Hemnes AR. Physical activity limitation as measured by accelerometry in pulmonary arterial hypertension. Chest 2012;142(6):1391-1398.
23. Mainguy V, Provencher S, Maltais F, Malenfant S, Saey D. Assessment of daily life physical activities in pulmonary arterial hypertension. PloS ONE 2011;6(11):e27993. doi:10.1371/journal.pone.0027993.
24. Jackman RW, Kandarian SC. The molecular basis of skeletal muscle atrophy. Am J Physiol Cell Physiol 2004;287(4):C834-C843.
25. Bodine SC. Disuse-induced muscle wasting. Int J Biochem Cell Biol 2013;45(10):2200-2208.
26. Li H, Malhotra S, Kumar A. Nuclear factor-kappa B signaling in skeletal muscle atrophy. J Mol Med 2008;86(10):1113-1126.
27. Meyer FJ, Lossnitzer D, Kristen AV, Schoene AM, Kübler W, Katus HA, Borst MM. Respiratory muscle dysfunction in idiopathic pulmonary arterial hypertension. Eur Respir J 2005;25(1):125-130.
28. Meyer FJ, Borst MM, Zugck C, Kirschke A, Schellberg D, Kübler W, Haass M. Respiratory muscle dysfunction in congestive heart failure: clinical correlation and prognostic significance. Circulation 2001;103(17): 2153-2158.
29. Kabitz HJ, Schwoerer A, Bremer HC, Sonntag F, Walterspacher S, Walker D, Schaefer V, et al. Impairment of respiratory muscle function in pulmonary hypertension. Clin Sci 2008;114(2):165-171.
30. American Thoracic Society/European Respiratory Society. ATS/ERS statement on respiratory muscle testing. Am J Respir Crit Care Med 2002;166(4):518-624.
31. Ahn B, Empinado HM, Al-Rajhi M, Judge AR, Ferreira LF. Diaphragm atrophy and contractile dysfunction in a murine model of pulmonary hypertension. PloS ONE 2013;8(4):e62702. doi:10.1371/journal.pone.0062702.
32. de Man FS, van Hees HW, Handoko ML, Niessen HW, Schalij I, Humbert M, Dorfmüller P, et al. Diaphragm muscle fiber weakness in pulmonary hypertension. Am J Respir Crit Care Med 2011;183(10): 1411-1418.
33. van Hees HW, van der Heijden HF, Hafmans T, Ennen L, Heunks LM, Verheugt FW, Dekhuijzen PN. Impaired isotonic contractility and structural abnormalities in the diaphragm of congestive heart failure rats. Int J Cardiol 2008;128(3):326-335.
34. Sun XG, Hansen JE, Oudiz RJ, Wasserman K. Exercise pathophysiology in patients with primary pulmonary hypertension. Circulation 2001;104 (4):429-435.
35. Manders E, de Man FS, Handoko ML, Westerhof N, van Hees HW, Stienen GJ, Vonk-Noordegraaf A, Ottenheijm CA. Diaphragm weakness in pulmonary arterial hypertension: role of sarcomeric dysfunction. Am J Physiol Lung Cell Mol Physiol 2012;303(12):L1070-L1078.
36. Kanj NA, Nasser MG, Medawar WA, Al Tayeh AU, Khoury MY, Nassar CF. Reversal of impaired calcium homeostasis in the rat diaphragm subjected to monocrotaline-induced pulmonary hypertension. Toxicol Lett 1999;105(3):177-182.
37. Bauer R, Dehnert C, Schoene P, Filusch A, Bartsch P, Borst MM, Katus HA, Meyer FJ. Skeletal muscle dysfunction in patients with idiopathic pulmonary arterial hypertension. Respir Med 2007;101(11):2366-2369.
38. Mainguy V, Maltais F, Saey D, Gagnon P, Martel S, Simon M, Provencher S. Peripheral muscle dysfunction in idiopathic pulmonary arterial hypertension. Thorax 2010;65(2):113-117.
39. Batt J, Ahmed SS, Correa J, Bain A, Granton J. Skeletal muscle dysfunction in idiopathic pulmonary arterial hypertension. Am J Respir Cell Mol Biol 2014;50(1):74-86.
40. Breda AP, Pereira de Albuquerque AL, Jardim C, Morinaga LK, Suesada MM, Fernandes CJ, Dias B, Lourenço RB, Salge JM, Souza R. Skeletal muscle abnormalities in pulmonary arterial hypertension. PloS ONE 2014;9(12):e114101. doi:10.1371/journal.pone.0114101.
41. Debigaré R, Marquis K, Côté CH, Tremblay RR, Michaud A, LeBlanc P, Maltais F. Catabolic/anabolic balance and muscle wasting in patients with COPD. Chest 2003;124(1):83-89.
42. Wüst RC, Myers DS, Stones R, Benoist D, Robinson PA, Boyle JP, Peers C, White E, Rossiter HB. Regional skeletal muscle remodeling and mitochondrial dysfunction in right ventricular heart failure. Am J Physiol Heart Circ Physiol 2012;302(2):H402-H411.
43. Dimopoulos S, Tzanis G, Manetos C, Tasoulis A, Mpouchla A, Tseliou E, Vasileiadis I, Diakos N, Terrovitis J, Nanas S. Peripheral muscle microcirculatory alterations in patients with pulmonary arterial hypertension: a pilot study. Respir Care 2013;58(12):2134-2141.
44. Peled N, Bendayan D, Shitrit D, Fox B, Yehoshua L, Kramer MR. Peripheral endothelial dysfunction in patients with pulmonary arterial hypertension. Respir Med 2008;102(12):1791-1796.
45. Wolff B, Lodziewski S, Bollmann T, Opitz CF, Ewert R. Impaired peripheral endothelial function in severe idiopathic pulmonary hypertension correlates with the pulmonary vascular response to inhaled iloprost. Am Heart J 2007;153(6):1088.e1-1088.e7.
46. Peled N, Shitrit D, Fox BD, Shlomi D, Amital A, Bendayan D, Kramer MR. Peripheral arterial stiffness and endothelial dysfunction in idiopathic and scleroderma associated pulmonary arterial hypertension. J Rheumatol 2009;36(5):970-975.
47. Gabrielli LA, Castro PF, Godoy I, Mellado R, Bourge RC, Alcaino H, Chiong M, et al. Systemic oxidative stress and endothelial dysfunction is associated with an attenuated acute vascular response to inhaled prostanoid in pulmonary artery hypertension patients. J Card Fail 2011; 17(12):1012-1017.
48. Friedman D, Szmuszkovicz J, Rabai M, Detterich JA, Menteer J, Wood JC. Systemic endothelial dysfunction in children with idiopathic pulmonary arterial hypertension correlates with disease severity. J Heart Lung Transplant 2012;31(6):642-647.
49. Dibble CT, Shimbo D, Barr RG, Bagiella E, Chahal H, Ventetuolo CE, Herrington DM, Lima JA, Bluemke DA, Kawut SM. Brachial artery diameter and the right ventricle: the Multi-Ethnic Study of Atherosclerosis-Right Ventricle Study. Chest 2012;142(6):1399-1405.
50. Garfield BE, Parfitt L, Harries C, Dimopoulos K, Gatzoulis M, Kemp P, Polkey MI, Wort SJ. S144. Quality of life in idiopathic pulmonary arterial hypertension is associated with quadriceps function and size. Thorax 2014;69(suppl. 2):A76-A77.
51. Miyamoto S, Nagaya N, Satoh T, Kyotani S, Sakamaki F, Fujita M, Nakanishi N, Miyatake K. Clinical correlates and prognostic significance of six-minute walk test in patients with primary pulmonary hypertension: comparison with cardiopulmonary exercise testing. Am J Respir Crit Care Med 2000;161(2):487-492.
52. Vogiatzis I, Zakynthinos S. Factors limiting exercise tolerance in chronic lung diseases. Compr Physiol 2012;2(3):1779-1817.
53. Chua TP, Anker SD, Harrington D, Coats AJ. Inspiratory muscle strength is a determinant of maximum oxygen consumption in chronic heart failure. Br Heart J 1995;74(4):381-385.
54. Boushel R. Muscle metaboreflex control of the circulation during exercise. Acta Physiol 2010;199(4):367-383.
55. Sheel AW, Derchak PA, Morgan BJ, Pegelow DF, Jacques AJ, Dempsey JA. Fatiguing inspiratory muscle work causes reflex reduction in resting leg blood flow in humans. J Physiol 2001;537(1):277-289.
56. Amann M, Pegelow DF, Jacques AJ, Dempsey JA. Inspiratory muscle work in acute hypoxia influences locomotor muscle fatigue and exercise performance of healthy humans. Am J Physiol Regul Integr Comp Physiol 2007;293(5):R2036-R2045.
57. Clark AL, Poole-Wilson PA, Coats AJ. Exercise limitation in chronic heart failure: central role of the periphery. J Am Coll Cardiol 1996;28 (5):1092-1102.
58. Chiappa GR, Vieira PJ, Umpierre D, Correa AP, Berton DC, Ribeiro JP, Neder JA. Inspiratory resistance decreases limb blood flow in COPD patients with heart failure. Eur Respir J 2014;43(5):1507-1510.
59. Smith SA, Downey RM, Williamson JW, Mizuno M. Autonomic dysfunction in muscular dystrophy: a theoretical framework for muscle reflex involvement. Front Physiol 2014;5:47. doi:10.3389/fphys.2014.00047.
60. Spruit MA, Singh SJ, Garvey C, ZuWallack R, Nici L, Rochester C, Hill K, 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(8):e13-e64.
61. Babu AS, Padmakumar R, Maiya AG. A review of ongoing trials in exercise based rehabilitation for pulmonary arterial hypertension. Indian J Med Res 2013;137(5):900-906.
62. Grünig E, Ehlken N, Ghofrani A, Staehler G, Meyer FJ, Juenger J, Opitz CF, et al. Effect of exercise and respiratory training on clinical progression and survival in patients with severe chronic pulmonary hypertension. Respiration 2011;81(5):394-401.
63. Mainguy V, Maltais F, Saey D, Gagnon P, Martel S, Simon M, Provencher S. Effects of a rehabilitation program on skeletal muscle function in idiopathic pulmonary arterial hypertension. J Cardiopulm Rehabil Prev 2010;30(5):319-323.
64. Zafrir B. Exercise training and rehabilitation in pulmonary arterial hypertension: rationale and current data evaluation. J Cardiopulm Rehabil Prev 2013;33(5):263-273.
65. Mereles D, Ehlken N, Kreuscher S, Ghofrani S, Hoeper MM, Halank M, Meyer FJ, et al. Exercise and respiratory training improve exercise capacity and quality of life in patients with severe chronic pulmonary hypertension. Circulation 2006;114(14):1482-1489.
66. de Man FS, Handoko ML, Groepenhoff H, van ’t Hul AJ, Abbink J, Koppers RJ, Grotjohan HP, et al. Effects of exercise training in patients with idiopathic pulmonary arterial hypertension. Eur Respir J 2009;34(3):669-675.
67. Kabitz HJ, Bremer HC, Schwoerer A, Sonntag F, Walterspacher S, Walker DJ, Ehlken N, Staehler G, Windisch W, Grünig E. The combination of exercise and respiratory training improves respiratory muscle function in pulmonary hypertension. Lung 2014;192(2):321-328.
68. Grünig E, Lichtblau M, Ehlken N, Ghofrani HA, Reichenberger F, Staehler G, Halank M, et al. Safety and efficacy of exercise training in various forms of pulmonary hypertension. Eur Respir J 2012;40(1): 84-92.
69. Gielen S, Adams V, Möbius-Winkler S, Linke A, Erbs S, Yu J, Kempf W, Schubert A, Schuler G, Hambrecht R. Anti-inflammatory effects of exercise training in the skeletal muscle of patients with chronic heart failure. J Am Coll Cardiol 2003;42(5):861-868.
70. Linke A, Schoene N, Gielen S, Hofer J, Erbs S, Schuler G, Hambrecht R. Endothelial dysfunction in patients with chronic heart failure: systemic effects of lower-limb exercise training. J Am Coll Cardiol 2001; 37(2):392-397.
71. Roveda F, Middlekauff HR, Rondon MU, Reis SF, Souza M, Nastari L, Barretto AC, Krieger EM, Negrão CE. The effects of exercise training on sympathetic neural activation in advanced heart failure: a randomized controlled trial. J Am Coll Cardiol 2003;42(5):854-860.
72. Gielen S, Adams V, Linke A, Erbs S, Möbius-Winkler S, Schubert A, Schuler G, Hambrecht R. Exercise training in chronic heart failure: correlation between reduced local inflammation and improved oxidative capacity in the skeletal muscle. Eur J Cardiovasc Prev Rehabil 2005; 12(4):393-400.
73. Gielen S, Laughlin MH, O’Conner C, Duncker DJ. Exercise training in patients with heart disease: review of beneficial effects and clinical recommendations. Prog Cardiovasc Dis 2015;57(4):347-355.
74. Simoneau JA, Bouchard C. Genetic determinism of fiber type proportion in human skeletal muscle. FASEB J 1995;9(11):1091-1095.
75. Andersen P, Henriksson J. Training induced changes in the subgroups of human type II skeletal muscle fibres. Acta Physiol Scand 1977;99(1):123-125.
76. Fukuda Y, Tanaka H, Motoji Y, Ryo K, Sawa T, Imanishi J, Miyoshi T, et al. Utility of combining assessment of right ventricular function and right atrial remodeling as a prognostic factor for patients with pulmonary hypertension. Int J Cardiovasc Imaging 2014;30(7):1269-1277.
77. Vonk Noordegraaf A, Galiè N. The role of the right ventricle in pulmonary arterial hypertension. Eur Respir Rev 2011;20(122):243-253.
78. Ross RM. ATS/ACCP statement on cardiopulmonary exercise testing. Am J Respir Crit Care Med 2003;167(10):1451; author reply 1451.