Heart Failure Reviews

, Volume 15, Issue 6, pp 563–579 | Cite as

Functional electrical stimulation of lower limbs in patients with chronic heart failure

  • Apostolos Karavidas
  • Sophia M. ArapiEmail author
  • Vlassios Pyrgakis
  • Stamatis AdamopoulosEmail author


Physical training is an important component of therapy for patients with chronic heart failure (CHF) and is considered complementary to their pharmacological treatment. The majority of conventional rehabilitation programs include aerobic training, which has been demonstrated to induce significant beneficial effects on the neurohumoral, immunoreactive and functional status of patients with moderate CHF. Functional electrical stimulation (FES) of skeletal muscles constitutes an alternative training mode with beneficial effects comparable to classical aerobic exercise, suitable for patients with CHF who cannot participate in traditional training programs due to either advanced grades of CHF or the presence of comorbidities. We present a review of the numerous studies evaluating the effects of FES in CHF, focusing on its main effects on skeletal myopathy reversal, exercise tolerance improvement and quality of life modification.


Functional electrical stimulation Neuromuscular stimulation Skeletal muscles Heart failure Exercise training 


Conflicts of interest statement



  1. 1.
    Sullivan MJ, Cobb FR (1992) Central hemodynamic response to exercise in patients with chronic heart failure. Chest 101(5 suppl):340S–346SPubMedGoogle Scholar
  2. 2.
    Franciosa JA, Park M, Levine TB (1981) Lack of correlation between exercise capacity and indexes of resting left ventricular performance in heart failure. Am J Cardiol 47:33–39PubMedGoogle Scholar
  3. 3.
    Wilson JR, Martin JL, Schwartz D et al (1984) Exercise intolerance in patients with chronic heart failure: role of impaired nutritive flow to skeletal muscle. Circulation 69:1079–1087PubMedGoogle Scholar
  4. 4.
    Cohn JN, Ferrari R, Sharpe N (2000) Cardiac remodeling: concepts and clinical implications: a consensus paper from an international forum on cardiac remodeling. J Am Coll Cardiol 35:569–582PubMedGoogle Scholar
  5. 5.
    Brunner-La Rocca HP, Weilenmann D, Schalcher C et al (1999) Prognostic significance of oxygen uptake kinetics during low level exercise in patients with heart failure. Am J Cardiol 84:741–744PubMedGoogle Scholar
  6. 6.
    Nanas S, Nanas J, Kassiotis C et al (1999) Respiratory muscles performance is related to oxygen kinetics during maximal exercise and early recovery in patients with congestive heart failure. Circulation 100:503–508PubMedGoogle Scholar
  7. 7.
    Puri S, Baker BL, Dutka DP, Oakley CM, Hughes JM, Cleland JG (1995) Reduced alveolar-capillary membrane diffusing capacity in chronic heart failure. Its pathophysiological relevance and relationship to exercise performance. Circulation 91(11):2769–2774PubMedGoogle Scholar
  8. 8.
    Clark AL, Volterrani M, Swan JW, Coats AJ (1997) The increased ventilatory response to exercise in chronic heart failure: relation to pulmonary pathology. Heart 77(2):138–146PubMedGoogle Scholar
  9. 9.
    Wilson JR, Mancini DM (1993) Factors contributing to exercise limitation of heart failure. J Am Coll Cardiol 22(Suppl A):93A–98APubMedGoogle Scholar
  10. 10.
    Drexler H, Riede U, Münzel T, König H, Funke E, Just H (1992) Alterations of skeletal muscle in chronic heart failure. Circulation 85:1751–1759PubMedGoogle Scholar
  11. 11.
    Mancini DM, Coyle E, Coggan A, Beltz J, Ferraro N, Montain S, Wilson JR (1989) Contribution of intrinsic skeletal muscle metabolic changes to 31P NMR skeletal muscle metabolic abnormalities in patients with chronic heart failure. Circulation 80:1338–1346PubMedGoogle Scholar
  12. 12.
    Sullivan MJ, Green HJ, Cobb FR (1991) Altered skeletal muscle metabolic response to exercise in chronic heart failure. Relation to skeletal muscle aerobic enzyme activity. Circulation 84:1868–1870Google Scholar
  13. 13.
    Piepoli M, Clark AL, Coats AJ (1995) Muscle metaboreceptors in hemodynamic, autonomic, and ventilatory responses to exercise in men. Am J Physiol 269(4 Pt 2):H1428–H1436PubMedGoogle Scholar
  14. 14.
    Coats AJS (1993) Exercise rehabilitation in chronic heart failure. Am Coll Cardiol 22:172A–177AGoogle Scholar
  15. 15.
    Katz SD, Krum H, Khan T, Knecht M (1996) Exercise-induced vasodilation in forearm circulation of normal subjects and patients with congestive heart failure: role of endothelium-derived nitric oxide. J Am Coll Cardiol 28(3):585–590PubMedGoogle Scholar
  16. 16.
    Piña IL, Apstein CS, Balady JG, Belardinelli R, Chaitman BR, Duscha BD (2003) AHA scientific statement: exercise and heart failure. A statement from the American Heart Association Committee on exercise, rehabilitation and prevention. Circulation 107:1210–1225PubMedGoogle Scholar
  17. 17.
    Sullivan MJ, Hawthorne MH (1995) Exercise intolerance in patients with chronic heart failure. Prog Cardiovasc Dis 38:1–22PubMedGoogle Scholar
  18. 18.
    Myers J, Froelicher VF (1991) Hemodynamic determinants of exercise capacity in chronic heart failure. Ann Int Med 115:377–386PubMedGoogle Scholar
  19. 19.
    Nakamura M, Ishikawa M, Funakoshi T et al (1994) Attenuated endothelium-dependent peripheral vasodilation and clinical characteristics in patients with chronic heart failure. Am Heart J 128:1164–1169PubMedGoogle Scholar
  20. 20.
    Zelis R, Sinoway LI, Musch TL et al (1988) Regional blood flow in congestive heart failure: concept of compensatory mechanisms with short and long time constants. Am J Cardiol 62:2E–8EPubMedGoogle Scholar
  21. 21.
    Le Jemtel T, Padeletti M, Jelic S (2007) Diagnostic and therapeutic challenges in patients with coexistent chronic obstructive pulmonary disease and chronic heart failure. J Am Coll Cardiol 49:171–180PubMedGoogle Scholar
  22. 22.
    Vescovo G, Zennaro R, Sandri M, Carraro U, Leprotti C, Ceconi C, Ambrosio GB, Dalla Libera L (1998) Apoptosis of skeletal muscle myofibers and interstitial cells in experimental heart failure. J Mol Cell Cardiol 30:2449–2459PubMedGoogle Scholar
  23. 23.
    Piepoli MF, Kaczmarek A, Francis DP, Davies LC, Rauchhaus M, Jankowska EA, Anker SC, Capucci A, Banasiak W, Ponikowski P (2006) Reduced peripheral skeletal muscle mass and abnormal reflex physiology in chronic heart failure. Circluation 114(2):126–134Google Scholar
  24. 24.
    Clark AL, Poole-Wilson PA (1996) Exercise limitation in chronic heart failure: central role of periphery. J Am Coll Cardiol 28:1092–1102PubMedGoogle Scholar
  25. 25.
    Bacurau AV, Jardim MA, Ferreira JC, Bechara LR, Bueno CR Jr, Alba-Loureiro TC, Negrao CE, Casarini DE, Curi R, Ramires PR, Moriscot AS, Brum PC (2009) Sympathetic hyperactivity differentially affects skeletal muscle mass in developing heart failure: role of exercise training. J Appl Physiol 106(5):1631–1640 (Epub 2009 Jan 29)PubMedGoogle Scholar
  26. 26.
    Adams V, Nehrhoff B, Späte U, Linke A, Schulze PC, Baur A, Gielen S, Hambrecht R, Schuler G (2002) Induction of iNOS expression in skeletal muscle by IL-1beta and NFkappaB activation: an in vitro and in vivo study. Cardiovasc Res 54(1):95–104PubMedGoogle Scholar
  27. 27.
    Schulze PC, Gielen S, Adams V, Linke A, Möbius-Winkler S, Erbs S, Kratzsch J, Hambrecht R, Schuler G (2003) Muscular levels of proinflammatory cytokines correlate with a reduced expression of insulin like growth factor-I in chronic heart failure. Basic Res Cardiol 98(4):267–274PubMedGoogle Scholar
  28. 28.
    Hambrecht R, Schulze PC, Gielen S, Linke A, Möbius-Winkler S, Yu J, Kratzsch JJ, Baldauf G, Busse MW, Schubert A, Adams V, Schuler G (2002) Reduction of insulin-like growth factor-I expression in the skeletal muscle of noncachectic patients with chronic heart failure. J Am Coll Cardiol 39:1175–1181PubMedGoogle Scholar
  29. 29.
    Latres E, Amini AR, Amini AA, Griffiths J, Martin FJ, Wei Y, Lin HC, Yancopoulos GD, Glass DJ (2005) Insulin-like growth factor-1 (IGF-1) inversely regulates atrophy-induced genes via the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin (PI3K/Akt/mTOR) pathway. J Biol Chem 280:2737–2744PubMedGoogle Scholar
  30. 30.
    Schulze PC, Fang J, Kassik KA, Gannon J, Cupesi M, MacGillivray C, Lee RT, Rosenthal N (2005) Transgenic overexpression of locally acting IGF-1 inhibits ubiquitin-mediated muscle atrophy in chronic left ventricular dysfunction. Circ Res 97:418–426PubMedGoogle Scholar
  31. 31.
    Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A, Walsh K, Schiaffino S, Lecker SH, Goldberg AL (2004) Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117:399–412PubMedGoogle Scholar
  32. 32.
    Du J, Wang X, Miereles C, Bailey JL, Debigare R, Zheng B, Price SR, Mitch WE (2004) Activation of caspase-3 is an initial step triggering accelerated muscle proteolysis in catabolic conditions. J Clin Invest 113:115–123PubMedGoogle Scholar
  33. 33.
    Conraads VM, Hoymans VY, Vermeulen T, Beckers P, Possemiers N, Maeseneer MD, Vrints C, Martinet W (2009) Exercise capacity in chronic heart failure patients is related to active gene transcription in skeletal muscle and not apoptosis. Eur J Cardiovasc Prev Rehabil 16(3):325–332PubMedGoogle Scholar
  34. 34.
    Giannuzzi P, Temporelli PL, Corra U, Tavazzi L, ELVD-CHF Study Group (2003) Antiremodelling effect of long-term exercise training in patients with stable chronic heart failure: results of the Exercise in Left Ventricular Dysfunction and Chronic Heart Failure (ELVD-CHF) Trial. Circulation 108(5):554–559PubMedGoogle Scholar
  35. 35.
    Guazzi M, Reina G, Tumminello G, Guazzi MD (2004) Improvement of alveolar-capillary membrane diffusing capacity with exercise training in chronic heart failure. J Appl Physiol 97(5):1866–1873PubMedGoogle Scholar
  36. 36.
    Piepoli ME (2005) Exercise training in heart failure. Curr Cardiol Reports 7(3):216–222Google Scholar
  37. 37.
    Hornig B, Maier V, Drexler H (1996) Physical training improves endothelial function in patients with chronic heart failure. Circulation 93(2):210–214PubMedGoogle Scholar
  38. 38.
    Hambrecht R, Fiehn E, Yu J, Niebauer J, Weigl C, Hilbrich L, Adams V, Riede U, Schuler G (1997) Effects of endurance training on mitochondrial ultrastructure and fiber type distribution in skeletal muscle of patients with stable chronic heart failure. J Am Coll Cardiol 29:1067–1073PubMedGoogle Scholar
  39. 39.
    Adamopoulos S, Coats AJ, Brunotte F, Arnolda L, Meyer T, Thompson CH, Dunn JF, Stratton J, Kemp GJ, Radda GK, Sleight P, Rajagopalan B (1993) Physical training improves skeletal muscle metabolism in patients with chronic heart failure. J Am Coll Cardiol 21(5):1101–1106PubMedGoogle Scholar
  40. 40.
    Schulze PC, Gielen S, Schuler G, Hambrecht R (2002) Chronic heart failure and skeletal muscle catabolism: effects of exercise training. Int J Cardiol 85(1):141–149PubMedGoogle Scholar
  41. 41.
    Piepoli M, Clark AL, Volterrani M, Adamopoulos S, Sleight P, Coats AJ (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(5):940–952PubMedGoogle Scholar
  42. 42.
    Roveda F, Middlekauff HR, Rondon MU et al (2003) The effects of exercise training on sympathetic neural activation in advanced heart failure: a randomized controlled trial. JACC 42(5):854–860PubMedGoogle Scholar
  43. 43.
    Coats AJS, Adamopoulos S, Radaelli A, McCance A, Meyer TE, Bernardi L, Solda PL, Davey P, Ormerod O, Forfar C, Conway J, Sleight P (1992) Controlled trial of physical training in chronic heart failure: exercise performance, hemodynamics, ventilation and autonomic function. Circulation 85:2119–2131PubMedGoogle Scholar
  44. 44.
    Adamopoulos S, Ponikowski P, Cerquetani E, Piepoli M, Rosano G, Sleight P, Coats AJ (1995) Circadian pattern of heart rate variability in chronic heart failure patients. Effects of physical training. Eur Heart J 16(10):1380–1386PubMedGoogle Scholar
  45. 45.
    Myers J, Hadley D, Oswald U et al (2007) Effects of exercise training on heart rate recovery in patients with chronic heart failure. Am Heart J 153(6):1056–1063PubMedGoogle Scholar
  46. 46.
    Liu JL, Kulakofsky J, Zucker IH (2002) Exercise training enhances baroreflex control of heart rate by a vagal mechanism in rabbits with heart failure. J Appl Physiol 92(6):2403–2408PubMedGoogle Scholar
  47. 47.
    Gao L, Wang W, Liu D, Zucker IH (2007) Exercise training normalizes sympathetic outflow by central antioxidant mechanisms in rabbits with pacing-induced chronic heart failure. Circulation 115(24):3095–3102PubMedGoogle Scholar
  48. 48.
    Passino C, Severino S, Poletti R, Piepoli MF, Mammini C, Clerico A, Gabutti A, Nassi G, Emdin M (2006) Aerobic training decreases B-type natriuretic peptide expression and adrenergic activation in patients with heart failure. JACC 47(9):1835–1839PubMedGoogle Scholar
  49. 49.
    Adamopoulos S, Parissis J, Karatzas D, Kroupis C, Georgiadis M, Karavolias D, Paraskevaidis J, Koniavitou K, Koats AJ, Kremastinos DT (2002) Physical training modulates proinflammatory cytokines and soluble Fas/soluble Fas ligand system in patients with chronic heart failure. J Am Coll Cardiol 39:653–663PubMedGoogle Scholar
  50. 50.
    Gielen S, Adams V, Möbius-Winkler S, Linke A, Erbs S, Yu J, Kempf W, Schubert A, Schuler G, Hambrecht R (2003) Anti-inflammatory effects of exercise training in the skeletal muscle of patients with chronic heart failure. J Am Coll Cardiol 42:861–868PubMedGoogle Scholar
  51. 51.
    Linke A, Adams V, Schulze PC et al (2005) Antioxidative effects of exercise training in patients with chronic heart failure: increase in radical scavenger enzyme activity in skeletal muscle. Circulation 111(14):1763–1770PubMedGoogle Scholar
  52. 52.
    Gielen S, Adams V, Linke A, Erbs S, Möbius-Winkler S, Schubert A, Schuler G, Hambrecht R (2005) Exercise training in chronic heart failure: correlation between reduced local inflammation and improved oxidative capacity in the skeletal muscle. Eur J Cardiovasc Prev Rehabil 12(4):393–400PubMedGoogle Scholar
  53. 53.
    Maiorana A, O’Driscoll G, Dembo L, Cheetham C, Goodman C, Taylor R, Green D (2000) Effect of aerobic and resistance exercise training on vascular function in heart failure. Am J Physiol Heart Circ Physiol 279(4):H1999–H2005PubMedGoogle Scholar
  54. 54.
    Laufs U, Werner N, Link A et al (2004) Physical training increases endothelial progenitor cells, inhibits neointima formation, and enhances angiogenesis. Circulation 109(2):220–226PubMedGoogle Scholar
  55. 55.
    Sarto P, Balducci E, Balconi G, Fiordaliso F, Merlo L, Tuzzato G, Pappagallo GL, Frigato N, Zanocco A, Forestieri C, Azzarello G, Mazzucco A, Valenti MT, Alborino F, Noventa D, Vinante O, Pascotto P, Sartore S, Dejana E, Latini R (2007) Effects of exercise training on endothelial progenitor cells in patients with chronic heart failure. J Card Fail 13(9):701–708PubMedGoogle Scholar
  56. 56.
    Hambrecht R, Fiehn E, Weigl C, Gielen S, Hamann C, Kaiser R, Yu J, Adams V, Niebauer J, Schuler G (1998) Regular physical exercise corrects endothelial dysfunction and improves exercise capacity in patients with chronic heart failure. Circulation 98(24):2709–2715PubMedGoogle Scholar
  57. 57.
    You Fang Z, Marwick T (2003) Mechanisms of exercise training in patients with heart failure. Am Heart J 145:904–911PubMedGoogle Scholar
  58. 58.
    Pu CT, Johnson MT, Forman DE, Hausdorff JM, Roubenoff R, Foldvari M, Fielding RA, Singh MA (2001) Randomized trial of progressive resistance training to counteract the myopathy of chronic heart failure. J Appl Physiol 90:2341–2350PubMedGoogle Scholar
  59. 59.
    Beckers PJ, Denollet J, Possemiers NM, Wuyts FL, Vrints CJ, Conraads VM (2008) Combined endurance-resistance training vs. endurance training in patients with chronic heart failure: a prospective randomized study. Eur Heart J 29(15):1858–1866PubMedGoogle Scholar
  60. 60.
    Larsen AI, Lindal S, Aukrust P, Toft I, Aarsland T, Dickstein K (2002) Effect of exercise training on skeletal muscle fibre characteristics in men with chronic heart failure. Correlation between skeletal muscle alterations, cytokines and exercise capacity. Int J Cardiol 83(1):25–32PubMedGoogle Scholar
  61. 61.
    Sullivan MJ, Higginbotham MB, Cobb FR (1988) Exercise training in patients with severe left ventricular dysfunction. Hemodynamic and metabolic effects. Circulation 78(3):506–515PubMedGoogle Scholar
  62. 62.
    Hambrecht R, Niebauer J, Fiehn E, Kälberer B, Offner B, Hauer K, Riede U, Schlierf G, Kübler W, Schuler G (1995) Physical training in patients with stable chronic heart failure: effects on cardiorespiratory fitness and ultrastructural abnormalities of leg muscles. J Am Coll Cardiol 25(6):1239–1249PubMedGoogle Scholar
  63. 63.
    Brunotte F, Thompson CH, Adamopoulos S, Coats A, Unitt J, Lindsay D, Kaklamanis L, Radda GK, Rajagopalan B (1995) Rat skeletal muscle metabolism in experimental heart failure: effects of physical training. Acta Physiol Scand 154(4):439–447PubMedGoogle Scholar
  64. 64.
    Ventura-Clapier R, Mettauer B, Bigard X (2007) Beneficial effects of endurance training on cardiac and skeletal muscle energy metabolism in heart failure. Cardiovasc Res 73(1):10–18PubMedGoogle Scholar
  65. 65.
    Garnier A, Fortin D, Delomenie C, Momken I, Veksler V, Ventura-Clapier R (2003) Depressed mitochondrial transcription factors and oxidative capacity in rat failing cardiac and skeletal muscles. J Physiol 551:491–501PubMedGoogle Scholar
  66. 66.
    Wisløff U, Støylen A, Loennechen JP, Bruvold M, Rognmo Ø, Haram PM, Tjønna AE, Helgerud J, Slørdahl SA, Lee SJ, Videm V, Bye A, Smith GL, Najjar SM, Ellingsen Ø, Skjaerpe T (2007) Superior cardiovascular effect of aerobic interval training versus moderate continuous training in heart failure patients: a randomized study. Circulation 115(24):3086–3094PubMedGoogle Scholar
  67. 67.
    Keteyian SJ, Levine AB, Brawner CA, Kataoka T, Rogers FJ, Schairer JR, Stein PD, Levine TB, Goldstein S (1996) Exercise training in patients with heart failure: a randomized, controlled trial. Ann Int Med 124:1051–1057PubMedGoogle Scholar
  68. 68.
    Dubach P, Myers J, Dziekan G, Goebbels U, Reinhart W, Muller P, Buser P, Stulz P, Vogt P, Ratti R (1997) The effect of high intensity exercise training on central hemodynamic response to exercise in men with reduced left ventricular function. J Am Coll Cardiol 29:1591–1598PubMedGoogle Scholar
  69. 69.
    Belardinelli R, Georgiou D, Cianci G, Purcaro A (1999) Randomized, controlled trial of long-term moderate exercise training in chronic heart failure: effects on functional capacity, quality of life, and clinical outcome. Circulation 99(9):1173–1182PubMedGoogle Scholar
  70. 70.
    Beer M, Wagner D, Myers J, Sandstede J, Köstler H, Hahn D, Neubauer S, Dubach P (2008) Effects of exercise training on myocardial energy metabolism and ventricular function assessed by quantitative phosphorus-31 magnetic resonance spectroscopy and magnetic resonance imaging in dilated cardiomyopathy. J Am Coll Cardiol 51(19):1883–1891PubMedGoogle Scholar
  71. 71.
    European Heart Failure Training Group (1998) Experience from controlled trials of physical training in chronic heart failure. Protocol and patient factors in effectiveness in the improvement in exercise tolerance. Eur Heart J 19(3):466–475Google Scholar
  72. 72.
    Piepoli MF, Davos C, Francis DP, Coats AJS, ExTraMATCH Collaborative (2004) Exercise training meta-analysis of trials in patients with chronic heart failure (ExTraMATCH). BMJ 328:189–198PubMedGoogle Scholar
  73. 73.
    O’Connor CM, Whellan DJ, Lee KL, Keteyian SJ, Cooper LS, Ellis SJ, Leifer ES, Kraus WE, Kitzman DW, Blumenthal JA, Rendall DS, Miller NH, Fleg JL, Schulman KA, McKelvie RS, Zannad F, Piña IL, HF-ACTION Investigators (2009) Efficacy and safety of exercise training in patients with chronic heart failure: HF-ACTION randomized controlled trial. JAMA 301(14):1439–1450PubMedGoogle Scholar
  74. 74.
    Dickstein K, Cohen-Solal A, Filippatos G, McMurray JJ, Ponikowski P, Poole-Wilson PA, Strömberg A, van Veldhuisen DJ, Atar D, Hoes AW, Keren A, Mebazaa A, Nieminen M, Priori SG, Swedberg K, Vahanian A, Camm J, De Caterina R, Dean V, Dickstein K, Filippatos G, Funck-Brentano C, Hellemans I, Kristensen SD, McGregor K, Sechtem U, Silber S, Tendera M, Widimsky P, Zamorano JL, Tendera M, Auricchio A, Bax J, Böhm M, Corrà U, della Bella P, Elliott PM, Follath F, Gheorghiade M, Hasin Y, Hernborg A, Jaarsma T, Komajda M, Kornowski R, Piepoli M, Prendergast B, Tavazzi L, Vachiery JL, Verheugt FW, Zamorano JL, Zannad F (2008) ESC guidelines for the diagnosis and treatment of acute and chronic heart failure 2008: the Task Force for the diagnosis and treatment of acute and chronic heart failure 2008 of the European Society of Cardiology. Developed in collaboration with the Heart Failure Association of the ESC (HFA) and endorsed by the European Society of Intensive Care Medicine (ESICM). Eur Heart J 10(10):933–989Google Scholar
  75. 75.
    Roy RR, Meadows ID, Baldwin KM, Edgerton VR (1982) Functional significance of compensatory overloaded rat fast muscle. J Appl Physiol 52:473–478PubMedGoogle Scholar
  76. 76.
    Buller AJ, Eccles JC, Eccles RM (1960) Interactions between motoneurones and muscles in respect of the characteristic speeds of their responses. J Physiol 150:417–439PubMedGoogle Scholar
  77. 77.
    Kanno S, Oda N, Abe M, Saito S, Hori K, Handa Y, Tabayashi K, Sato Y (1999) Establishment of a simple and practical procedure applicable to therapeutic angiogenesis. Circulation 99:2682–2687PubMedGoogle Scholar
  78. 78.
    Annex BH, Torgan CE, Lin P, Taylor DA, Thompson MA, Peters KG, Kraus WE (1998) Induction and maintenance of increased VEGF protein by chronic motor nerve stimulation in skeletal muscle. Am J Physiol 274:H860–H867PubMedGoogle Scholar
  79. 79.
    Pette D, Vrbová G (1999) What does chronic electrical stimulation teach us about muscle plasticity? Muscle Nerve 22:666–677 (Review)PubMedGoogle Scholar
  80. 80.
    Browson C, Isenberg H, Brown W, Salmons S, Edwards Y (1988) Changes in skeletal muscle gene transcription induced by chronic stimulation. Muscle Nerve 11:1183–1189Google Scholar
  81. 81.
    Williams RS, Garcia-Moll M, Mellor J, Salmons S, Harlan W (1987) Adaptation of skeletal muscle to increase contractile activity. Expression of nuclear genes encoding mitochondrial proteins. J Biol Chem 262:2764–2767PubMedGoogle Scholar
  82. 82.
    Heilmann C, Muller W, Pette D (1981) Correlation between ultrastructural and functional changes in sarcoplasmic reticulum during chronic stimulation of fast muscle. J Membrane Biol 59:143–149Google Scholar
  83. 83.
    Hudlická O, Dodd L, Renkin EM, Gray SD (1982) Early changes in fiber profile and capillary density in long-term stimulated muscles. Am J Physiol 243:H528–H535PubMedGoogle Scholar
  84. 84.
    Salmons S, Gale DR, Sreter FA (1978) Ultrastructural aspects of the transformation of muscle fibre type by long-term stimulation: changes in Z discs and mitochondria. J Anat 127:17–31PubMedGoogle Scholar
  85. 85.
    Salmons S, Sreter FA (1976) Significance of impulse activity in the transformation of skeletal muscle type. Nature 263:30–34PubMedGoogle Scholar
  86. 86.
    Gordon T, Mao J (1994) Muscle atrophy and procedures for training after spinal cord injury. Phys Ther 74:50–60 (Review)PubMedGoogle Scholar
  87. 87.
    Jacobs PL, Nash MS (2001) Modes, benefits and risks of voluntary and electrically induced exercise in persons with spinal cord injury. J Spinal Cord Med 24:10–18 (Review)PubMedGoogle Scholar
  88. 88.
    Hillegass EA, Dudley CA (1999) Surface electrical stimulation of skeletal muscle after spinal cord injury. Spinal Cord 37:251–257PubMedGoogle Scholar
  89. 89.
    Scremin AM, Kurta L, Gentili A, Wiseman B, Perell K, Krunkel C, Scremin OU (1999) Increasing muscle mass in spinal cord injured persons with a functional electrical stimulation exercise programme. Arch Phys Med Rehabil 80:1531–1536PubMedGoogle Scholar
  90. 90.
    Arcidsson I, Arcidsson H, Eriksson E, Jansson E (1986) Prevention of quadriceps wasting after immobilization: an evaluation of the effect of electrical stimulation. Orthopedics 9:1519–1528Google Scholar
  91. 91.
    Gibson JN, Morrison WL, Scrimgeour CM, Smith K, Stoward PJ, Rennie MJ (1989) Effects of therapeutic percutaneous electrical stimulation of atrophic human quadriceps on muscle composition, protein synthesis and contractile properties. Eur J Clin Invest 19:206–212PubMedGoogle Scholar
  92. 92.
    Vinge O, Edvardsen L, Jensen F, Jensen FG, Wernerman J, Kehlet H (1996) Effect of transcutaneous electrical muscle stimulation on postoperative muscle mass and protein synthesis. Br J Surg 83:360–363PubMedGoogle Scholar
  93. 93.
    Lewek M, Stevens J, Snyder-Mackler L (2001) The use of electrical stimulation to increase quadriceps femoris muscle force in an elderly patient following a total knee arthroplasty. Phys Ther 81:1565–1571PubMedGoogle Scholar
  94. 94.
    Maillefert JF, Eicher JC, Walker P, Dulieu V, Rouhier-Marcer I, Branly F, Cohen M, Brunotte F, Wolf JE, Casillas JM, Didier JP (1998) Effects of low-frequency electrical stimulation of quadriceps and calf muscles in patients with chronic heart failure. J Cardiopulm Rehabil 18:277–282PubMedGoogle Scholar
  95. 95.
    Vaquero AF, Chicharro JL, Gil L, Ruiz MP, Sánchez V, Lucía A, Urrea S, Gómez MA (1998) Effects of muscle electrical stimulation on peak VO2 in cardiac transplant patients. Int J Sports Med 19:317–322PubMedGoogle Scholar
  96. 96.
    Quittan M, Sochor A, Wiesinger G, Kollmitzer J, Sturm B, Pacher R, Mayr W (1999) Strength improvement of knee extensor muscles in patients with chronic heart failure by neuromuscular electrical stimulation. Artif Organs 23(5):432–435PubMedGoogle Scholar
  97. 97.
    Quittan M, Wiesinger GF, Sturm B, Puiq S, Mayr W, Sochor A, Paternostro T, Resch KL, Pacher R, Fialka-Moser V (2001) Improvement of thigh muscles by neuromuscular electrical stimulation in patients with refractory heart failure. Am J Phys Med Rehabil 80:206–214PubMedGoogle Scholar
  98. 98.
    Harris S, LeMaitre JP, Machenzie G, Fox KA, Denvir MA (2003) A randomized study of home-based electrical stimulation of the legs and conventional bicycle exercise for patients with chronic heart failure. Eur Heart J 24:871–878PubMedGoogle Scholar
  99. 99.
    Nuhr MJ, Pette D, Berger R, Quittan M, Crevenna R, Huelsman M, Wiesinger GF, Moser P, Fialka-Moser V, Pacher R (2004) Beneficial effects of chronic low-frequency stimulation of thigh muscles in patients with advanced chronic heart failure. Eur Heart J 25:136–143PubMedGoogle Scholar
  100. 100.
    Deley G, Kervio G, Verges B, Hannequin A, Petitdant MF, Salmi-Belmihoub S, Grassi B, Casillas JM (2005) Comparison of low-frequency electrical myostimulation and conventional aerobic exercise training in patients with chronic heart failure. Eur J Cardiovasc Prev Rehabil 12:226–233PubMedGoogle Scholar
  101. 101.
    Dobsák P, Nováková M, Siegelová J, Fiser B, Vítovec J, Naqasaka M, Kohzuki M, Yambe T, Nitta S, Eicher JC, Wolf JE, Imachi K (2006) Low-frequency electrical stimulation increases muscle strength and improves blood supply in patients with chronic heart failure. Circ J 70:75–82PubMedGoogle Scholar
  102. 102.
    Dobsák P, Nováková M, Fiser B, Siegelová J, Balcárková P, Spinarová L, Vítovec J, Minami N, Naqasaka M, Kohzuki M, Yambe T, Imachi K, Nitta S, Eicher JC, Wolf JE (2005) Electrical stimulation of skeletal muscles. An alternative to aerobic exercise training in patients with chronic heart failure. Int Heart J 47(3):441–453Google Scholar
  103. 103.
    Karavidas AI, Raisakis KG, Parissis JT, Tsekoura DK, Adamopoulos S, Korres DA, Farmakis D, Zacharoulis A, Fotiadis I, Matsakas E, Zacharoulis A (2006) Functional electrical stimulation improves endothelial function and reduces peripheral immune responses in patients with chronic heart failure. Eur J Cardiovasc Prev Rehabil 13:592–597PubMedGoogle Scholar
  104. 104.
    Karavidas A, Parissis J, Arapi S, Farmakis D, Korres D, Nikolaou M, Fotiadis J, Potamitis N, Driva X, Paraskevaidis I, Matsakas E, Filippatos G, Kremastinos DT (2008) Effects of functional electrical stimulation on quality of life and emotional stress in patients with chronic heart failure secondary to ischemic or idiopathic dilated cardiomyopathy: a randomized, placebo-controlled trial. Eur J Heart Failure 10(7):709–713Google Scholar
  105. 105.
    Banerjee P, Caulfield B, Crowe L, Clark A (2009) Prolonged electrical muscle stimulation exercise improves strength, peak VO2 and exercise capacity in patients with stable chronic heart failure. J Card Fail 15(4):319–326PubMedGoogle Scholar
  106. 106.
    Karavidas A, Parissis J, Matzaraki V, Arapi S, Varounis C, Ikonomidis I, Grillias P, Paraskevaidis I, Pyrgakis V, Filippatos G, Kremastinos D (2010) Functional electrical stimulation is more effective in severe symptomatic heart failure patients and improves their adherence to rehabilitation programs. J Card Fail 16:244–249PubMedGoogle Scholar
  107. 107.
    Wiesinger GF, Crevenna R, Nuhr MJ, Huelsmann M, Fialka-Moser V, Quittan M (2001) Neuromuscular electric stimulation in heart transplantation candidates with cardiac pacemakers. Arch Phys Med Rehabill 82(10):1476–1477Google Scholar
  108. 108.
    Crevenna R, Mayr W, Keilani M, Pleiner J, Nuhr M, Quittan M, Pacher R, Fialka-Moser V, Woltz M (2003) Safety of a combined strength and endurance training using neuromuscular electrical stimulation of thigh muscles in patients with heart failure and bipolar sensing cardiac pacemakers. Wien Klin Wochenschr 115(19–20):710–714PubMedGoogle Scholar
  109. 109.
    Crevenna R, Wolzt M, Fialka-Moser V, Keilani M, Nuhr M, Paternostra-Sluga T, Pacher R, Mayr W, Quittan M (2004) Long-term transcutaneous neuromuscular electrical stimulation in patients with bipolar sensing implantable cardioverter defibrillators: a pilot safety study. Artif Organs 28(1):99–102PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.G. Gennimatas’ General Hospital of AthensAthensGreece
  2. 2.Second Cardiology DepartmentOnassis Cardiac Surgery CenterAthensGreece

Personalised recommendations