Effects of stimulation frequency and pulse duration on fatigue and metabolic cost during a single bout of neuromuscular electrical stimulation

Muscle and Nerve

Volumn 41, Issue 5, 2010, Pages 667-678

  Gondin, Julien ^a   Giannesini, Benoît ^a   Vilmen, Christophe ^a   Dalmasso, Christiane ^a   Le Fur, Yann ^a   Cozzone, Patrick J ^a   Bendahan, David ^a  

^a University of Aix Marseille   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL TISSUE; ARTICLE; ENERGY METABOLISM; EVOKED RESPONSE; GASTROCNEMIUS MUSCLE; IN VITRO STUDY; IN VIVO STUDY; MALE; MUSCLE CONTRACTION; MUSCLE FATIGUE; NEUROMUSCULAR ELECTRICAL STIMULATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PULSE RATE; RAT;

ADENOSINE TRIPHOSPHATE; ANIMALS; ELECTRIC STIMULATION; ELECTRIC STIMULATION THERAPY; ENERGY METABOLISM; EXERCISE TOLERANCE; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MOTOR NEURONS; MUSCLE CONTRACTION; MUSCLE FATIGUE; MUSCLE FIBERS, SKELETAL; MUSCLE WEAKNESS; MUSCLE, SKELETAL; NEUROMUSCULAR JUNCTION; PERIPHERAL NERVES; RATS; RATS, WISTAR; TIME FACTORS;

EID: 77951266805     PISSN: 0148639X     EISSN: 10974598     Source Type: Journal    
DOI: 10.1002/mus.21572     Document Type: Article

References (52)

1. Hainaut K, Duchateau J. Neuromuscular electrical stimulation and voluntary exercise. Sports Med 1992;14:100-113.
2. Snyder-Mackler L, Delitto A, Bailey SL, Stralka SW. Strength of the quadriceps femoris muscle and functional recovery after reconstruction of the anterior cruciate ligament. A prospective, randomized clinical trial of electrical stimulation. J Bone Joint Surg Am 1995;77:1166-1173.
3. Suetta C, Aagaard P, Rosted A, Jakobsen AK, Duus B, Kjaer M, et al. Training-induced changes in muscle CSA, muscle strength, EMG, and rate of force development in elderly subjects after long-term unilateral disuse. J Appl Physiol 2004;97:1954-1961. (Pubitemid 39426016)
4. Nuhr MJ, Pette D, Berger R, Quittan M, Crevenna R, Huelsman M, et al. Beneficial effects of chronic low-frequency stimulation of thigh muscles in patients with advanced chronic heart failure. Eur Heart J 2004;25:136-143. (Pubitemid 38112152)
5. Vivodtzev I, Pepin JL, Vottero G, Mayer V, Porsin B, Levy P, et al. Improvement in quadriceps strength and dyspnea in daily tasks after 1 month of electrical stimulation in severely deconditioned and malnourished COPD. Chest 2006;129:1540-1548. (Pubitemid 43894983)
6. Vanderthommen M, Duteil S, Wary C, Raynaud JS, Leroy-Willig A, Crielaard JM, et al. A comparison of voluntary and electrically induced contractions by interleaved 1H- and 31P-NMRS in humans. J Appl Physiol 2003;94:1012-1024. (Pubitemid 36232017)
7. Gandevia SC. Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 2001;81:1725-1789. (Pubitemid 32951808)
8. Lake DA. Neuromuscular electrical stimulation. An overview and its application in the treatment of sports injuries. Sports Med 1992;13:320-336.
9. Binder-Macleod SA, Halden EE, Jungles KA. Effects of stimulation intensity on the physiological responses of human motor units. Med Sci Sports Exerc 1995;27:556-565.
10. Lieber RL, Kelly MJ. Torque history of electrically stimulated human quadriceps: implications for stimulation therapy. J Orthop Res 1993;11:131-141.
11. Bigland-Ritchie B, Jones DA, Woods JJ. Excitation frequency and muscle fatigue: electrical responses during human voluntary and stimulated contractions. Exp Neurol 1979;64:414-427. (Pubitemid 9182888)
12. Jones DA, Bigland-Ritchie B, Edwards RH. Excitation frequency and muscle fatigue: mechanical responses during voluntary and stimulated contractions. Exp Neurol 1979;64:401-413. (Pubitemid 9182887)
13. Bergstrom M, Hultman E. Energy cost and fatigue during intermittent electrical stimulation of human skeletal muscle. J Appl Physiol 1988;65:1500-1505.
14. Russ DW, Elliott MA, Vandenborne K, Walter GA, Binder-Macleod SA. Metabolic costs of isometric force generation and maintenance of human skeletal muscle. Am J Physiol Endocrinol Metab 2002;282:E448-E457. (Pubitemid 34654816)
15. Russ DW, Vandenborne K, Walter GA, Elliott M, Binder-Macleod SA. Effects of muscle activation on fatigue and metabolism in human skeletal muscle. J Appl Physiol 2002;92:1978-1986. (Pubitemid 34666425)
16. Adams GR, Harris RT, Woodard D, Dudley GA. Mapping of electrical muscle stimulation using MRI. J Appl Physiol 1993;74:532-537. (Pubitemid 23078140)
17. Gorgey AS, Dudley GA. The role of pulse duration and stimulation duration in maximizing the normalized torque during neuromuscular electrical stimulation. J Orthop Sports Phys Ther 2008;38:508-516.
18. Matheson GO, McKenzie DC, Gheorghiu D, Ellinger DC, Quinney HA, Allen PS. 31P NMR of electrically stimulated rectus femoris muscle: an in vivo graded exercise model. Magn Reson Med 1992;26:60-70.
19. Kesar T, Binder-Macleod S. Effect of frequency and pulse duration on human muscle fatigue during repetitive electrical stimulation. Exp Physiol 2006;91:967-976. (Pubitemid 44690808)
20. Gregory CM, Dixon W, Bickel CS. Impact of varying pulse frequency and duration on muscle torque production and fatigue. Muscle Nerve 2007;35:504-509. (Pubitemid 46542971)
21. Binder-Macleod SA, Russ DW. Effects of activation frequency and force on low-frequency fatigue in human skeletal muscle. J Appl Physiol 1999;86:1337-1346. (Pubitemid 29172169)
22. Russ DW, Vandenborne K, Binder-Macleod SA. Factors in fatigue during intermittent electrical stimulation of human skeletal muscle. J Appl Physiol 2002;93:469-478. (Pubitemid 34810206)
23. Giannesini B, Izquierdo M, Le Fur Y, Cozzone PJ, Fingerle J, Himber J, et al. New experimental setup for studying strictly noninvasively skeletal muscle function in rat using 1H-magnetic resonance (MR) imaging and 31P-MR spectroscopy. Magn Reson Med 2005;54:1058-1064. (Pubitemid 41567182)
24. Hultman E, Sjoholm H, Jaderholm-Ek I, Krynicki J. Evaluation of methods for electrical stimulation of human skeletal muscle in situ. Pflugers Arch 1983;398:139-141. (Pubitemid 13035119)
25. Gondin J, Guette M, Ballay Y, Martin A. Electromyostimulation training effects on neural drive and muscle architecture. Med Sci Sports Exerc 2005;37:1291-1299. (Pubitemid 41209282)
26. Giannesini B, Izquierdo M, Dalmasso C, Le Fur Y, Cozzone PJ, Verleye M, et al. Endotoxemia causes a paradoxical intracellular pH recovery in exercising rat skeletal muscle. Muscle Nerve 2007;36:505-514. (Pubitemid 47512076)
27. Moon RB, Richards JH. Determination of intracellular pH by 31P magnetic resonance. J Biol Chem1973;248:7276-7278.
28. Kemp GJ, Radda GK. Quantitative interpretation of bioenergetic data from 31P and 1H magnetic resonance spectroscopic studies of skeletal muscle: an analytical review. Magn Reson Q 1994;10:43-63.
29. Armstrong RB, Phelps RO. Muscle fiber type composition of the rat hindlimb. Am J Anat 1984;171:259-272. (Pubitemid 15189959)
30. Prior BM, Ploutz-Snyder LL, Cooper TG, Meyer RA. Fiber type and metabolic dependence of T2 increases in stimulated rat muscles. J Appl Physiol 2001;90:615-623.
31. Binder-Macleod SA, Snyder-Mackler L. Muscle fatigue: clinical implications for fatigue assessment and neuromuscular electrical stimulation. Phys Ther 1993;73:902-910.
32. Willems ME, Stauber WT. The effect of number of lengthening contractions on rat isometric force production at different frequencies of nerve stimulation. Acta Physiol (Oxf) 2009;196:351-356.
33. Allen DG, Lamb GD, Westerblad H. Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 2008;88:287-332.
34. Bruton JD, Place N, Yamada T, Silva JP, Andrade FH, Dahlstedt AJ, et al. Reactive oxygen species and fatigue-induced prolonged low-frequency force depression in skeletal muscle fibres of rats, mice and SOD2 overexpressing mice. J Physiol 2008;586:175-184.
35. Westerblad H, Bruton JD, Allen DG, Lannergren J. Functional significance of Ca2+ in long-lasting fatigue of skeletal muscle. Eur J Appl Physiol 2000;83:166-174.
36. Darques JL, Bendahan D, Roussel M, Giannesini B, Tagliarini F, Le Fur Y, et al. Combined in situ analysis of metabolic and myoelectrical changes associated with electrically induced fatigue. J Appl Physiol 2003;95:1476-1484.
37. Matsunaga T, Shimada Y, Sato K. Muscle fatigue from intermittent stimulation with low and high frequency electrical pulses. Arch Phys Med Rehabil 1999;80:48-53.
38. Le Rumeur E, Le Moyec L, de Certaines JD. Rat gastrocnemius high and low frequency fatigue without metabolic impairment by 31P NMR. Arch Int Physiol Biochim Biophys 1993;101:371-376.
39. Takata S, Ikata T. Differences in energy metabolism and neuromuscular transmission between 30-Hz and 100-Hz stimulation in rat skeletal muscle. Arch Phys Med Rehabil 2001;82:666-670.
40. Hogan MC, Ingham E, Kurdak SS. Contraction duration affects metabolic energy cost and fatigue in skeletal muscle. Am J Physiol 1998;274:E397-E402.
41. Boska M. ATP production rates as a function of force level in the human gastrocnemius/soleus using 31P MRS. Magn Reson Med 1994;32:1-10.
42. Giannesini B, Izquierdo M, Le Fur Y, Cozzone PJ, Bendahan D. In vivo reduction in ATP cost of contraction is not related to fatigue level in stimulated rat gastrocnemius muscle. J Physiol 2001;536:905-915.
43. Stienen GJ, Zaremba R, Elzinga G. ATP utilization for calcium uptake and force production in skinned muscle fibres of Xenopus laevis. J Physiol 1995;482(Pt 1):109-122.
44. Badier M, Guillot C, Danger C, Tagliarini F, Jammes Y. M-wave changes after high- and low-frequency electrically induced fatigue in different muscles. Muscle Nerve 1999;22:488-496.
45. Boerio D, Jubeau M, Zory R, Maffiuletti NA. Central and peripheral fatigue after electrostimulation-induced resistance exercise. Med Sci Sports Exerc 2005;37:973-978. (Pubitemid 40847459)
46. Allon G, Allin J, Inbar GJ. Optimization of pulse duration and pulse charge during transcutaneous electrical nerve stimulation. Aust J Physiother 1983;29:195-201.
47. Notermans SL. Measurement of the pain threshold determined by electrical stimulation and its clinical application. I. Method and factors possibly influencing the pain threshold. Neurology 1966;16:1071-1086.
48. Thompson CH, Kemp GJ, Sanderson AL, Radda GK. Skeletal muscle mitochondrial function studied by kinetic analysis of postexercise phosphocreatine resynthesis. J Appl Physiol 1995;78:2131-2139.
49. Roth K, Weiner MW. Determination of cytosolic ADP and AMP concentrations and the free energy of ATP hydrolysis in human muscle and brain tissues with 31P NMR spectroscopy. Magn Reson Med 1991;22:505-511.
50. Hochachka PW, Mommsen TP. Protons and anaerobiosis. Science 1983;219:1391-1397.
51. Wolfe CL, Gilbert HF, Brindle KM, Radda GK. Determination of buffering capacity of rat myocardium during ischemia. Biochim Biophys Acta 1988;971:9-20.
52. Adams GR, Foley JM, Meyer RA. Muscle buffer capacity estimated from pH changes during rest-to-work transitions. J Appl Physiol 1990;69:968-972.