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Potassium kinetics in human muscle interstitium during repeated intense exercise in relation to fatigue

  • Skeletal Muscle
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Abstract

Accumulation of K+ in skeletal muscle interstitium during intense exercise has been suggested to cause fatigue in humans. The present study examined interstitial K+ kinetics and fatigue during repeated, intense, exhaustive exercise in human skeletal muscle. Ten subjects performed three repeated, intense (61.6±4.1 W; mean±SEM), one-legged knee extension exercise bouts (EX1, EX2 and EX3) to exhaustion separated by 10-min recovery periods. Interstitial [K+] ([K+]interst) in the vastus lateralis muscle were determined using microdialysis. Time-to-fatigue decreased progressively (P<0.05) during the protocol (5.1±0.4, 4.2±0.3 and 3.2±0.2 min for EX1, EX2 and EX3 respectively). Prior to these bouts, [K+]interst was 4.1±0.2, 4.8±0.2 and 5.2±0.2 mM, respectively. During the initial 1.5 min of exercise the accumulation rate of interstitial K+ was 85% greater (P<0.05) in EX1 than in EX3. At exhaustion [K+]interst was 11.4±0.8 mM in EX1, which was not different from that in EX2 (10.4±0.8 mM), but higher (P<0.05) than in EX3 (9.1±0.3 mM). The study demonstrated that the rate of accumulation of K+ in the muscle interstitium declines during intense repetitive exercise. Furthermore, whilst [K+]interst at exhaustion reached levels high enough to impair performance, the concentration decreased with repeated exercise, suggesting that accumulation of interstitial K+ per se does not cause fatigue when intense exercise is repeated.

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References

  1. Andersen P, Adams RP, Sjögaard G, Thorboe A, Saltin B (1985) Dynamic knee extension as model for study of isolated exercising muscle in humans. J Appl Physiol 59:1647–1653

    CAS  PubMed  Google Scholar 

  2. Bangsbo J, Graham T, Kiens B, Saltin B (1992) Elevated muscle glycogen and anaerobic energy production during exhaustive exercise in man. J Physiol (Lond) 451:205–227

    Google Scholar 

  3. Bangsbo J, Graham T, Johansen L, Strange S, Christensen C, Saltin B (1992) Elevated muscle acidity and energy production during exhaustive exercise in man. Am J Physiol Physiol 263:R881–R899

    Google Scholar 

  4. Bangsbo J, Madsen K, Kiens B, Richter EA (1996) Effect of muscle acidity on muscle metabolism and fatigue during intense exercise in man. J Physiol (Lond) 495:587–596

    Google Scholar 

  5. Bangsbo J, Krustrup P, Gonzáles-Alonso J, Saltin B (2001) ATP production and efficiency of human skeletal muscle during intense exercise: effect of previous exercise. Am J Physiol 208:E956–E964

    Google Scholar 

  6. Cairnes SP, Dulhunty AF (1995) High-frequency fatigue in rat skeletal muscle: role of extracellulary ion concentrations. Muscle Nerve 18:890–898

    PubMed  Google Scholar 

  7. Cairnes SP, Hing WA, Slack JR, Mills RG, Loiselle DS (1997) Different effects of raised [K+] on membrane potential and contraction in mouse fast- and slow-twich muscle. Am J Physiol 273:C598–C611

    PubMed  Google Scholar 

  8. Davies NW (1990) Modulation of ATP-sensitive K+ channels in skeletal muscle by intracellular protons. Nature 343:375–377

    Article  CAS  PubMed  Google Scholar 

  9. Davies NW, Standen NB, Stanfield PR (1991) ATP-dependent potassium channels of muscle cells: their properties, regulation and possible functions. J Bioenerg Biomembr 23:509–523

    CAS  PubMed  Google Scholar 

  10. Fitts RH (1994) Cellular mechanisms of muscle fatigue. Physiol Rev 74:49–94

    CAS  PubMed  Google Scholar 

  11. Fitts RH, Balog EM (1996) Effects of intracellular and extracellular ion changes on E-C coupling and skeletal muscle fatigue. Acta Physiol Scand 156:169–181

    CAS  PubMed  Google Scholar 

  12. Gaitanos GC, Williams C, Boobis LH, Brooks S. (1993) Human muscle metabolism during intermittent maximal exercise. J Appl Physiol 75:712–719

    Google Scholar 

  13. Hellsten Y, Richter EA, Kiens B, Bangsbo J (1999) AMP deamination and purine exchange in human skeletal muscle during and after intense exercise. J Physiol (Lond) 520:909–920

    Google Scholar 

  14. Hocherman SD, Bezanilla F (1996) A patch-clamp study of delayed rectifier currents in skeletal muscle of control and mdx mice. J Physiol (Lond) 493:113–128

    Google Scholar 

  15. Jones PR, Pearson J (1969) Antrophometric determination of leg fat and muscle plus bone volumes in young male and female adults. J Physiol (Lond) 204:63P–66P

    Google Scholar 

  16. Juel C (1988) The effect of beta 2-adrenoceptor activation on ion-shifts and fatigue in mouse soleus muscle stimulated in vitro. Acta Physiol Scand 134:209–216

    CAS  PubMed  Google Scholar 

  17. Juel C, Bangsbo J, Graham T, Saltin B (1990) Lactate and potassium fluxes from human skeletal muscle during and after intense, dynamic, knee extensor exercise. Acta Physiol Scand 140:147–159

    CAS  PubMed  Google Scholar 

  18. Juel C, Pilegaard H, Nielsen JJ, Bangsbo J (2000) Interstitial K+ in human skeletal muscle during and after dynamic graded exercise determined by microdialysis. Am J Physiol 278:R400–R406

    CAS  Google Scholar 

  19. Juel C, Nielsen JJ, Bangsbo J (2000) Exercise induced translocation of Na+,K+ pump subunits to the plasma membrane in human skeletal muscle Am J Physiol 278:R1107–R1110

    Google Scholar 

  20. Juel C, Grunnet L, Holse M, Kenworthy S, Sommer A, Wulff T (2001) Reversibility of exercise-induced translocation of Na+-K+ pump subunits to the plasma membrane in rat skeletal muscle. Pflugers Arch 443:212–217

    Article  CAS  PubMed  Google Scholar 

  21. Kristensen M, Hellsten Y, Juel C (2002) Potassium channels involved in potassium release from active skeletal muscle (abstract). FASEB J 16:609–609

    Google Scholar 

  22. Krustrup P, González-Alonso J, Quistorff B, Bangsbo J (2001) Muscle heat production and anaerobic energy turnover during repeated intense dynamic exercise in humans. J Physiol (Lond) 536:947–956

    Google Scholar 

  23. Lowry OH, Passonneau JV (1972) A flexible system of enzymatic analysis. Academic Press, New York

  24. Medbø JI, Sejersted OM (1990) Plasma potassium changes with high intensity exercise. J Physiol (Lond) 421:105–122

    Google Scholar 

  25. Nielsen JJ, Kristensen M, Hellsten Y, Bangsbo J, Juel C (2003) Localization and function of ATP-sensitive potassium channels in human skeletal muscle. Am J Physiol 284:R558–R563

    CAS  Google Scholar 

  26. Nordsborg N, Mohr M, Danneman LD, Nielsen JJ, Langberg H, Bangsbo J (2003) Muscle interstitial potassium kinetics during intense exhaustive exercise—effect of previous arm exercise. Am J Physiol 285:R143–R148

    CAS  Google Scholar 

  27. Radegran G, Pilegaard H, Nielsen JJ, Bangsbo, J (1998) Microdialyse ethanol removal reflects probe recovery rather than local blood flow in skeletal muscle. J Appl Physiol 85:751–757

    CAS  PubMed  Google Scholar 

  28. Ruff RL, Simoncini L, Stuhmer W (1988) Slow sodium channel inactivation in mammalian muscle: a possible role in regulating excitability. Muscle Nerve 11:502–510

    CAS  PubMed  Google Scholar 

  29. Sejersted OM, Sjögaard G (2000) Dynamics and consequences of potassium shifts in skeletal muscle and heart during exercise. Physiol Rev 80:1411–1481

    CAS  PubMed  Google Scholar 

  30. Sjögaard G (1983) Electrolytes in slow and fast muscle fibers of humans at rest and with dynamic exercise. Am J Physiol 245:R25–R31

    CAS  Google Scholar 

  31. Sjögaard G, Adams P, Saltin B (1985) Water and ion shifts in skeletal muscle of humans with intense dynamic knee extensions. Am J Physiol 248:R190–R196

    PubMed  Google Scholar 

  32. Spriet LL, Lindinger MI, McKelvie RS, Heigenhauser GJ, Jones NL (1989) Muscle glycogenolysis and H+ concentration during maximal intermittent cycling. J Appl Physiol 66:8–13

    Google Scholar 

  33. Spruce AE, Standen NB, Standfield PR (1985) Voltage-dependent ATP-sensitive potassium channels of skeletal muscle membrane. Nature 316:736–738

    CAS  PubMed  Google Scholar 

  34. Sréter FA (1963) Cell water, sodium and potassium in stimulated red and white mammalian muscle. Am J Physiol 205:1295–1298

    PubMed  Google Scholar 

  35. Standen NB, Pettit AI, Davies NW, Stanfield PR (1992) Activation of ATP-dependent K+ currents in intact skeletal muscle fibres by reduced intracellular pH. Proc R Soc Lond B Biol Sci 247:195–198

    CAS  PubMed  Google Scholar 

  36. Vøllestad NK, Hallen J, Sejersted OM (1994) Effect of exercise intensity on potassium balance in muscle and blood of man. J Physiol (Lond) 475:359–368

    Google Scholar 

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Acknowledgements

The excellent technical assistant of Ingelise Kring, Merete Vannby and Winnie Taagerup is greatly appreciated. The study was supported by a grant from The Danish National Research Foundation (504-14). In addition support was obtained from The Sports Reasearch Council (Idraettens Forskningsråd) and Team Denmark.

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Correspondence to Jens Bangsbo.

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Mohr, M., Nordsborg, N., Nielsen, J.J. et al. Potassium kinetics in human muscle interstitium during repeated intense exercise in relation to fatigue. Pflugers Arch - Eur J Physiol 448, 452–456 (2004). https://doi.org/10.1007/s00424-004-1257-6

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  • DOI: https://doi.org/10.1007/s00424-004-1257-6

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