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European Journal of Applied Physiology

, Volume 96, Issue 4, pp 370–378 | Cite as

Blood flow does not limit skeletal muscle force production during incremental isometric contractions

  • D. M. Wigmore
  • K. Propert
  • J. A. Kent-BraunEmail author
Article

Abstract

It has been suggested that a transient limitation in blood flow during intermittent muscular contractions can contribute to muscle fatigue, and that this limitation is greater as contraction intensity increases. We investigated skeletal muscle blood flow and fatigue in 13 healthy, untrained men (21–27 years) during 16 min of intermittent (4 s contract, 6 s relax) isometric dorsiflexor contractions. Contractions began at 10% of pre-exercise maximal voluntary contraction (MVC) force and increased by 10% every 2 min. Hyperemia (i.e., post-contraction blood flow, measured by venous occlusion plethysmography) and MVC were measured at the end of each stage. Muscle volume measures were obtained using magnetic resonance imaging. After 10 min of exercise, submaximal force and post-contraction hyperemia plateaued. MVC fell from 8 min of exercise onwards (p=0.004), and this onset of fatigue preceded the plateau in submaximal force and hyperemia. Despite a large range in dorsiflexor muscle size (66.3–176.4 cm3) and strength (112.5–421.8 N), neither muscle size nor strength were related to fatigue. The temporal dissociation between changes in blood flow and the onset of fatigue (fall of MVC) suggest that limited blood flow was not a factor in the impaired force production observed during intermittent isometric dorsiflexor contractions in healthy young men. Additionally, post-contraction hyperemia increased linearly with increasing contraction intensity, reflecting a match between blood flow and force production throughout the protocol that was independent of fatigue.

Keywords

Muscle fatigue Venous occlusion plethysmography Oxygenation Dorsiflexor muscles 

Notes

Acknowledgments

We thank Dr. Graham Caldwell for the muscle size analysis program, Dr. Todd Constable for use of the MRI facilities, Anita Christie for the blood flow analysis programs, Dr. Patty Freedson for use of the accelerometers, Linda Chung, Amy Kearns, and Karen Martin for assistance with data collection, and all of the subjects for their participation in this study. This work was supported by the National Institute on Aging Grant R01AG-21094.

References

  1. Andersen P, Saltin B (1985) Maximal perfusion of skeletal muscle in man. J Physiol 366:233–249PubMedGoogle Scholar
  2. Authier B, Rossi A, Albrand JP, Decorps M, Reutenauer H (1987) Effects of acute arterial-occlusion on muscle energy-metabolism—experimental-model using phosphorus MR spectroscopy in the rat. J Mal Vasc 12:323–328PubMedGoogle Scholar
  3. Barnes W (1980) The relationship between maximum isometric strength and intramuscular circulatory occlusion. Ergonomics 23:351–357PubMedCrossRefGoogle Scholar
  4. Degens H, Salmons S, Jarvis JC (1998) Intramuscular pressure, force and blood flow in rabbit tibialis anterior muscles during single and repetitive contractions. Eur J Appl Physiol Occup Physiol 78:13–19PubMedCrossRefGoogle Scholar
  5. Ditor DS, Hicks AL (2000) The effect of age and gender on the relative fatigability of the human adductor pollicis muscle. Can J Physiol Pharmacol 78:781–790PubMedCrossRefGoogle Scholar
  6. Dyke CK, Proctor DN, Dietz NM, Joyner MJ (1995) Role of nitric oxide in exercise hyperaemia during prolonged rhythmic handgripping in humans. J Physiol 488:259–265PubMedGoogle Scholar
  7. Fitts RH (1994) Cellular mechanisms of muscle fatigue. Physiol Rev 74:49–94PubMedGoogle Scholar
  8. Fitzpatrick R, Taylor JL, McCloskey DI (1996) Effects of arterial perfusion pressure on force production in working human hand muscles. J Physiol 495:885–891PubMedGoogle Scholar
  9. Fulco CS, Rock PB, Muza SR, Lammi E, Cymerman A, Butterfield G, Moore LG, Braun B, Lewis SF (1999) Slower fatigue and faster recovery of the adductor pollicis muscle in women matched for strength with men. Acta Physiol Scand 167:233–239PubMedCrossRefGoogle Scholar
  10. Hicks AL, Kent-Braun J, Ditor DS (2001) Sex differences in human skeletal muscle fatigue. Exerc Sport Sci Rev 29:109–112PubMedCrossRefGoogle Scholar
  11. Hoelting BD, Scheuermann BW, Barstow TJ (2001) Effect of contraction frequency on leg blood flow during knee extension exercise in humans. J Appl Physiol 91:671–679PubMedGoogle Scholar
  12. Hokanson DE, Sumner DS, Strandness DE, Jr. (1975) An electrically calibrated plethysmograph for direct measurement of limb blood flow. IEEE Trans Biomed Eng 22:25–29PubMedCrossRefGoogle Scholar
  13. Humphreys PW, Lind AR (1963) The blood flow through active and inactive muscles of the forearm during sustained hand-grip contractions. J Physiol 166:120–135PubMedGoogle Scholar
  14. Hunter SK, Enoka RM (2001) Sex differences in the fatigability of arm muscles depends on absolute force during isometric contractions. J Appl Physiol 91:2686–2694PubMedGoogle Scholar
  15. Jacobs TL, Segal SS (2000) Attenuation of vasodilatation with skeletal muscle fatigue in hamster retractor. J Physiol 524:929–941PubMedCrossRefGoogle Scholar
  16. Jasperse JL, Seals DR, Callister R (1994) Active forearm blood flow adjustments to handgrip exercise in young and older healthy men. J Physiol 474:353–360PubMedGoogle Scholar
  17. Joyner MJ, Dietz NM (1997) Nitric oxide and vasodilation in human limbs. J Appl Physiol 83:1785–1796PubMedGoogle Scholar
  18. Joyner MJ, Dietz NM, Shepherd JT (2001) From Belfast to Mayo and beyond: the use and future of plethysmography to study blood flow in human limbs. J Appl Physiol 91:2431–2441PubMedGoogle Scholar
  19. Kent-Braun JA (1999) Central and peripheral contributions to muscle fatigue in humans during sustained maximal effort. Eur J Appl Physiol Occup Physiol 80:57–63PubMedCrossRefGoogle Scholar
  20. Kent-Braun JA, Le Blanc R (1996) Quantitation of central activation failure during maximal voluntary contractions in humans. Muscle Nerve 19:861–869PubMedCrossRefGoogle Scholar
  21. Kent-Braun JA, Miller RG, Weiner MW (1993) Phases of metabolism during progressive exercise to fatigue in human skeletal muscle. J Appl Physiol 75:573–580PubMedGoogle Scholar
  22. Kent-Braun JA, Ng AV, Doyle JW, Towse TF (2002) Human skeletal muscle responses vary with age and gender during fatigue due to incremental isometric exercise. J Appl Physiol 93:1813–1823PubMedGoogle Scholar
  23. Lind AR, Williams CA (1979) The control of blood flow through human forearm muscles following brief isometric contractions. J Physiol 288:529–549PubMedGoogle Scholar
  24. McDermott MM, Greenland P, Liu K, Guralnik JM, Criqui MH, Dolan NC, Chan C, Celic L, Pearce WH, Schneider JR, Sharma L, Clark E, Gibson D, Martin GJ (2001) Leg symptoms in peripheral arterial disease: associated clinical characteristics and functional impairment. JAMA 286:1599–1606PubMedCrossRefGoogle Scholar
  25. Nosek TM, Fender KY, Godt RE (1987) It is diprotonated inorganic-phosphate that depresses force in skinned skeletal-muscle fibers. Science 236:191–193PubMedCrossRefGoogle Scholar
  26. Pitcher JB, Miles TS (1997) Influence of muscle blood flow on fatigue during intermittent human hand-grip exercise and recovery. Clin Exp Pharmacol Physiol 24:471–476PubMedCrossRefGoogle Scholar
  27. Proctor DN, Shen PH, Dietz NM, Eickhoff TJ, Lawler LA, Ebersold EJ, Loeffler DL, Joyner MJ (1998) Reduced leg blood flow during dynamic exercise in older endurance-trained men. J Appl Physiol 85:68–75PubMedGoogle Scholar
  28. Radegran G, Saltin B (1998) Muscle blood flow at onset of dynamic exercise in humans. Am J Physiol 43:H314–H322Google Scholar
  29. Robergs RA, Icenogle MV, Hudson TL, Greene ER (1997) Temporal inhomogeneity in brachial artery blood flow during forearm exercise. Med Sci Sports Exerc 29:1021–1027PubMedGoogle Scholar
  30. Russ DW, Kent-Braun JA (2003) Sex differences in human skeletal muscle fatigue are eliminated under ischemic conditions. J Appl Physiol 94:2414–2422PubMedGoogle Scholar
  31. Segal SS, Duling BR (1986) Communication between feed arteries and microvessels in hamster striated muscle: segmental vascular responses are functionally coordinated. Circ Res 59:283–290PubMedGoogle Scholar
  32. Sjogaard G, Kiens B, Jorgensen K, Saltin B (1986) Intramuscular pressure, EMG and blood flow during low-level prolonged static contraction in man. Acta Physiol Scand 128:475–484PubMedCrossRefGoogle Scholar
  33. Sjogaard G, Savard G, Juel C (1988) Muscle blood flow during isometric activity and its relation to muscle fatigue. Eur J Appl Physiol Occup Physiol 57:327–335PubMedCrossRefGoogle Scholar
  34. Stienen GJ, Papp Z, Zaremba R (1999) Influence of inorganic phosphate and pH on sarcoplasmic reticular ATPase in skinned muscle fibres of Xenopus laevis. J Physiol 518:735–744PubMedCrossRefGoogle Scholar
  35. Tachi M, Kouzaki M, Kanehisa H, Fukunaga T (2004) The influence of circulatory difference on muscle oxygenation and fatigue during intermittent static dorsiflexion. Eur J Appl Physiol Occup Physiol 91:682–688CrossRefGoogle Scholar
  36. Wascher TC, Bammer R, Stollberger R, Bahadori B, Wallner S, Toplak H (1998) Forearm composition contributes to differences in reactive hyperaemia between healthy men and women. Eur J Clin Invest 28:243–248PubMedCrossRefGoogle Scholar
  37. Welsh DG, Segal SS (1997) Coactivation of resistance vessels and muscle fibers with acetylcholine release from motor nerves. Am J Physiol 273:H156–H163PubMedGoogle Scholar
  38. Westerblad H, Allen DG (2002) Recent advances in the understanding of skeletal muscle fatigue. Curr Opin Rheumatol 14:648–652PubMedCrossRefGoogle Scholar
  39. Wigmore DM, Damon BM, Pober DM, Kent-Braun JA (2004) MRI measures of perfusion-related changes in human skeletal muscle during progressive contractions. J Appl Physiol 97:2385–2394PubMedCrossRefGoogle Scholar
  40. Wilkinson IB, Webb DJ (2001) Venous occlusion plethysmography in cardiovascular research: methodology and clinical applications. Br J Clin Pharmacol 52:631–646PubMedCrossRefGoogle Scholar
  41. Wright JR, McCloskey DI, Fitzpatrick RC (1999) Effects of muscle perfusion pressure on fatigue and systemic arterial pressure in human subjects. J Appl Physiol 86:845–851PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Department of Exercise ScienceUniversity of MassachusettsAmherstUSA

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