European Journal of Applied Physiology

, Volume 114, Issue 8, pp 1619–1633 | Cite as

Locomotor and diaphragm muscle fatigue in endurance athletes performing time-trials of different durations

  • Thomas U. Wüthrich
  • Elisabeth C. Eberle
  • Christina M. SpenglerEmail author
Original Article



Fatigue in leg muscles might differ between running and cycling due to inherent differences in muscle activation patterns. Moreover, postural demand placed upon the diaphragm during running could augment the development of diaphragm fatigue.


We investigated quadriceps and diaphragm fatigue in 11 runners and 11 cyclists (age: 29 ± 5 years; \(\dot{V}\)O2,peak: 66.9 ± 5.5 ml min−1 kg−1) by assessing quadriceps twitch force (Q tw) and transdiaphragmatic twitch pressure (P di,tw) before and after 15- and 30-min time-trials (15TT, 30TT). Inspiratory muscle fatigue was also obtained after volitional normocapnic hyperpnoea (NH) where postural demand is negligible. We hypothesized that running and cycling would induce different patterns of fatigue and that runners would develop less respiratory muscle fatigue when performing NH.


The reduction in Q tw was greater in cyclists (32 ± 6 %) compared to runners (13 ± 8 %, p < 0.01), but not different for 15TTs (23 ± 13 %) and 30TTs (21 ± 11 %, p = 0.34). Overall P di,tw was more reduced after 15TTs (24 ± 8 %) than after 30TTs (20 ± 9 %, p = 0.04) while being similar for runners and cyclists (p = 0.78). Meanwhile, breathing duration in NH and the magnitude of inspiratory muscle fatigue were also not different (both p > 0.05).


Different levels of leg muscle fatigue in runners and cyclists could in part be related to the specific muscle activation patterns including concentric contractions in both modalities but eccentric contractions in runners only. Diaphragm fatigue likely resulted from the large ventilatory load which is characteristic for both exercise modalities and which was higher in 15TTs than in 30TTs (+27 %, p < 0.01) while postural demand appears to be of less importance.


Self-paced exercise Fatigue Locomotor muscles Respiratory muscles Hyperpnoea 



Coefficient of variation


Maximal voluntary ventilation


Compound muscle action potential


Transdiaphragmatic pressure


Transdiaphragmatic twitch pressure


Esophageal pressure


Esophageal twitch pressure


Gastric pressure


Gastric twitch pressure


Mouth pressure


Mouth twitch pressure


Inspiratory transdiaphragmatic pressure–time product


Inspiratory transdiaphragmatic pressure–time product


Inspiratory esophageal pressure–time product


Expiratory esophageal pressure–time product


Expiratory gastric pressure–time product


Quadriceps twitch force


Oxygen consumption


Oxygen consumption at peak workload


Work of breathing


Reduction in transdiaphragmatic twitch pressure


Reduction in quadriceps twitch force


15 min time-trial


30 min time-trial



We thank all the subjects for their time and maximal efforts put into this study and Dr. Ruth Briggs for English editing. This research is financially supported by the Swiss Office of Sports (Grant No. 11-11).

Conflict of interest

The authors declare that no conflict of interest exists.


  1. Aaron EA, Seow KC, Johnson BD, Dempsey JA (1992) Oxygen cost of exercise hyperpnea: implications for performance. J Appl Physiol 72:1818–1825PubMedGoogle Scholar
  2. Abbiss CR, Laursen PB (2005) Models to explain fatigue during prolonged endurance cycling. Sports Med 35:865–898PubMedCrossRefGoogle Scholar
  3. Allen DG, Lamb GD, Westerblad H (2008) Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88:287–332PubMedCrossRefGoogle Scholar
  4. Amann M (2011) Central and peripheral fatigue: interaction during cycling exercise in humans. Med Sci Sports Exerc 43:2039–2045PubMedCrossRefGoogle Scholar
  5. Amann M, Dempsey JA (2008) Locomotor muscle fatigue modifies central motor drive in healthy humans and imposes a limitation to exercise performance. J Physiol 586:161–173PubMedCentralPubMedCrossRefGoogle Scholar
  6. Amann M, Secher NH (2010) Point: counterpoint: Afferent feedback from fatigued locomotor muscles is/is not an important determinant of endurance exercise performance. J Appl Physiol 108:452–454PubMedCrossRefGoogle Scholar
  7. Amann M, Eldridge MW, Lovering AT, Stickland MK, Pegelow DF, Dempsey JA (2006) Arterial oxygenation influences central motor output and exercise performance via effects on peripheral locomotor muscle fatigue in humans. J Physiol 575:937–952PubMedCentralPubMedCrossRefGoogle Scholar
  8. Amann M, Proctor LT, Sebranek JJ, Pegelow DF, Dempsey JA (2009) Opioid-mediated muscle afferents inhibit central motor drive and limit peripheral muscle fatigue development in humans. J Physiol 587:271–283PubMedCentralPubMedCrossRefGoogle Scholar
  9. ATS/ERS (2002) Statement on respiratory muscle testing. Am J Respir Crit Care Med 166:518–624Google Scholar
  10. Babcock MA, Johnson BD, Pegelow DF, Suman OE, Griffin D, Dempsey JA (1995a) Hypoxic effects on exercise-induced diaphragmatic fatigue in normal healthy humans. J Appl Physiol 78:82–92PubMedGoogle Scholar
  11. Babcock MA, Pegelow DF, McClaran SR, Suman OE, Dempsey JA (1995b) Contribution of diaphragmatic power output to exercise-induced diaphragm fatigue. J Appl Physiol 78:1710–1719PubMedGoogle Scholar
  12. Babcock MA, Pegelow DF, Johnson BD, Dempsey JA (1996) Aerobic fitness effects on exercise-induced low-frequency diaphragm fatigue. J Appl Physiol 81:2156–2164PubMedGoogle Scholar
  13. Babcock MA, Pegelow DF, Harms CA, Dempsey JA (2002) Effects of respiratory muscle unloading on exercise-induced diaphragm fatigue. J Appl Physiol 93:201–206PubMedGoogle Scholar
  14. Bentley DJ, Smith PA, Davie AJ, Zhou S (2000) Muscle activation of the knee extensors following high intensity endurance exercise in cyclists. Eur J Appl Physiol 81:297–302PubMedCrossRefGoogle Scholar
  15. Bigland-Ritchie B, Woods JJ (1984) Changes in muscle contractile properties and neural control during human muscular fatigue. Muscle Nerve 7:691–699PubMedCrossRefGoogle Scholar
  16. Bijker KE, de Groot G, Hollander AP (2002) Differences in leg muscle activity during running and cycling in humans. Eur J Appl Physiol 87:556–561PubMedCrossRefGoogle Scholar
  17. Decorte N, Lafaix PA, Millet GY, Wuyam B, Verges S (2012) Central and peripheral fatigue kinetics during exhaustive constant-load cycling. Scand J Med Sci Sports 22:381–391Google Scholar
  18. Fowles JR, Green HJ, Tupling R, O’Brien S, Roy BD (2002) Human neuromuscular fatigue is associated with altered Na+-K+-ATPase activity following isometric exercise. J Appl Physiol 92:1585–1593PubMedGoogle Scholar
  19. Gandevia SC (2001) Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81:1725–1789PubMedGoogle Scholar
  20. Girard O, Millet GP, Micallef JP, Racinais S (2012) Alteration in neuromuscular function after a 5 km running time trial. Eur J Appl Physiol 112:2323–2330PubMedCrossRefGoogle Scholar
  21. Guenette JA, Romer LM, Querido JS, Chua R, Eves ND, Road JD, McKenzie DC, Sheel AW (2010) Sex differences in exercise-induced diaphragmatic fatigue in endurance-trained athletes. J Appl Physiol 109:35–46PubMedCrossRefGoogle Scholar
  22. Hamnegard CH, Wragg S, Mills G, Kyroussis D, Road J, Daskos G, Bake B, Moxham J, Green M (1995) The effect of lung volume on transdiaphragmatic pressure. Eur Respir J 8:1532–1536PubMedGoogle Scholar
  23. Harms CA, Babcock MA, McClaran SR, Pegelow DF, Nickele GA, Nelson WB, Dempsey JA (1997) Respiratory muscle work compromises leg blood flow during maximal exercise. J Appl Physiol 82:1573–1583PubMedGoogle Scholar
  24. Henderson WR, Guenette JA, Dominelli PB, Griesdale DE, Querido JS, Boushel R, Sheel AW (2012) Limitations of respiratory muscle and vastus lateralis blood flow during continuous exercise. Respir Physiol Neurobiol 181:302–307PubMedCrossRefGoogle Scholar
  25. Henke KG, Sharratt M, Pegelow D, Dempsey JA (1988) Regulation of end-expiratory lung volume during exercise. J Appl Physiol 64:135–146PubMedGoogle Scholar
  26. Hodges PW, Gandevia SC (2000) Activation of the human diaphragm during a repetitive postural task. J Physiol 522(Pt 1):165–175PubMedCentralPubMedCrossRefGoogle Scholar
  27. Hodges PW, Heijnen I, Gandevia SC (2001) Postural activity of the diaphragm is reduced in humans when respiratory demand increases. J Physiol 537:999–1008PubMedCentralPubMedCrossRefGoogle Scholar
  28. Hodges PW, Eriksson AE, Shirley D, Gandevia SC (2005) Intra-abdominal pressure increases stiffness of the lumbar spine. J Biomech 38:1873–1880PubMedCrossRefGoogle Scholar
  29. Iguchi M, Shields RK (2010) Quadriceps low-frequency fatigue and muscle pain are contraction-type-dependent. Muscle Nerve 42:230–238PubMedCentralPubMedCrossRefGoogle Scholar
  30. Johnson BD, Babcock MA, Suman OE, Dempsey JA (1993) Exercise-induced diaphragmatic fatigue in healthy humans. J Physiol 460:385–405PubMedCentralPubMedGoogle Scholar
  31. Kufel TJ, Pineda LA, Mador MJ (2002) Comparison of potentiated and unpotentiated twitches as an index of muscle fatigue. Muscle Nerve 25:438–444PubMedCrossRefGoogle Scholar
  32. Lansing RW, Im BS, Thwing JI, Legedza AT, Banzett RB (2000) The perception of respiratory work and effort can be independent of the perception of air hunger. Am J Respir Crit Care Med 162:1690–1696PubMedCrossRefGoogle Scholar
  33. Lepers R, Maffiuletti NA, Rochette L, Brugniaux J, Millet GY (2002) Neuromuscular fatigue during a long-duration cycling exercise. J Appl Physiol 92:1487–1493PubMedGoogle Scholar
  34. Mador MJ, Magalang UJ, Rodis A, Kufel TJ (1993) Diaphragmatic fatigue after exercise in healthy human subjects. Am Rev Respir Dis 148:1571–1575PubMedCrossRefGoogle Scholar
  35. Mador M, Kufel TJ, Pineda LA (2000a) Quadriceps and diaphragmatic function after exhaustive cycle exercise in the healthy elderly. Am J Respir Crit Care Med 162:1760–1766CrossRefGoogle Scholar
  36. Mador MJ, Kufel TJ, Pineda LA, Sharma GK (2000b) Diaphragmatic fatigue and high-intensity exercise in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 161:118–123PubMedCrossRefGoogle Scholar
  37. Mador MJ, Kufel TJ, Pineda LA, Steinwald A, Aggarwal A, Upadhyay AM, Khan MA (2001) Effect of pulmonary rehabilitation on quadriceps fatiguability during exercise. Am J Respir Crit Care Med 163:930–935PubMedCrossRefGoogle Scholar
  38. Marcora SM, Bosio A, de Morree HM (2008) Locomotor muscle fatigue increases cardiorespiratory responses and reduces performance during intense cycling exercise independently from metabolic stress. Am J Physiol-Reg 294:R874–R883Google Scholar
  39. Martin V, Kerherve H, Messonnier LA, Banfi JC, Geyssant A, Bonnefoy R, Feasson L, Millet GY (2010) Central and peripheral contributions to neuromuscular fatigue induced by a 24-h treadmill run. J Appl Physiol 108:1224–1233PubMedCrossRefGoogle Scholar
  40. Miller MR, Crapo R, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, Enright P, van der Grinten CP, Gustafsson P, Jensen R, Johnson DC, MacIntyre N, McKay R, Navajas D, Pedersen OF, Pellegrino R, Viegi G, Wanger J (2005) General considerations for lung function testing. Eur Respir J 26:153–161PubMedCrossRefGoogle Scholar
  41. Millet GY, Tomazin K, Verges S, Vincent C, Bonnefoy R, Boisson RC, Gergele L, Feasson L, Martin V (2011) Neuromuscular consequences of an extreme mountain ultra-marathon. PLoS One 6:e17059PubMedCentralPubMedCrossRefGoogle Scholar
  42. Nummela AT, Heath KA, Paavolainen LM, Lambert MI, St Clair Gibson A, Rusko HK, Noakes TD (2008) Fatigue during a 5-km running time trial. Int J Sports Med 29:738–745PubMedCrossRefGoogle Scholar
  43. Polkey MI, Kyroussis D, Keilty SE, Hamnegard CH, Mills GH, Green M, Moxham J (1995) Exhaustive treadmill exercise does not reduce twitch transdiaphragmatic pressure in patients with COPD. Am J Respir Crit Care Med 152:959–964PubMedCrossRefGoogle Scholar
  44. Quanjer PH, Tammeling GJ, Cotes JE, Pedersen OF, Peslin R, Yernault JC (1993) Lung volumes and forced ventilatory flows. Report Working Party Standardization of Lung Function Tests, European Community for Steel and Coal. Official Statement of the European Respiratory Society. Eur Respir J Suppl 16:5–40PubMedCrossRefGoogle Scholar
  45. Racinais S, Girard O, Micallef JP, Perrey S (2007) Failed excitability of spinal motoneurons induced by prolonged running exercise. J Neurophysiol 97:596–603PubMedCrossRefGoogle Scholar
  46. Ross EZ, Goodall S, Stevens A, Harris I (2010) Time course of neuromuscular changes during running in well-trained subjects. Med Sci Sports Exerc 42:1184–1190PubMedGoogle Scholar
  47. Saey D, Michaud A, Couillard A, Cote CH, Mador MJ, LeBlanc P, Jobin J, Maltais F (2005) Contractile fatigue, muscle morphometry, and blood lactate in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 171:1109–1115PubMedCrossRefGoogle Scholar
  48. Sargeant AJ (2007) Structural and functional determinants of human muscle power. Exp Physiol 92:323–331PubMedCrossRefGoogle Scholar
  49. Saugy J, Place N, Millet GY, Degache F, Schena F, Millet GP (2013) Alterations of neuromuscular function after the World’s most challenging mountain Ultra-Marathon. PLoS One 8:e65596PubMedCentralPubMedCrossRefGoogle Scholar
  50. Scheer FA, Hu K, Evoniuk H, Kelly EE, Malhotra A, Hilton MF, Shea SA (2010) Impact of the human circadian system, exercise, and their interaction on cardiovascular function. Proc Natl Acad Sci USA 107:20541–20546PubMedCentralPubMedCrossRefGoogle Scholar
  51. Similowski T, Straus C, Attali V, Duguet A, Derenne JP (1998) Cervical magnetic stimulation as a method to discriminate between diaphragm and rib cage muscle fatigue. J Appl Physiol 84:1692–1700PubMedGoogle Scholar
  52. Skof B, Strojnik V (2006a) Neuro-muscular fatigue and recovery dynamics following anaerobic interval workload. Int J Sports Med 27:220–225PubMedCrossRefGoogle Scholar
  53. Skof B, Strojnik V (2006b) Neuromuscular fatigue and recovery dynamics following prolonged continuous run at anaerobic threshold. Br J Sports Med 40:219–222PubMedCentralPubMedCrossRefGoogle Scholar
  54. Smith IC, Newham DJ (2007) Fatigue and functional performance of human biceps muscle following concentric or eccentric contractions. J Appl Physiol 102:207–213PubMedCrossRefGoogle Scholar
  55. Taylor BJ, How SC, Romer LM (2006) Exercise-induced abdominal muscle fatigue in healthy humans. J Appl Physiol 100:1554–1562PubMedCrossRefGoogle Scholar
  56. Verges S, Notter D, Spengler CM (2006a) Influence of diaphragm and rib cage muscle fatigue on breathing during endurance exercise. Respir Physiol Neurobiol 154:431–442PubMedCrossRefGoogle Scholar
  57. Verges S, Schulz C, Perret C, Spengler CM (2006b) Impaired abdominal muscle contractility after high-intensity exhaustive exercise assessed by magnetic stimulation. Muscle Nerve 34:423–430PubMedCrossRefGoogle Scholar
  58. Verges S, Lenherr O, Haner AC, Schulz C, Spengler CM (2007) Increased fatigue resistance of respiratory muscles during exercise after respiratory muscle endurance training. Am J Physiol Regul Integr Comp Physiol 292:R1246–R1253PubMedCrossRefGoogle Scholar
  59. Vogiatzis I, Athanasopoulos D, Habazettl H, Kuebler WM, Wagner H, Roussos C, Wagner PD, Zakynthinos S (2009) Intercostal muscle blood flow limitation in athletes during maximal exercise. J Physiol 587:3665–3677PubMedCentralPubMedCrossRefGoogle Scholar
  60. Walker DJ, Walterspacher S, Schlager D, Ertl T, Roecker K, Windisch W, Kabitz HJ (2011) Characteristics of diaphragmatic fatigue during exhaustive exercise until task failure. Respir Physiol Neurobiol 176:14–20PubMedCrossRefGoogle Scholar
  61. Wilson SH, Cooke NT, Edwards RH, Spiro SG (1984) Predicted normal values for maximal respiratory pressures in caucasian adults and children. Thorax 39:535–538PubMedCentralPubMedCrossRefGoogle Scholar
  62. Wuthrich TU, Notter DA, Spengler CM (2013) Effect of inspiratory muscle fatigue on exercise performance taking into account the fatigue-induced excess respiratory drive. Exp Physiol 98:1705–1717PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Thomas U. Wüthrich
    • 1
  • Elisabeth C. Eberle
    • 1
  • Christina M. Spengler
    • 1
    • 2
    Email author
  1. 1.Exercise Physiology LabInstitute of Human Movement Sciences and Sport, ETH ZurichZurichSwitzerland
  2. 2.Zurich Center for Integrative Human Physiology (ZIHP), University of ZurichZurichSwitzerland

Personalised recommendations