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

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Abstract

Purpose

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.

Methods

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.

Results

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).

Conclusion

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.

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Abbreviations

CV:

Coefficient of variation

MVV:

Maximal voluntary ventilation

M-wave:

Compound muscle action potential

P di :

Transdiaphragmatic pressure

P di,tw :

Transdiaphragmatic twitch pressure

P es :

Esophageal pressure

P es,tw :

Esophageal twitch pressure

P ga :

Gastric pressure

P ga,tw :

Gastric twitch pressure

P m :

Mouth pressure

P m,tw :

Mouth twitch pressure

PTPdi,in :

Inspiratory transdiaphragmatic pressure–time product

PTPga,in :

Inspiratory transdiaphragmatic pressure–time product

PTPes,in :

Inspiratory esophageal pressure–time product

PTPes,ex :

Expiratory esophageal pressure–time product

PTPga,ex :

Expiratory gastric pressure–time product

Q tw :

Quadriceps twitch force

\(\dot{V}\)O2 :

Oxygen consumption

\(\dot{V}\)O2,peak :

Oxygen consumption at peak workload

WOB:

Work of breathing

∆P di,tw :

Reduction in transdiaphragmatic twitch pressure

∆Q tw :

Reduction in quadriceps twitch force

15TT:

15 min time-trial

30TT:

30 min time-trial

References

  • Aaron EA, Seow KC, Johnson BD, Dempsey JA (1992) Oxygen cost of exercise hyperpnea: implications for performance. J Appl Physiol 72:1818–1825

    CAS  PubMed  Google Scholar 

  • Abbiss CR, Laursen PB (2005) Models to explain fatigue during prolonged endurance cycling. Sports Med 35:865–898

    Article  PubMed  Google Scholar 

  • Allen DG, Lamb GD, Westerblad H (2008) Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88:287–332

    Article  CAS  PubMed  Google Scholar 

  • Amann M (2011) Central and peripheral fatigue: interaction during cycling exercise in humans. Med Sci Sports Exerc 43:2039–2045

    Article  PubMed  Google Scholar 

  • Amann M, Dempsey JA (2008) Locomotor muscle fatigue modifies central motor drive in healthy humans and imposes a limitation to exercise performance. J Physiol 586:161–173

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 108:452–454

    Article  PubMed  Google Scholar 

  • 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 575:937–952

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 587:271–283

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • ATS/ERS (2002) Statement on respiratory muscle testing. Am J Respir Crit Care Med 166:518–624

  • 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 78:82–92

    CAS  PubMed  Google Scholar 

  • Babcock MA, Pegelow DF, McClaran SR, Suman OE, Dempsey JA (1995b) Contribution of diaphragmatic power output to exercise-induced diaphragm fatigue. J Appl Physiol 78:1710–1719

    CAS  PubMed  Google Scholar 

  • Babcock MA, Pegelow DF, Johnson BD, Dempsey JA (1996) Aerobic fitness effects on exercise-induced low-frequency diaphragm fatigue. J Appl Physiol 81:2156–2164

    CAS  PubMed  Google Scholar 

  • Babcock MA, Pegelow DF, Harms CA, Dempsey JA (2002) Effects of respiratory muscle unloading on exercise-induced diaphragm fatigue. J Appl Physiol 93:201–206

    PubMed  Google Scholar 

  • 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 81:297–302

    Article  CAS  PubMed  Google Scholar 

  • Bigland-Ritchie B, Woods JJ (1984) Changes in muscle contractile properties and neural control during human muscular fatigue. Muscle Nerve 7:691–699

    Article  CAS  PubMed  Google Scholar 

  • Bijker KE, de Groot G, Hollander AP (2002) Differences in leg muscle activity during running and cycling in humans. Eur J Appl Physiol 87:556–561

    Article  CAS  PubMed  Google Scholar 

  • 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 22:381–391

  • 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 92:1585–1593

    CAS  PubMed  Google Scholar 

  • Gandevia SC (2001) Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81:1725–1789

    CAS  PubMed  Google Scholar 

  • Girard O, Millet GP, Micallef JP, Racinais S (2012) Alteration in neuromuscular function after a 5 km running time trial. Eur J Appl Physiol 112:2323–2330

    Article  CAS  PubMed  Google Scholar 

  • 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 109:35–46

    Article  PubMed  Google Scholar 

  • 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 8:1532–1536

    CAS  PubMed  Google Scholar 

  • 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 82:1573–1583

    CAS  PubMed  Google Scholar 

  • 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 181:302–307

    Article  PubMed  Google Scholar 

  • Henke KG, Sharratt M, Pegelow D, Dempsey JA (1988) Regulation of end-expiratory lung volume during exercise. J Appl Physiol 64:135–146

    CAS  PubMed  Google Scholar 

  • Hodges PW, Gandevia SC (2000) Activation of the human diaphragm during a repetitive postural task. J Physiol 522(Pt 1):165–175

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hodges PW, Heijnen I, Gandevia SC (2001) Postural activity of the diaphragm is reduced in humans when respiratory demand increases. J Physiol 537:999–1008

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hodges PW, Eriksson AE, Shirley D, Gandevia SC (2005) Intra-abdominal pressure increases stiffness of the lumbar spine. J Biomech 38:1873–1880

    Article  PubMed  Google Scholar 

  • Iguchi M, Shields RK (2010) Quadriceps low-frequency fatigue and muscle pain are contraction-type-dependent. Muscle Nerve 42:230–238

    Article  PubMed Central  PubMed  Google Scholar 

  • Johnson BD, Babcock MA, Suman OE, Dempsey JA (1993) Exercise-induced diaphragmatic fatigue in healthy humans. J Physiol 460:385–405

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kufel TJ, Pineda LA, Mador MJ (2002) Comparison of potentiated and unpotentiated twitches as an index of muscle fatigue. Muscle Nerve 25:438–444

    Article  PubMed  Google Scholar 

  • 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 162:1690–1696

    Article  CAS  PubMed  Google Scholar 

  • Lepers R, Maffiuletti NA, Rochette L, Brugniaux J, Millet GY (2002) Neuromuscular fatigue during a long-duration cycling exercise. J Appl Physiol 92:1487–1493

    PubMed  Google Scholar 

  • Mador MJ, Magalang UJ, Rodis A, Kufel TJ (1993) Diaphragmatic fatigue after exercise in healthy human subjects. Am Rev Respir Dis 148:1571–1575

    Article  CAS  PubMed  Google Scholar 

  • 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 162:1760–1766

    Article  Google Scholar 

  • 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 161:118–123

    Article  CAS  PubMed  Google Scholar 

  • 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 163:930–935

    Article  CAS  PubMed  Google Scholar 

  • 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–R883

    CAS  Google Scholar 

  • 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 108:1224–1233

    Article  PubMed  Google Scholar 

  • 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 26:153–161

    Article  CAS  PubMed  Google Scholar 

  • 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:e17059

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 29:738–745

    Article  CAS  PubMed  Google Scholar 

  • 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 152:959–964

    Article  CAS  PubMed  Google Scholar 

  • 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 16:5–40

    Article  CAS  PubMed  Google Scholar 

  • Racinais S, Girard O, Micallef JP, Perrey S (2007) Failed excitability of spinal motoneurons induced by prolonged running exercise. J Neurophysiol 97:596–603

    Article  CAS  PubMed  Google Scholar 

  • Ross EZ, Goodall S, Stevens A, Harris I (2010) Time course of neuromuscular changes during running in well-trained subjects. Med Sci Sports Exerc 42:1184–1190

    PubMed  Google Scholar 

  • 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 171:1109–1115

    Article  PubMed  Google Scholar 

  • Sargeant AJ (2007) Structural and functional determinants of human muscle power. Exp Physiol 92:323–331

    Article  CAS  PubMed  Google Scholar 

  • 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:e65596

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 107:20541–20546

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 84:1692–1700

    CAS  PubMed  Google Scholar 

  • Skof B, Strojnik V (2006a) Neuro-muscular fatigue and recovery dynamics following anaerobic interval workload. Int J Sports Med 27:220–225

    Article  CAS  PubMed  Google Scholar 

  • Skof B, Strojnik V (2006b) Neuromuscular fatigue and recovery dynamics following prolonged continuous run at anaerobic threshold. Br J Sports Med 40:219–222

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Smith IC, Newham DJ (2007) Fatigue and functional performance of human biceps muscle following concentric or eccentric contractions. J Appl Physiol 102:207–213

    Article  PubMed  Google Scholar 

  • Taylor BJ, How SC, Romer LM (2006) Exercise-induced abdominal muscle fatigue in healthy humans. J Appl Physiol 100:1554–1562

    Article  PubMed  Google Scholar 

  • Verges S, Notter D, Spengler CM (2006a) Influence of diaphragm and rib cage muscle fatigue on breathing during endurance exercise. Respir Physiol Neurobiol 154:431–442

    Article  PubMed  Google Scholar 

  • Verges S, Schulz C, Perret C, Spengler CM (2006b) Impaired abdominal muscle contractility after high-intensity exhaustive exercise assessed by magnetic stimulation. Muscle Nerve 34:423–430

    Article  PubMed  Google Scholar 

  • 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–R1253

    Article  CAS  PubMed  Google Scholar 

  • 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 587:3665–3677

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 176:14–20

    Article  PubMed  Google Scholar 

  • Wilson SH, Cooke NT, Edwards RH, Spiro SG (1984) Predicted normal values for maximal respiratory pressures in caucasian adults and children. Thorax 39:535–538

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 98:1705–1717

    Article  PubMed  Google Scholar 

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Acknowledgments

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.

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Authors and Affiliations

  1. Exercise Physiology Lab, Institute of Human Movement Sciences and Sport, ETH Zurich, Winterthurerstrasse 190, 8057, Zurich, Switzerland

    Thomas U. Wüthrich, Elisabeth C. Eberle & Christina M. Spengler

  2. Zurich Center for Integrative Human Physiology (ZIHP), University of Zurich, Zurich, Switzerland

    Christina M. Spengler

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  1. Thomas U. Wüthrich
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  2. Elisabeth C. Eberle
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  3. Christina M. Spengler
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Correspondence to Christina M. Spengler.

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Communicated by Nicolas Place.

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Wüthrich, T.U., Eberle, E.C. & Spengler, C.M. Locomotor and diaphragm muscle fatigue in endurance athletes performing time-trials of different durations. Eur J Appl Physiol 114, 1619–1633 (2014). https://doi.org/10.1007/s00421-014-2889-7

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  • DOI: https://doi.org/10.1007/s00421-014-2889-7

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