Sport Sciences for Health

, Volume 12, Issue 3, pp 369–375 | Cite as

Lower fatigability of locomotor than non-locomotor muscles in endurance runners

  • Gennaro BocciaEmail author
  • Davide Dardanello
  • Cantor Tarperi
  • Luca Festa
  • Antonio La Torre
  • Federico Schena
  • Alberto Rainoldi
Original Article


Knee extensor and elbow flexor muscles have been demonstrated to have similar fatigability, i.e. time to task failure at submaximal force level, in healthy non-trained individuals. This experiment investigated if continuative endurance training can influence the fatigability of these two muscle groups in amateur runners. Surface electromyography was used to assess fatigability in twelve amateur runners. Participants were requested to sustain for 30 s the 70 % of their maximum voluntary contraction of knee extensor and elbow flexor muscles. During contractions, electromyographic signals were recorded, respectively, from vastus lateralis and biceps brachii muscles with linear array of eight electrodes. Muscle fiber conduction velocity (CV), mean power spectral frequency (MNF), and fractal dimension (FD) of electromyographic signals were calculated. During the sustained contraction vastus lateralis muscle showed smaller decrease of CV (p = 0.006), MNF (p = 0.001), and FD (p = 0.001) than biceps brachii muscle. The lower fatigability found in knee extensors than in elbow flexors suggests that the physiological adaptation promoted by the endurance training was specific to the musculature involved in the training (i.e. the lower limbs).


Fatigue Electromyography Vastus lateralis Biceps brachii Muscle fiber conduction velocity Fractal dimension 



We would like to thank Valentina Bellini, Valeria Rosso, and Emma Colamarino for their valuable help in data collection. The help of Corrado Cescon for the signal processing was much appreciated.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Ethical approval

The study was approved by the local ethical committee (Department of Neurological, Neuropsychological, Morphological and Movement Sciences, University of Verona) and performed in accordance with the Helsinki Declaration.

Informed consent

All participants provided their written informed consent before participation in the experiments.


  1. 1.
    Frey Law LA, Avin KG (2010) Endurance time is joint-specific: a modelling and meta-analysis investigation. Ergonomics 53(1):109–129. doi: 10.1080/00140130903389068 CrossRefPubMedGoogle Scholar
  2. 2.
    Fuglevand AJ, Zackowski KM, Huey KA, Enoka RM (1993) Impairment of neuromuscular propagation during human fatiguing contractions at submaximal forces. J Physiol 460:549–572CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Hunter SK, Critchlow A, Shin IS, Enoka RM (2004) Men are more fatigable than strength-matched women when performing intermittent submaximal contractions. J Appl Physiol 96(6):2125–2132. doi: 10.1152/japplphysiol.01342.2003 CrossRefPubMedGoogle Scholar
  4. 4.
    Avin KG, Naughton MR, Ford BW, Moore HE, Monitto-Webber MN, Stark AM, Gentile AJ, Law LA (2010) Sex differences in fatigue resistance are muscle group dependent. Med Sci Sports Exerc 42(10):1943–1950. doi: 10.1249/MSS.0b013e3181d8f8fa CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Burke RE, Levine DN, Tsairis P, Zajac FE 3rd (1973) Physiological types and histochemical profiles in motor units of the cat gastrocnemius. J Physiol 234(3):723–748CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Yassierli Nussbaum MA, Iridiastadi H, Wojcik LA (2007) The influence of age on isometric endurance and fatigue is muscle dependent: a study of shoulder abduction and torso extension. Ergonomics 50(1):26–45. doi: 10.1080/00140130600967323 CrossRefPubMedGoogle Scholar
  7. 7.
    Hunter SK, Ryan DL, Ortega JD, Enoka RM (2002) Task differences with the same load torque alter the endurance time of submaximal fatiguing contractions in humans. J Neurophysiol 88(6):3087–3096. doi: 10.1152/jn.00232.2002 CrossRefPubMedGoogle Scholar
  8. 8.
    Clark BC, Collier SR, Manini TM, Ploutz-Snyder LL (2005) Sex differences in muscle fatigability and activation patterns of the human quadriceps femoris. Eur J Appl Physiol 94(1–2):196–206. doi: 10.1007/s00421-004-1293-0 CrossRefPubMedGoogle Scholar
  9. 9.
    Hunter SK, Enoka RM (2001) Sex differences in the fatigability of arm muscles depends on absolute force during isometric contractions. J Appl Physiol 91(6):2686–2694PubMedGoogle Scholar
  10. 10.
    Place N, Maffiuletti NA, Ballay Y, Lepers R (2005) Twitch potentiation is greater after a fatiguing submaximal isometric contraction performed at short vs. long quadriceps muscle length. J Appl Physiol (1985) 98(2):429–436. doi: 10.1152/japplphysiol.00664.2004 CrossRefGoogle Scholar
  11. 11.
    Enoka RM (2012) Muscle fatigue—from motor units to clinical symptoms. J Biomech 45(3):427–433. doi: 10.1016/j.jbiomech.2011.11.047 CrossRefPubMedGoogle Scholar
  12. 12.
    Marcora SM, Staiano W (2010) The limit to exercise tolerance in humans: mind over muscle? Eur J Appl Physiol 109(4):763–770. doi: 10.1007/s00421-010-1418-6 CrossRefPubMedGoogle Scholar
  13. 13.
    Merletti R, Rainoldi A, Farina D (2001) Surface electromyography for noninvasive characterization of muscle. Exerc Sport Sci Rev 29(1):20–25CrossRefPubMedGoogle Scholar
  14. 14.
    Merletti R, Farina D, Gazzoni M (2003) The linear electrode array: a useful tool with many applications. J Electromyogr Kinesiol 13(1):37–47CrossRefPubMedGoogle Scholar
  15. 15.
    Merletti R, Knaflitz M, De Luca CJ (1990) Myoelectric manifestations of fatigue in voluntary and electrically elicited contractions. J Appl Physiol 69(5):1810–1820PubMedGoogle Scholar
  16. 16.
    Merletti R, Roy S (1996) Myoelectric and mechanical manifestations of muscle fatigue in voluntary contractions. J Orthop Sports Phys Ther 24(6):342–353CrossRefPubMedGoogle Scholar
  17. 17.
    Boccia G, Dardanello D, Rinaldo N, Coratella G, Schena F, Rainoldi A (2015) Electromyographic manifestations of fatigue correlate with pulmonary function, 6-min walk test, and time to exhaustion in COPD. Respir Care 60(9):1295–1302. doi: 10.4187/respcare.04138 CrossRefPubMedGoogle Scholar
  18. 18.
    Beck TW, Ye X, Wages NP (2015) Local muscle endurance is associated with fatigue-based changes in electromyographic spectral properties, but not with conduction velocity. J Electromyogr Kinesiol 25(3):451–456. doi: 10.1016/j.jelekin.2015.02.006 CrossRefPubMedGoogle Scholar
  19. 19.
    Rainoldi A, Galardi G, Maderna L, Comi G, Lo Conte L, Merletti R (1999) Repeatability of surface EMG variables during voluntary isometric contractions of the biceps brachii muscle. J Electromyogr Kinesiol 9(2):105–119CrossRefPubMedGoogle Scholar
  20. 20.
    Kupa EJ, Roy SH, Kandarian SC, De Luca CJ (1995) Effects of muscle fiber type and size on EMG median frequency and conduction velocity. J Appl Physiol 79(1):23–32PubMedGoogle Scholar
  21. 21.
    Sadoyama T, Masuda T, Miyata H, Katsuta S (1988) Fibre conduction velocity and fibre composition in human vastus lateralis. Eur J Appl Physiol Occup Physiol 57(6):767–771CrossRefPubMedGoogle Scholar
  22. 22.
    McCarthy JP, Pozniak MA, Agre JC (2002) Neuromuscular adaptations to concurrent strength and endurance training. Med Sci Sports Exerc 34(3):511–519CrossRefPubMedGoogle Scholar
  23. 23.
    Vila-Cha C, Falla D, Farina D (2010) Motor unit behavior during submaximal contractions following 6 weeks of either endurance or strength training. J Appl Physiol 109(5):1455–1466. doi: 10.1152/japplphysiol.01213.2009 CrossRefPubMedGoogle Scholar
  24. 24.
    Wasserman K (1984) The anaerobic threshold measurement to evaluate exercise performance. Am Rev Respir Dis 129(2 Pt 2):S35–S40CrossRefPubMedGoogle Scholar
  25. 25.
    Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G (2000) Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol 10(5):361–374CrossRefPubMedGoogle Scholar
  26. 26.
    Beretta Piccoli M, Rainoldi A, Heitz C, Wuthrich M, Boccia G, Tomasoni E, Spirolazzi C, Egloff M, Barbero M (2014) Innervation zone locations in 43 superficial muscles: toward a standardization of electrode positioning. Muscle Nerve 49(3):413–421CrossRefPubMedGoogle Scholar
  27. 27.
    Gitter JA, Czerniecki MJ (1995) Fractal analysis of the electromyographic interference pattern. J Neurosci Methods 58(1–2):103–108CrossRefPubMedGoogle Scholar
  28. 28.
    Mesin L, Cescon C, Gazzoni M, Merletti R, Rainoldi A (2009) A bi-dimensional index for the selective assessment of myoelectric manifestations of peripheral and central muscle fatigue. J Electromyogr Kinesiol 19(5):851–863. doi: 10.1016/j.jelekin.2008.08.003 CrossRefPubMedGoogle Scholar
  29. 29.
    Boccia G, Dardanello D, Beretta-Piccoli M, Cescon C, Coratella G, Rinaldo N, Barbero M, Lanza M, Schena F, Rainoldi A (2016) Muscle fiber conduction velocity and fractal dimension of EMG during fatiguing contraction of young and elderly active men. Physiol Meas 37(1):162–174. doi: 10.1088/0967-3334/37/1/162 CrossRefPubMedGoogle Scholar
  30. 30.
    Neyroud D, Ruttimann J, Mannion AF, Millet GY, Maffiuletti NA, Kayser B, Place N (2013) Comparison of neuromuscular adjustments associated with sustained isometric contractions of four different muscle groups. J Appl Physiol (1985) 114(10):1426–1434. doi: 10.1152/japplphysiol.01539.2012 CrossRefGoogle Scholar
  31. 31.
    Yan Z, Okutsu M, Akhtar YN, Lira VA (2011) Regulation of exercise-induced fiber type transformation, mitochondrial biogenesis, and angiogenesis in skeletal muscle. J Appl Physiol (1985) 110(1):264–274. doi: 10.1152/japplphysiol.00993.2010 CrossRefGoogle Scholar
  32. 32.
    Pietrangelo T, Mancinelli R, Doria C, Di Tano G, Loffredo B, Fanò-Illic G, Fulle S (2012) Endurance and resistance training modifies the transcriptional profile of the vastus lateralis skeletal muscle in healthy elderly subjects. Sport Sci Health 7:19–27. doi: 10.1007/s11332-012-0107-8 CrossRefGoogle Scholar
  33. 33.
    Mannion AF, Dumas GA, Stevenson JM, Cooper RG (1998) The influence of muscle fiber size and type distribution on electromyographic measures of back muscle fatigability. Spine (Phila Pa 1976) 23(5):576–584CrossRefGoogle Scholar
  34. 34.
    Schiaffino S, Reggiani C (2011) Fiber types in mammalian skeletal muscles. Physiol Rev 91(4):1447–1531. doi: 10.1152/physrev.00031.2010 CrossRefPubMedGoogle Scholar
  35. 35.
    Coyle EF (2005) Improved muscular efficiency displayed as Tour de France champion matures. J Appl Physiol (1985) 98(6):2191–2196. doi: 10.1152/japplphysiol.00216.2005 CrossRefGoogle Scholar
  36. 36.
    Costill DL, Daniels J, Evans W, Fink W, Krahenbuhl G, Saltin B (1976) Skeletal muscle enzymes and fiber composition in male and female track athletes. J Appl Physiol 40(2):149–154PubMedGoogle Scholar
  37. 37.
    Casale R, Rainoldi A, Nilsson J, Bellotti P (2003) Can continuous physical training counteract aging effect on myoelectric fatigue? A surface electromyography study application. Arch Phys Med Rehabil 84(4):513–517. doi: 10.1053/apmr.2003.50083 CrossRefPubMedGoogle Scholar
  38. 38.
    Melchiorri G, Rainoldi A (2008) Mechanical and myoelectric manifestations of fatigue in subjects with anorexia nervosa. J Electromyogr Kinesiol 18(2):291–297. doi: 10.1016/j.jelekin.2006.10.002 CrossRefPubMedGoogle Scholar
  39. 39.
    Falla D, Rainoldi A, Merletti R, Jull G (2003) Myoelectric manifestations of sternocleidomastoid and anterior scalene muscle fatigue in chronic neck pain patients. Clin Neurophysiol 114(3):488–495CrossRefPubMedGoogle Scholar
  40. 40.
    Pedrinelli R, Marino L, Dell’Omo G, Siciliano G, Rossi B (1998) Altered surface myoelectric signals in peripheral vascular disease: correlations with muscle fiber composition. Muscle Nerve 21(2):201–210CrossRefPubMedGoogle Scholar
  41. 41.
    Boccia G, Coratella G, Dardanello D, Rinaldo N, Lanza M, Schena F, Rainoldi A (2016) Severe COPD alters muscle fiber conduction velocity during knee extensors fatiguing contraction. COPD:1–6. doi: 10.3109/15412555.2016.1139561
  42. 42.
    Merletti R, Farina D, Gazzoni M, Schieroni MP (2002) Effect of age on muscle functions investigated with surface electromyography. Muscle Nerve 25(1):65–76. doi: 10.1002/mus.10014 CrossRefPubMedGoogle Scholar
  43. 43.
    Bazzucchi I, Felici F, Macaluso A, De Vito G (2004) Differences between young and older women in maximal force, force fluctuations, and surface EMG during isometric knee extension and elbow flexion. Muscle Nerve 30(5):626–635. doi: 10.1002/mus.20151 CrossRefPubMedGoogle Scholar
  44. 44.
    Bazzucchi I, Marchetti M, Rosponi A, Fattorini L, Castellano V, Sbriccoli P, Felici F (2005) Differences in the force/endurance relationship between young and older men. Eur J Appl Physiol 93(4):390–397. doi: 10.1007/s00421-004-1277-0 CrossRefPubMedGoogle Scholar
  45. 45.
    Fluck M (2006) Functional, structural and molecular plasticity of mammalian skeletal muscle in response to exercise stimuli. J Exp Biol 209(Pt 12):2239–2248. doi: 10.1242/jeb.02149 CrossRefPubMedGoogle Scholar
  46. 46.
    Fluck M, Hoppeler H (2003) Molecular basis of skeletal muscle plasticity–from gene to form and function. Rev Physiol Biochem Pharmacol 146:159–216. doi: 10.1007/s10254-002-0004-7 CrossRefPubMedGoogle Scholar
  47. 47.
    Hargreaves M, McKenna MJ, Jenkins DG, Warmington SA, Li JL, Snow RJ, Febbraio MA (1998) Muscle metabolites and performance during high-intensity, intermittent exercise. J Appl Physiol (1985) 84(5):1687–1691Google Scholar
  48. 48.
    Schmitz JP, van Dijk JP, Hilbers PA, Nicolay K, Jeneson JA, Stegeman DF (2012) Unchanged muscle fiber conduction velocity relates to mild acidosis during exhaustive bicycling. Eur J Appl Physiol 112(5):1593–1602. doi: 10.1007/s00421-011-2119-5 CrossRefPubMedGoogle Scholar
  49. 49.
    Brody LR, Pollock MT, Roy SH, De Luca CJ, Celli B (1991) pH-induced effects on median frequency and conduction velocity of the myoelectric signal. J Appl Physiol 71(5):1878–1885PubMedGoogle Scholar
  50. 50.
    Gonzalez-Izal M, Malanda A, Gorostiaga E, Izquierdo M (2012) Electromyographic models to assess muscle fatigue. J Electromyogr Kinesiol 22(4):501–512. doi: 10.1016/j.jelekin.2012.02.019 CrossRefPubMedGoogle Scholar
  51. 51.
    Kauffman LH (1986) The fractal geometry of nature—Mandelbrot, B. J Soc Biol Struct 9(1):33–36CrossRefGoogle Scholar
  52. 52.
    Beretta-Piccoli M, D’Antona G, Barbero M, Fisher B, Dieli-Conwright CM, Clijsen R, Cescon C (2015) Evaluation of central and peripheral fatigue in the quadriceps using fractal dimension and conduction velocity in young females. PLoS One 10(4):e0123921. doi: 10.1371/journal.pone.0123921 CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Coronell C, Orozco-Levi M, Mendez R, Ramirez-Sarmiento A, Galdiz JB, Gea J (2004) Relevance of assessing quadriceps endurance in patients with COPD. Eur Respir J 24(1):129–136CrossRefPubMedGoogle Scholar
  54. 54.
    Bawa P, Pang MY, Olesen KA, Calancie B (2006) Rotation of motoneurons during prolonged isometric contractions in humans. J Neurophysiol 96(3):1135–1140. doi: 10.1152/jn.01063.2005 CrossRefPubMedGoogle Scholar
  55. 55.
    Taylor JL, Gandevia SC (2008) A comparison of central aspects of fatigue in submaximal and maximal voluntary contractions. J Appl Physiol 104(2):542–550. doi: 10.1152/japplphysiol.01053.2007 CrossRefPubMedGoogle Scholar
  56. 56.
    Anderson T (1996) Biomechanics and running economy. Sports Med 22(2):76–89CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Italia 2016

Authors and Affiliations

  1. 1.CeRiSM Research Center “Sport, Mountain, and Health”RoveretoItaly
  2. 2.Motor Science Research Center, School of Exercise and Sport Sciences, SUISM, Department of Medical SciencesUniversity of TurinTurinItaly
  3. 3.School of Sport and Exercise Sciences, Department of Neurosciences, Biomedicine and Movement SciencesUniversity of VeronaVeronaItaly
  4. 4.Department of Biomedical Sciences for HealthUniversità degli Studi di MilanoMilanItaly

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