European Journal of Applied Physiology

, Volume 113, Issue 6, pp 1605–1615 | Cite as

Exercise-induced changes in triceps surae tendon stiffness and muscle strength affect running economy in humans

  • Kirsten Albracht
  • Adamantios Arampatzis
Original Article


The purpose of the present study was to investigate whether increased tendon-aponeurosis stiffness and contractile strength of the triceps surae (TS) muscle-tendon units induced by resistance training would affect running economy. Therefore, an exercise group (EG, n = 13) performed a 14-week exercise program, while the control group (CG, n = 13) did not change their training. Maximum isometric voluntary contractile strength and TS tendon-aponeurosis stiffness, running kinematics and fascicle length of the gastrocnemius medialis (GM) muscle during running were analyzed. Furthermore, running economy was determined by measuring the rate of oxygen consumption at two running velocities (3.0, 3.5 ms−1). The intervention resulted in a ∼7 % increase in maximum plantarflexion muscle strength and a ∼16 % increase in TS tendon-aponeurosis stiffness. The EG showed a significant ∼4 % reduction in the rate of oxygen consumption and energy cost, indicating a significant increase in running economy, while the CG showed no changes. Neither kinematics nor fascicle length and elongation of the series-elastic element (SEE) during running were affected by the intervention. The unaffected SEE elongation of the GM during the stance phase of running, in spite of a higher tendon-aponeurosis stiffness, is indicative of greater energy storage and return and a redistribution of muscular output within the lower extremities while running after the intervention, which might explain the improved running economy.


Running economy Tendon adaptation Fascicle behavior running Achilles tendon 



Energy cost


Control group


Exercise group


Effective mechanical advantage


Gastrocnemius medialis


Ground reaction force


Fascicle length


Reference fascicle length


Length of the muscle-tendon unit


Length of the series-elastic element


Muscle-tendon unit


Maximum voluntary contraction


Point of force application


Root mean square


Standard error of mean


Series elastic element


Standard deviation


Triceps surae


Pennation angle


Reference pennation angle

\(\overline{v}_{\rm fl}\)

Average fascicle shortening velocity

vmax, fl

Maximum fascicle shortening velocity

\({\dot{V}{\rm O}}_{\rm 2,max}\)

Rate of oxygen consumption



This research has been supported by The Federal Institute of Sport Science (BISp), Germany.


  1. Aggeloussis N, Giannakou E, Albracht K, Arampatzis A (2010) Reproducibility of fascicle length and pennation angle of gastrocnemius medialis in human gait in vivo. Gait Posture 31(1):73–77PubMedCrossRefGoogle Scholar
  2. Alexander RM (2002) Tendon elasticity and muscle function. Comp Biochem Physiol A Mol Integr Physiol 133(4):1001–1011PubMedCrossRefGoogle Scholar
  3. Alexander RM, Bennet-Clark HC (1977) Storage of elastic strain energy in muscle and other tissues. Nat Biotechnol 265(5590):114–117PubMedCrossRefGoogle Scholar
  4. Arampatzis A, Morey-Klapsing G, Karamanidis K, DeMonte G, Stafilidis S, Brüggemann GP (2005a) Differences between measured and resultant joint moments during isometric contractions at the ankle joint. J Biomech 38(4):885–892PubMedCrossRefGoogle Scholar
  5. Arampatzis A, Stafilidis S, DeMonte G, Karamanidis K, Morey-Klapsing G, Brüggemann GP (2005b) Strain and elongation of the human gastrocnemius tendon and aponeurosis during maximal plantarflexion effort. J Biomech 38(4):833–841PubMedCrossRefGoogle Scholar
  6. Arampatzis A, De Monte G, Karamanidis K, Morey-Klapsing G, Stafilidis S, Brüggemann GP (2006) Influence of the muscle-tendon unit’s mechanical and morphological properties on running economy. J Exp Biol 209(Pt 17):3345–3357PubMedCrossRefGoogle Scholar
  7. Arampatzis A, Karamanidis K, Albracht K (2007a) Adaptational responses of the human achilles tendon by modulation of the applied cyclic strain magnitude. J Exp Biol 210(Pt 15):2743–2753PubMedCrossRefGoogle Scholar
  8. Arampatzis A, Karamanidis K, Morey-Klapsing G, Monte GD, Stafilidis S (2007b) Mechanical properties of the triceps surae tendon and aponeurosis in relation to intensity of sport activity. J Biomech 40(9):1946–1952PubMedCrossRefGoogle Scholar
  9. Biewener AA, Roberts TJ (2000) Muscle and tendon contributions to force, work, and elastic energy savings: a comparative perspective. Exerc Sport Sci Rev 28(3):99–107PubMedGoogle Scholar
  10. Biewener AA, Farley CT, Roberts TJ, Temaner M (2004) Muscle mechanical advantage of human walking and running: implications for energy cost. J Appl Physiol 97(6):2266–2274PubMedCrossRefGoogle Scholar
  11. Capelli C (1999) Physiological determinants of best performances in human locomotion. Eur J Appl Physiol Occup Physiol 80(4):298–307PubMedCrossRefGoogle Scholar
  12. Cormie P, McGuigan MR, Newton RU (2010) Influence of strength on magnitude and mechanisms of adaptation to power training. Med Sci Sports Exerc 42(8):1566–1581PubMedCrossRefGoogle Scholar
  13. Costill DL, Thomason H, Roberts E (1973) Fractional utilization of the aerobic capacity during distance running. Med Sci Sports 5(4):248–252PubMedGoogle Scholar
  14. Daniels JT (1985) A physiologist’s view of running economy. Med Sci Sports Exerc 17(3):332–338PubMedGoogle Scholar
  15. de Monte G, Arampatzis A, Stogiannari C, Karamanidis K (2006) In vivo motion transmission in the inactive gastrocnemius medialis muscle-tendon unit during ankle and knee joint rotation. J Electromyogr Kinesiol 16(5):413–422PubMedCrossRefGoogle Scholar
  16. di Prampero PE, Atchou G, J C Brückner JC, C Moia C (1986) The energetics of endurance running. Eur J Appl Physiol Occup Physiol 55(3):259–266PubMedCrossRefGoogle Scholar
  17. di Prampero PE, Capelli C, Pagliaro P, Antonutto G, Girardis M, Zamparo P, Soule RG (1993) Energetics of best performances in middle-distance running. J Appl Physiol 74(5):2318–2324PubMedGoogle Scholar
  18. Dorn TW, Schache AG, Pandy MG (2012) Muscular strategy shift in human running: dependence of running speed on hip and ankle muscle performance. J Exp Biol 215(Pt 11):1944–1956PubMedCrossRefGoogle Scholar
  19. Epstein M, Herzog W (1998) Theoretical models of skeletal muscle: biological and mathematical considerations. Wiley Chichester, UKGoogle Scholar
  20. Fletcher JR, Esau SP, Macintosh BR (2009) Economy of running: beyond the measurement of oxygen uptake. J Appl Physiol 107(6):1918–1922PubMedCrossRefGoogle Scholar
  21. Fletcher JR, Esau SP, MacIntosh BR (2010) Changes in tendon stiffness and running economy in highly trained distance runners. Eur J Appl Physiol 110(5):1037–1046PubMedCrossRefGoogle Scholar
  22. Foster C, Lucia A (2007) Running economy : the forgotten factor in elite performance. Sports Med 37(4–5):316–319PubMedCrossRefGoogle Scholar
  23. Foure A, Nordez A, Cornu C (2010) Plyometric training effects on achilles tendon stiffness and dissipative properties. J Appl Physiol 109(3):849–854PubMedCrossRefGoogle Scholar
  24. Fukunaga T, Kubo K, Kawakami Y, Fukashiro S, Kanehisa H, Maganaris C (2001) In vivo behaviour of human muscle tendon during walking. Proc Biol Sci 268(1464):229–233PubMedCrossRefGoogle Scholar
  25. Hansen P, Aagaard P, Kjaer M, Larsson B, Magnusson SP (2003) Effect of habitual running on human achilles tendon load-deformation properties and cross-sectional area. J Appl Physiol 95(6):2375–2380PubMedGoogle Scholar
  26. Hawkins D, Hull ML (1990) A method for determining lower extremity muscle-tendon lengths during flexion/extension movements. J Biomech 23(5):487–494PubMedCrossRefGoogle Scholar
  27. Hayashi K (1996) Biomechanical studies of the remodeling of knee joint tendons and ligaments. J Biomech 29(6):707–716PubMedCrossRefGoogle Scholar
  28. Heise GD, Martin PE (2001) Are variations in running economy in humans associated with ground reaction force characteristics? Eur J Appl Physiol 84(5):438–442PubMedCrossRefGoogle Scholar
  29. Hill A (1938) The heat of shortening and the dynamic constants of muscle. Proc R Soc Lond B Biol Sci 1:136–195CrossRefGoogle Scholar
  30. Houdijk H, Bobbert MF, de Haan A (2006) Evaluation of a Hill based muscle model for the energy cost and efficiency of muscular contraction. J Biomech 39(3):536–543PubMedCrossRefGoogle Scholar
  31. Ishikawa M, Pakaslahti J, Komi P (2007) Medial gastrocnemius muscle behavior during human running and walking. Gait Posture 25(3):380–384PubMedCrossRefGoogle Scholar
  32. Johnson RE, Quinn T, Kertzer R, Vroman N (1997) Strength training in female distance runners: impact on running economy. J Strength Cond Res 11(4):224Google Scholar
  33. Ker RF, Bennett MB, Bibby SR, Kester RC, Alexander RM (1987) The spring in the arch of the human foot. Nat Biotechnol 325(7000):147–149PubMedCrossRefGoogle Scholar
  34. Krabbe B, Farkas R, Baumann W (1997) Influence of inertia on intersegment moments of the lower extremity joints. J Biomech 30(5):517–519PubMedCrossRefGoogle Scholar
  35. Kubo K, Kanehisa H, Fukunaga T (2002) Effects of resistance and stretching training programmes on the viscoelastic properties of human tendon structures in vivo. J Physiol 538(Pt 1):219–226PubMedCrossRefGoogle Scholar
  36. Kyröläinen H, Belli A, Komi PV (2001) Biomechanical factors affecting running economy. Med Sci Sports Exerc 33(8):1330–1337PubMedCrossRefGoogle Scholar
  37. Lichtwark GA, Wilson AM (2005) In vivo mechanical properties of the human achilles tendon during one-legged hopping. J Exp Biol 208(Pt 24):4715–4725PubMedCrossRefGoogle Scholar
  38. Lichtwark GA, Wilson AM (2008) Optimal muscle fascicle length and tendon stiffness for maximising gastrocnemius efficiency during human walking and running. J Theor Biol 252(4):662–673PubMedCrossRefGoogle Scholar
  39. Lichtwark GA, Bougoulias K, Wilson AM (2007) Muscle fascicle and series elastic element length changes along the length of the human gastrocnemius during walking and running. J Biomech 40(1):157–164PubMedCrossRefGoogle Scholar
  40. Lusk G (1924) Animal calorimetry: analysis of the oxidation of mixtures of carbohydrate and fat. J Biol Chem 59(1):41Google Scholar
  41. Mademli L, Arampatzis A, Morey-Klapsing G, Brüggemann GP (2004) Effect of ankle joint position and electrode placement on the estimation of the antagonistic moment during maximal plantarflexion. J Electromyogr Kinesiol 14(5):591–597PubMedCrossRefGoogle Scholar
  42. Maganaris CN, Baltzopoulos V, Sargeant AJ (2000) In vivo measurement-based estimations of the human achilles tendon moment arm. Eur J Appl Physiol 83(4–5):363–369PubMedCrossRefGoogle Scholar
  43. Magnusson SP, Aagaard P, Dyhre-Poulsen P, Kjaer M (2001) Load-displacement properties of the human triceps surae aponeurosis in vivo. J Physiol 531(Pt 1):277–288PubMedCrossRefGoogle Scholar
  44. Margaria R, Cerretelli P, Aghemo P, Sassi G (1963) Energy cost of running. J Appl Physiol 18:367–370PubMedGoogle Scholar
  45. Martin PE, Morgan DW (1992) Biomechanical considerations for economical walking and running. Med Sci Sports Exerc 24(4):467–474PubMedGoogle Scholar
  46. Millet GP, Jaouen B, Borrani F, Candau R (2002) Effects of concurrent endurance and strength training on running economy and .vo(2) kinetics. Med Sci Sports Exerc 34(8):1351–1359PubMedCrossRefGoogle Scholar
  47. Morgan DW, Baldini FD, Martin PE, Kohrt WM (1989a) Ten kilometer performance and predicted velocity at vo2max among well-trained male runners. Med Sci Sports Exerc 21(1):78–83PubMedCrossRefGoogle Scholar
  48. Morgan DW, Martin PE, Krahenbuhl GS (1989b) Factors affecting running economy. Sports Med 7(5):310–330PubMedCrossRefGoogle Scholar
  49. Morgan DW, Martin PE, Krahenbuhl GS, Baldini FD (1991) Variability in running economy and mechanics among trained male runners. Med Sci Sports Exerc 23(3):378–383PubMedGoogle Scholar
  50. Morgan DW, Craib MW, Krahenbuhl GS, Woodall K, Jordan S, Filarski K, Burleson C, Williams T (1994) Daily variability in running economy among well-trained male and female distance runners. Res Q Exerc Sport 65(1):72–77PubMedGoogle Scholar
  51. Muramatsu T, Muraoka T, Takeshita D, Kawakami Y, Hirano Y, Fukunaga T (2001) Mechanical properties of tendon and aponeurosis of human gastrocnemius muscle in vivo. J Appl Physiol 90(5):1671–1678PubMedGoogle Scholar
  52. Paavolainen L, Häkkinen K, Hämäläinen I, Nummela A, Rusko H (1999) Explosive-strength training improves 5-km running time by improving running economy and muscle power. J Appl Physiol 86(5):1527–1533PubMedGoogle Scholar
  53. Pereira MA, Freedson PS (1997) Intraindividual variation of running economy in highly trained and moderately trained males. Int J Sports Med 18(2):118–124PubMedCrossRefGoogle Scholar
  54. Reeves ND, Maganaris CN, Narici MV (2003) Effect of strength training on human patella tendon mechanical properties of older individuals. J Physiol 548(Pt 3):971–981PubMedCrossRefGoogle Scholar
  55. Roberts TJ, Marsh RL, Weyand PG, Taylor CR (1997) Muscular force in running turkeys: the economy of minimizing work. Sci Agric 275(5303):1113–1115PubMedCrossRefGoogle Scholar
  56. Rossiter HB, Howe FA, Ward SA, Kowalchuk JM, Griffiths JR, Whipp BJ (2000) Intersample fluctuations in phosphocreatine concentration determined by 31p-magnetic resonance spectroscopy and parameter estimation of metabolic responses to exercise in humans. J Physiol 528(Pt 2):359–369PubMedCrossRefGoogle Scholar
  57. Saunders PU, Pyne DB, Telford RD, Hawley JA (2004a) Factors affecting running economy in trained distance runners. Sports Med 34(7):465–485PubMedCrossRefGoogle Scholar
  58. Saunders PU, Pyne DB, Telford RD, Hawley JA (2004b) Reliability and variability of running economy in elite distance runners. Med Sci Sports Exerc 36(11):1972–1976PubMedCrossRefGoogle Scholar
  59. Spurrs RW, Murphy AJ, Watsford ML (2003) The effect of plyometric training on distance running performance. Eur J Appl Physiol 89(1):1–7PubMedCrossRefGoogle Scholar
  60. Wickiewicz TL, Roy RR, Powell PL, Edgerton VR (1983) Muscle architecture of the human lower limb. Clin Orthop Relat Res 1(179):275–283Google Scholar
  61. Williams KR, Cavanagh PR (1987) Relationship between distance running mechanics, running economy, and performance. J Appl Physiol 63(3):1236–1245PubMedGoogle Scholar
  62. Woledge RC, Curtin NA, Homsher E (1985) Energetic aspects of muscle contraction. Monogr Physiol Soc 41:1–357PubMedGoogle Scholar
  63. Woo SL, Ritter MA, Amiel D, Sanders TM, Gomez MA, Kuei SC, Garfin SR, Akeson WH (1980) The biomechanical properties of swine tendon—long term effects of exercise on the digital extensors. Connect Tissue Res 7(3):177–183PubMedCrossRefGoogle Scholar
  64. Zajac FE (1989) Muscle and tendon: properties, models, scaling, and application to biomechanics and motor control. Crit Rev Biomed Eng 17(4):359–411PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Institute of Biomechanics and OrthopaedicsGerman Sport UniversityCologneGermany
  2. 2.Department of Training and Movement Science, Centre of Sport Science and Sport MedicineHumboldt UniversityBerlinGermany

Personalised recommendations