Abstract
Purpose
It remains unclear whether the acute effect of stretching on passive muscle stiffness differs among the synergists. We examined the muscle stiffness responses of the medial (MG) and lateral gastrocnemii (LG), and soleus (Sol) during passive dorsiflexion before and after a static stretching by using ultrasound shear wave elastography.
Methods
Before and after a 5-min static stretching by passive dorsiflexion, shear modulus of the triceps surae and the Achilles tendon (AT) during passive dorsiflexion in the knee extended position were measured in 12 healthy subjects.
Results
Before the static stretching, shear modulus was the greatest in MG and smallest in Sol. The stretching induced significant reductions in shear modulus of MG, but not in shear modulus of LG and Sol. The slack angle was observed at more plantar flexed position in the following order: AT, MG, LG, and Sol. After the stretching, the slack angles of each muscle and AT were significantly shifted to more dorsiflexed positions with a similar extent. When considering the shift in slack angle, the change in MG shear modulus became smaller.
Conclusion
The present study indicates that passive muscle stiffness differs among the triceps surae, and that the acute effect of a static stretching is observed only in the stiff muscle. However, a large part of the reduction of passive muscle stiffness at a given joint angle could be due to an increase in the slack length.
Similar content being viewed by others
Abbreviations
- ANOVA:
-
Analysis of variance
- AT:
-
Achilles tendon
- EMG:
-
Electromyography
- LG:
-
Lateral gastrocnemius
- MG:
-
Medial gastrocnemius
- MTU:
-
Muscle–tendon unit
- MVC:
-
Maximal voluntary contraction
- RMS:
-
Root mean square
- ROM:
-
Range of motion
- Sol:
-
Soleus
References
Abellaneda S, Guissard N, Duchateau J (2009) The relative lengthening of the myotendinous structures in the medial gastrocnemius during passive stretching differs among individuals. J Appl Physiol 106:169–177
Agur AM, Ng-Thow-Hing V, Ball KA, Fiume E, McKee NH (2003) Documentation and three-dimensional modelling of human soleus muscle architecture. Clin Anat 16:285–293
Bercoff J, Tanter M, Fink M (2004) Supersonic shear imaging: a new technique for soft tissue elasticity mapping. IEEE Trans Ultrason Ferroelectr Freq Control 51:396–409
Blazevich AJ, Cannavan D, Waugh CM, Fath F, Miller SC, Kay AD (2012) Neuromuscular factors influencing the maximum stretch limit of the human plantar flexors. J Appl Physiol 113:1446–1455
Campbell KS, Lakie M (1998) A cross-bridge mechanism can explain the thixotropic short-range elastic component of relaxed frog skeletal muscle. J Physiol 510:941–962
Davis J, Kaufman KR, Lieber RL (2003) Correlation between active and passive isometric force and intramuscular pressure in the isolated rabbit tibialis anterior muscle. J Biomech 36:505–512
Eby SF, Song P, Chen S, Chen Q, Greenleaf JF, An KN (2013) Validation of shear wave elastography in skeletal muscle. J Biomech 46:2381–2387
Freitas SR, Andrade RJ, Larcoupaille L, Mil-Homens P, Nordez A (2015) Muscle and joint responses during and after static stretching performed at different intensities. Eur J Appl Physiol 115:1263–1272
Friden J, Lieber RL (2002) Mechanical considerations in the design of surgical reconstructive procedures. J Biomech 35:1039–1045
Gajdosik RL (2001) Passive extensibility of skeletal muscle: review of the literature with clinical implications. Clin Biomech (Bristol, Avon) 16:87–101
Gennisson JL, Deffieux T, Mace E, Montaldo G, Fink M, Tanter M (2010) Viscoelastic and anisotropic mechanical properties of in vivo muscle tissue assessed by supersonic shear imaging. Ultrasound Med Biol 36:789–801
Herbert RD, Moseley AM, Butler JE, Gandevia SC (2002) Change in length of relaxed muscle fascicles and tendons with knee and ankle movement in humans. J Physiol 539:637–645
Hirata K, Kanehisa H, Miyamoto-Mikami E, Miyamoto N (2015) Evidence for intermuscle difference in slack angle in human triceps surae. J Biomech 48:1210–1213
Hodgson JA, Finni T, Lai AM, Edgerton VR, Sinha S (2006) Influence of structure on the tissue dynamics of the human soleus muscle observed in MRI studies during isometric contractions. J Morphol 267:584–601
Hug F, Lacourpaille L, Maisetti O, Nordez A (2013) Slack length of gastrocnemius medialis and Achilles tendon occurs at different ankle angles. J Biomech 46:2534–2538
Johnson MA, Polgar J, Weightman D, Appleton D (1973) Data on the distribution of fibre types in thirty-six human muscles. An autopsy study. J Neurol Sci 18:111–129
Kato E, Kanehisa H, Fukunaga T, Kawakami Y (2010) Changes in ankle joint stiffness due to stretching: the role of tendon elongation of the gastrocnemius muscle. Eur J Sport Sci 10:111–119
Kawakami Y, Kumagai K, Huijing PA, Hijikata T, Fukunaga T (2000) The length–force characteristics of human gastrocnemius and soleus muscles in vivo. In: Herzog W (ed) Skeletal muscle mechanics: mechanisms to function. Wiley, New York, pp 398–404
Konrad A, Tilp M (2014a) Effects of ballistic stretching training on the properties of human muscle and tendon structures. J Appl Physiol 117:29–35
Konrad A, Tilp M (2014b) Increased range of motion after static stretching is not due to changes in muscle and tendon structures. Clin Biomech (Bristol, Avon) 29:636–642
Kovanen V, Suominen H, Heikkinen E (1984a) Collagen of slow twitch and fast twitch muscle fibres in different types of rat skeletal muscle. Eur J Appl Physiol Occup Physiol 52:235–242
Kovanen V, Suominen H, Heikkinen E (1984b) Mechanical properties of fast and slow skeletal muscle with special reference to collagen and endurance training. J Biomech 17:725–735
Lacourpaille L, Nordez A, Hug F, Couturier A, Dibie C, Guilhem G (2014) Time-course effect of exercise-induced muscle damage on localized muscle mechanical properties assessed using elastography. Acta Physiol (Oxf) 211:135–146
Magnusson SP (1998) Passive properties of human skeletal muscle during stretch maneuvers. A review. Scand J Med Sci Sports 8:65–77
Magnusson SP, Simonsen EB, Aagaard P, Boesen J, Johannsen F, Kjaer M (1997) Determinants of musculoskeletal flexibility: viscoelastic properties, cross-sectional area, EMG and stretch tolerance. Scand J Med Sci Sports 7:195–202
Maïsetti O, Hug F, Bouillard K, Nordez A (2012) Characterization of passive elastic properties of the human medial gastrocnemius muscle belly using supersonic shear imaging. J Biomech 45:978–984
Miyamoto N, Hirata K, Kanehisa H, Yoshitake Y (2015a) Validity of measurement of shear modulus by ultrasound shear wave elastography in human pennate muscle. PLoS One 10:e0124311
Miyamoto N, Hirata K, Kanehisa H (2015b) Effects of hamstring stretching on passive muscle stiffness vary between hip flexion and knee extension maneuvers. Scand J Med Sci Sports. doi:10.1111/sms.12620
Morse CI, Degens H, Seynnes OR, Maganaris CN, Jones DA (2008) The acute effect of stretching on the passive stiffness of the human gastrocnemius muscle tendon unit. J Physiol 586:97–106
Mutungi G, Ranatunga KW (1996) The viscous, viscoelastic and elastic characteristics of resting fast and slow mammalian (rat) muscle fibres. J Physiol 496:827–836
Mutungi G, Ranatunga KW (1998) Temperature-dependent changes in the viscoelasticity of intact resting mammalian (rat) fast- and slow-twitch muscle fibres. J Physiol 508:253–265
Nakamura M, Ikezoe T, Takeno Y, Ichihashi N (2011) Acute and prolonged effect of static stretching on the passive stiffness of the human gastrocnemius muscle tendon unit in vivo. J Orthop Res 29:1759–1763
Palmeri ML, Wang MH, Dahl JJ, Frinkley KD, Nightingale KR (2008) Quantifying hepatic shear modulus in vivo using acoustic radiation force. Ultrasound Med Biol 34:546–558
Purslow PP (1989) Strain-induced reorientation of an intramuscular connective tissue network: implications for passive muscle elasticity. J Biomech 22:21–31
Rassier DE, Lee EJ, Herzog W (2005) Modulation of passive force in single skeletal muscle fibres. Biol Lett 1:342–345
Wang K, McCarter R, Wright J, Beverly J, Ramirez-Mitchell R (1991) Regulation of skeletal muscle stiffness and elasticity by titin isoforms: a test of the segmental extension model of resting tension. Proc Natl Acad Sci USA 88:7101–7105
Yoshitake Y, Takai Y, Kanehisa H, Shinohara M (2014) Muscle shear modulus measured with ultrasound shear-wave elastography across a wide range of contraction intensity. Muscle Nerve 50:103–113
Zimmerman SD, McCormick RJ, Vadlamudi RK, Thomas DP (1993) Age and training alter collagen characteristics in fast- and slow-twitch rat limb muscle. J Appl Physiol 75:1670–1674
Acknowledgments
This work was supported by JSPS KAKENHI Grant Number 25702038.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Olivier Seynnes.
Rights and permissions
About this article
Cite this article
Hirata, K., Miyamoto-Mikami, E., Kanehisa, H. et al. Muscle-specific acute changes in passive stiffness of human triceps surae after stretching. Eur J Appl Physiol 116, 911–918 (2016). https://doi.org/10.1007/s00421-016-3349-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00421-016-3349-3