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Muscle-specific acute changes in passive stiffness of human triceps surae after stretching

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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.

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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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Friden J, Lieber RL (2002) Mechanical considerations in the design of surgical reconstructive procedures. J Biomech 35:1039–1045

    Article  PubMed  Google Scholar 

  • Gajdosik RL (2001) Passive extensibility of skeletal muscle: review of the literature with clinical implications. Clin Biomech (Bristol, Avon) 16:87–101

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Magnusson SP (1998) Passive properties of human skeletal muscle during stretch maneuvers. A review. Scand J Med Sci Sports 8:65–77

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Purslow PP (1989) Strain-induced reorientation of an intramuscular connective tissue network: implications for passive muscle elasticity. J Biomech 22:21–31

    Article  CAS  PubMed  Google Scholar 

  • Rassier DE, Lee EJ, Herzog W (2005) Modulation of passive force in single skeletal muscle fibres. Biol Lett 1:342–345

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by JSPS KAKENHI Grant Number 25702038.

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Correspondence to Naokazu Miyamoto.

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The authors declare that they have no conflict of interest.

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Communicated by Olivier Seynnes.

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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

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  • DOI: https://doi.org/10.1007/s00421-016-3349-3

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