European Journal of Applied Physiology

, Volume 117, Issue 5, pp 843–852 | Cite as

Relationship between isometric contraction intensity and muscle hardness assessed by ultrasound strain elastography

  • Takayuki Inami
  • Toru Tsujimura
  • Takuya Shimizu
  • Takemasa Watanabe
  • Wing Yin Lau
  • Kazunori Nosaka
Original Article

Abstract

Introduction

Ultrasound elastography is used to assess muscle hardness or stiffness; however, no previous studies have validated muscle hardness measures using ultrasound strain elastography (SE). This study investigated the relationship between plantar flexor isometric contraction intensity and gastrocnemius hardness assessed by SE. We hypothesised that the muscle would become harder linearly with an increase in the contraction intensity of the plantar flexors.

Methods

Fifteen young women (20.1 ± 0.8 years) performed isometric contractions of the ankle plantar flexors at four different intensities (25, 50, 75, 100% of maximal voluntary contraction force: MVC) at 0° plantar flexion. Using SE images, the strain ratio (SR) between the muscle and an acoustic coupler (elastic modulus 22.6 kPa) placed over the skin was calculated (muscle/coupler); pennation angle and muscle thickness were measured for the resting and contracting conditions.

Results

SR decreased with increasing contraction intensity from rest (1.28 ± 0.20) to 25% (0.99 ± 0.21), 50% (0.61 ± 0.15), 75% (0.34 ± 0.1) and 100% MVC (0.20 ± 0.05). SR decreased linearly (P < 0.05) with increasing MVC from rest to 75% MVC, but levelled off from 75 and 100% MVC. SR was negatively correlated with pennation angle (r = −0.80, P < 0.01) and muscle thickness ( r= −0.78,  P< 0.01).

Conclusion

SR appears to represent muscle hardness changes in response to contraction intensity changes, in the assumption that the gastrocnemius muscle contraction intensity is proportional to the plantar flexion intensity. We concluded that gastrocnemius muscle hardness changes could be validly assessed by SR, and the force–hardness relationship was not linear.

Keywords

Gastrocnemius Strain ratio Muscle force Pennation angle Muscle thickness 

Abbreviations

ANOVA

Analysis of variance

CV

Coefficient of variation

EVA

Ethylene vinyl acetate

MVC

Maximum voluntary contraction

ROI

Region of interest

SD

Standard deviation

SE

Strain elastography

SR

Strain ratio

Notes

Acknowledgements

The authors would like to thank Mr. Naoyuki Murayama and Ms. Yoko Fujihara of Hitachi, Ltd. (Japan) for their technical assistance in the study.

References

  1. Akagi R, Chino K, Dohi M, Takahashi H (2012) Relationships between muscle size and hardness of the medial gastrocnemius at different ankle joint angles in young men. Acta Radiol 53:307–311CrossRefPubMedGoogle Scholar
  2. Ariji Y, Katsumata A, Hiraiwa Y, Izumi M, Iida Y, Goto M, Sakuma S, Ogi N, Kurita K, Ariji E (2009) Use of sonographic elastography of the masseter muscles for optimizing massage pressure: a preliminary study. J Oral Rehabil 36:627–635CrossRefPubMedGoogle Scholar
  3. Ashina M, Bendtsen L, Jensen R, Sakai F, Olesen J (1999) Muscle hardness in patients with chronic tension-type headache: relation to actual headache state. Pain 79:201–205CrossRefPubMedGoogle Scholar
  4. Ates F, Hug F, Bouillard K, Jubeau M, Frappart T, Couade M, Bercoff J, Nordez A (2015) Muscle shear elastic modulus is linearly related to muscle torque over the entire range of isometric contraction intensiy. J Electromyogr Kinesiol 25:703–708CrossRefPubMedGoogle Scholar
  5. Brandenburg JE, Eby SF, Song P, Zhao H, Brault JS, Chen S, An KN (2014) Ultrasound elastography: The new frontier in direct muasument of muscle stiffness. Arch Phys Med Rehabil 95:2207–2219CrossRefPubMedPubMedCentralGoogle Scholar
  6. Chino K, Akagi R, Dohi M, Fukashiro S, Takahashi H (2012) Reliability and validity of quantifying absolute muscle hardness using ultrasound elastography. PLoS One 7:e45764CrossRefPubMedPubMedCentralGoogle Scholar
  7. de Oliveira LF, Menegaldo LL (2010) Individual-specific muscle maximum force estimation using ultrasound for ankle joint torque prediction using an EMG-driven Hill-type model. J Biomech 43:2816–2821CrossRefPubMedGoogle Scholar
  8. Ewertsen C, Carlsen JF, Christiansen IR, Jensen JA, Nielsen MB (2016) Evaluation of healthy muscle tissue by strain and shear wave elastography—dependency on depth and ROI position in relation to underlying bone. Ultrasonics 71:127–133CrossRefPubMedGoogle Scholar
  9. Ford LE, Huxley AF, Simmons RM (1981) The relation between stiffness and filament overlap in stimulated frog muscle fibres. J Physiol 311:219–249CrossRefPubMedPubMedCentralGoogle Scholar
  10. Fujihara Y, Matsumura T, Murayama N, Motoki M, Mitake T (2011) Development of acoustic coupler for elastography. Medix 55: 40–44Google Scholar
  11. Fukunaga T, Roy RR, Shellock FG, Hodgson JA, Edgerton VR (1996) Specific tension of human plantar flexors and dorsiflexors. J Appl Physiol 80:158–165PubMedGoogle Scholar
  12. Gennisson JL, Cornu C, Catheline S, Fink M, Portero P (2005) Human muscle hardness assessment during incremental isometric contraction using transient elastography. J Biomech 38:1543–1550CrossRefPubMedGoogle Scholar
  13. Horowits R, Kempner ES, Bisher ME, Podolsky RJ (1986) A physiological role for titin and nebulin in skeletal muscle. Nature 323:160–164CrossRefPubMedGoogle Scholar
  14. Hug F, Tucker K, Gennisson JL, Tanter M, Nordez A (2015) Elastography for muscle biomechanics: Toward the estimation of individual muscle force. Exerc Sports Sci Rev 43:125–133CrossRefGoogle Scholar
  15. Ikezoe T, Mori N, Nakamura M, Ichihashi N (2011) Atrophy of the lower limbs in elderly women: is it related to walking ability? Eur J Appl Physiol 111:989–995CrossRefPubMedGoogle Scholar
  16. Kawakami Y, Ichinose Y, Kubo K, Ito M, Imai M, Fukunaga T (2000) Architecture of human muscle and it’s functional significance. J Appl Biomech 16:88–98CrossRefGoogle Scholar
  17. Kubo K, Morimoto M, Komuro T, Yata H, Tsunoda N, Kanehisa H, Fukunaga T (2007) Effects of plyometric and weight training on muscle–tendon complex and jump performance. Med Sci Sports Exerc 39:1801–1810CrossRefPubMedGoogle Scholar
  18. Leonard CT, Deshner WP, Romo JW, Suoja ES, Fehrer SC, Mikhailenok EL (2003) Myotonometer intra- and interrater reliabilities. Arch Phys Med Rehabil 84:928–932CrossRefPubMedGoogle Scholar
  19. Mademli L, Arampatzis A (2005) Behaviour of the human gastrocnemius muscle architecture during submaximal isometric fatigue. Eur J Appl Physiol 94:611–617CrossRefPubMedGoogle Scholar
  20. Maganaris CN, Baltzopoulos V, Sargeant AJ (2002) Repeated contractions alter the geometry of human skeletal muscle. J Appl Physiol 93:2089–2094CrossRefPubMedGoogle Scholar
  21. Maisetti 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 45:978–984CrossRefPubMedGoogle Scholar
  22. Marusiak J, Jaskolska A, Koszewicz M, Budrewicz S, Jaskolski A (2012) Myometry revealed medication-induced decrease in resting skeletal muscle stiffness in Parkinson’s disease patients. Clin Biomech 27:632–635CrossRefGoogle Scholar
  23. Morisada M, Okada K, Kawakita K (2006) Quantitative analysis of muscle hardness in tetanic contractions induced by electrical stimulation in rats. Eur J Appl Physiol 97:681–686CrossRefPubMedGoogle Scholar
  24. Murayama M, Nosaka K, Yoneda T, Minamitani K (2000) Changes in hardness of the human elbow flexor muscles after eccentric exercise. Eur J Appl Physiol 82:361–367CrossRefPubMedGoogle Scholar
  25. Murayama M, Watanabe K, Kato R, Uchiyama T, Yoneda T (2012) Association of muscle hardness with muscle tension dynamics: a physiological property. Eur J Appl Physiol 112:105–112CrossRefPubMedGoogle Scholar
  26. Nordez A, Hug F (2010) Muscle shear elastic modulus measured using supersonic shear imaging is highly related to muscle activity level. J Appl Physiol 108:1389–1394CrossRefPubMedGoogle Scholar
  27. Sasaki K, Toyama S, Ishii N (2014) Length–force characteristics of in vivo human muscle reflected by supersonic shear imaging. J Appl Physiol 117:153–162CrossRefPubMedGoogle Scholar
  28. Witvrouw E, Danneels L, Asselman P, D’Have T, Cambier D (2003) Muscle flexibility as a risk factor for developing muscle injuries in male professional soccer players. A prospective study. Am J Sports Med 31:41–46PubMedGoogle Scholar
  29. Woods JJ, Bigland-Ritchie B (1983) Linear and non-linear surface EMG/force relationships in human muscles. An anatomical/functional argument for the existence of both. Am J Phys Med 62:287–299PubMedGoogle Scholar
  30. Yanagisawa O, Niitsu M, Kurihara T, Fukubayashi T (2011) Evaluation of human muscle hardness after dynamic exercise with ultrasound real-time tissue elastography: a feasibility study. Clin Radiol 66:815–819CrossRefPubMedGoogle Scholar
  31. Yoshii Y, Ishii T, Tanaka T, Tung WL, Sakai S (2014) Detecting medican nerve strain changes with cyclic compression apparatus: a comparison of carpal tunnel syndrome patients and healthy controls. Ultrasound Med Biol 41:669–674CrossRefGoogle Scholar
  32. 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 50:103–113CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Takayuki Inami
    • 1
    • 2
  • Toru Tsujimura
    • 3
  • Takuya Shimizu
    • 4
  • Takemasa Watanabe
    • 4
  • Wing Yin Lau
    • 1
  • Kazunori Nosaka
    • 1
  1. 1.Centre for Exercise and Sports Science Research, School of Medical and Health SciencesEdith Cowan UniversityJoondalupAustralia
  2. 2.Faculty of Sport SciencesWaseda UniversityTokorozawaJapan
  3. 3.Tsujimura Surgery HospitalKariyaJapan
  4. 4.Graduate School of Health and Sport SciencesChukyo UniversityNagoyaJapan

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