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.
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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
References
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 53:307–311
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 36:627–635
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 79:201–205
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 25:703–708
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 95:2207–2219
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:e45764
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 43:2816–2821
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 71:127–133
Ford LE, Huxley AF, Simmons RM (1981) The relation between stiffness and filament overlap in stimulated frog muscle fibres. J Physiol 311:219–249
Fujihara Y, Matsumura T, Murayama N, Motoki M, Mitake T (2011) Development of acoustic coupler for elastography. Medix 55: 40–44
Fukunaga T, Roy RR, Shellock FG, Hodgson JA, Edgerton VR (1996) Specific tension of human plantar flexors and dorsiflexors. J Appl Physiol 80:158–165
Gennisson JL, Cornu C, Catheline S, Fink M, Portero P (2005) Human muscle hardness assessment during incremental isometric contraction using transient elastography. J Biomech 38:1543–1550
Horowits R, Kempner ES, Bisher ME, Podolsky RJ (1986) A physiological role for titin and nebulin in skeletal muscle. Nature 323:160–164
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 43:125–133
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 111:989–995
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 16:88–98
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 39:1801–1810
Leonard CT, Deshner WP, Romo JW, Suoja ES, Fehrer SC, Mikhailenok EL (2003) Myotonometer intra- and interrater reliabilities. Arch Phys Med Rehabil 84:928–932
Mademli L, Arampatzis A (2005) Behaviour of the human gastrocnemius muscle architecture during submaximal isometric fatigue. Eur J Appl Physiol 94:611–617
Maganaris CN, Baltzopoulos V, Sargeant AJ (2002) Repeated contractions alter the geometry of human skeletal muscle. J Appl Physiol 93:2089–2094
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 45:978–984
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 27:632–635
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 97:681–686
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 82:361–367
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 112:105–112
Nordez A, Hug F (2010) Muscle shear elastic modulus measured using supersonic shear imaging is highly related to muscle activity level. J Appl Physiol 108:1389–1394
Sasaki K, Toyama S, Ishii N (2014) Length–force characteristics of in vivo human muscle reflected by supersonic shear imaging. J Appl Physiol 117:153–162
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 31:41–46
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 62:287–299
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 66:815–819
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 41:669–674
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
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.
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Communicated by Nicolas Place.
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Inami, T., Tsujimura, T., Shimizu, T. et al. Relationship between isometric contraction intensity and muscle hardness assessed by ultrasound strain elastography. Eur J Appl Physiol 117, 843–852 (2017). https://doi.org/10.1007/s00421-016-3528-2
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DOI: https://doi.org/10.1007/s00421-016-3528-2