Skip to main content
Top
Published in: European Journal of Applied Physiology 5/2017

01-05-2017 | Original Article

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

Authors: Takayuki Inami, Toru Tsujimura, Takuya Shimizu, Takemasa Watanabe, Wing Yin Lau, Kazunori Nosaka

Published in: European Journal of Applied Physiology | Issue 5/2017

Login to get access

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.
Literature
go back to reference 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 53:307–311CrossRefPubMed 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 53:307–311CrossRefPubMed
go back to reference 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 36:627–635CrossRefPubMed 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 36:627–635CrossRefPubMed
go back to reference 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 79:201–205CrossRefPubMed 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 79:201–205CrossRefPubMed
go back to reference 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 25:703–708CrossRefPubMed 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 25:703–708CrossRefPubMed
go back to reference 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 95:2207–2219CrossRefPubMedPubMedCentral 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 95:2207–2219CrossRefPubMedPubMedCentral
go back to reference 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:e45764CrossRefPubMedPubMedCentral 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:e45764CrossRefPubMedPubMedCentral
go back to reference 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 43:2816–2821CrossRefPubMed 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 43:2816–2821CrossRefPubMed
go back to reference 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 71:127–133CrossRefPubMed 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 71:127–133CrossRefPubMed
go back to reference Fujihara Y, Matsumura T, Murayama N, Motoki M, Mitake T (2011) Development of acoustic coupler for elastography. Medix 55: 40–44 Fujihara Y, Matsumura T, Murayama N, Motoki M, Mitake T (2011) Development of acoustic coupler for elastography. Medix 55: 40–44
go back to reference Fukunaga T, Roy RR, Shellock FG, Hodgson JA, Edgerton VR (1996) Specific tension of human plantar flexors and dorsiflexors. J Appl Physiol 80:158–165PubMed Fukunaga T, Roy RR, Shellock FG, Hodgson JA, Edgerton VR (1996) Specific tension of human plantar flexors and dorsiflexors. J Appl Physiol 80:158–165PubMed
go back to reference Gennisson JL, Cornu C, Catheline S, Fink M, Portero P (2005) Human muscle hardness assessment during incremental isometric contraction using transient elastography. J Biomech 38:1543–1550CrossRefPubMed Gennisson JL, Cornu C, Catheline S, Fink M, Portero P (2005) Human muscle hardness assessment during incremental isometric contraction using transient elastography. J Biomech 38:1543–1550CrossRefPubMed
go back to reference Horowits R, Kempner ES, Bisher ME, Podolsky RJ (1986) A physiological role for titin and nebulin in skeletal muscle. Nature 323:160–164CrossRefPubMed Horowits R, Kempner ES, Bisher ME, Podolsky RJ (1986) A physiological role for titin and nebulin in skeletal muscle. Nature 323:160–164CrossRefPubMed
go back to reference 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 43:125–133CrossRef 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 43:125–133CrossRef
go back to reference 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 111:989–995CrossRefPubMed 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 111:989–995CrossRefPubMed
go back to reference 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 16:88–98CrossRef 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 16:88–98CrossRef
go back to reference 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 39:1801–1810CrossRefPubMed 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 39:1801–1810CrossRefPubMed
go back to reference Leonard CT, Deshner WP, Romo JW, Suoja ES, Fehrer SC, Mikhailenok EL (2003) Myotonometer intra- and interrater reliabilities. Arch Phys Med Rehabil 84:928–932CrossRefPubMed Leonard CT, Deshner WP, Romo JW, Suoja ES, Fehrer SC, Mikhailenok EL (2003) Myotonometer intra- and interrater reliabilities. Arch Phys Med Rehabil 84:928–932CrossRefPubMed
go back to reference Mademli L, Arampatzis A (2005) Behaviour of the human gastrocnemius muscle architecture during submaximal isometric fatigue. Eur J Appl Physiol 94:611–617CrossRefPubMed Mademli L, Arampatzis A (2005) Behaviour of the human gastrocnemius muscle architecture during submaximal isometric fatigue. Eur J Appl Physiol 94:611–617CrossRefPubMed
go back to reference Maganaris CN, Baltzopoulos V, Sargeant AJ (2002) Repeated contractions alter the geometry of human skeletal muscle. J Appl Physiol 93:2089–2094CrossRefPubMed Maganaris CN, Baltzopoulos V, Sargeant AJ (2002) Repeated contractions alter the geometry of human skeletal muscle. J Appl Physiol 93:2089–2094CrossRefPubMed
go back to reference 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 45:978–984CrossRefPubMed 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 45:978–984CrossRefPubMed
go back to reference 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 27:632–635CrossRef 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 27:632–635CrossRef
go back to reference 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 97:681–686CrossRefPubMed 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 97:681–686CrossRefPubMed
go back to reference 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 82:361–367CrossRefPubMed 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 82:361–367CrossRefPubMed
go back to reference 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 112:105–112CrossRefPubMed 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 112:105–112CrossRefPubMed
go back to reference Nordez A, Hug F (2010) Muscle shear elastic modulus measured using supersonic shear imaging is highly related to muscle activity level. J Appl Physiol 108:1389–1394CrossRefPubMed Nordez A, Hug F (2010) Muscle shear elastic modulus measured using supersonic shear imaging is highly related to muscle activity level. J Appl Physiol 108:1389–1394CrossRefPubMed
go back to reference Sasaki K, Toyama S, Ishii N (2014) Length–force characteristics of in vivo human muscle reflected by supersonic shear imaging. J Appl Physiol 117:153–162CrossRefPubMed Sasaki K, Toyama S, Ishii N (2014) Length–force characteristics of in vivo human muscle reflected by supersonic shear imaging. J Appl Physiol 117:153–162CrossRefPubMed
go back to reference 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 31:41–46PubMed 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 31:41–46PubMed
go back to reference 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 62:287–299PubMed 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 62:287–299PubMed
go back to reference 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 66:815–819CrossRefPubMed 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 66:815–819CrossRefPubMed
go back to reference 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 41:669–674CrossRef 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 41:669–674CrossRef
go back to reference 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 50:103–113CrossRefPubMed 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 50:103–113CrossRefPubMed
Metadata
Title
Relationship between isometric contraction intensity and muscle hardness assessed by ultrasound strain elastography
Authors
Takayuki Inami
Toru Tsujimura
Takuya Shimizu
Takemasa Watanabe
Wing Yin Lau
Kazunori Nosaka
Publication date
01-05-2017
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Applied Physiology / Issue 5/2017
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI
https://doi.org/10.1007/s00421-016-3528-2

Other articles of this Issue 5/2017

European Journal of Applied Physiology 5/2017 Go to the issue