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Early detection of exercise-induced muscle damage using elastography

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European Journal of Applied Physiology Aims and scope Submit manuscript

Abstract

Purpose

This study aimed to determine whether an increase in muscle shear modulus measured 30 min after eccentric exercise (30 min) reflects the magnitude of force deficit measured 48-h post-exercise (48 H).

Methods

A total of 53 healthy participants were distributed in five groups. Four groups performed either repeated eccentric elbow flexions or knee extensions at either a low or high load. A fifth group performed repeated concentric elbow flexions (control load).

Results

A significant decreased peak torque was found for elbow flexors and knee extensors 48 h after the eccentric exercises (all P values < 0.001). A significant increase in shear modulus was found at 30 min for the elbow flexors for low (+70.5 ± 44.3%, P < 0.001) and high load (+153.9 ± 192.4%, P < 0.001). Similarly, the shear modulus of knee extensors increased for low (+26.7 ± 19.1%, P < 0.001) and high load (+79.4 ± 67.1%, P < 0.001). The relative increase in shear modulus measured at 30 min was significantly correlated to the relative decrease in peak torque measured at 48 H for both elbow flexors (r = −0.80) and knee extensors (r = −0.82). A further analysis suggested that biceps brachii and rectus femoris were more affected by muscle damage than their synergists.

Conclusion

This study shows that an increase in muscle shear modulus measured 30 min after a damaging exercise reflects the decrease in peak torque measured at 48 H. Shear modulus may therefore, provide a useful tool for coaches and clinicians to non-invasively estimate the amount of muscle damage induced by a damaging exercise.

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Abbreviations

ANOVA:

Analysis of variance

BA:

Brachialis

BB:

Biceps brachii

MVC:

Maximal voluntary contraction

RF:

Rectus femoris

SSI:

Supersonic shear imaging

VL:

Vastus lateralis

VM:

Vastus medialis

References

  • Agten CA, Buck FM, Dyer L et al (2016) Delayed-onset muscle soreness: temporal assessment with quantitative MRI and shear-wave ultrasound elastography. AJR Am J Roentgenol. doi:10.2214/AJR.16.16617

    Google Scholar 

  • Balnave CD, Allen DG (1995) Intracellular calcium and force in single mouse muscle fibres following repeated contractions with stretch. J Physiol 488:25

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balnave CD, Allen DG (1996) The effect of muscle length on intracellular calcium and force in single fibres from mouse skeletal muscle. J Physiol 492:705–713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beaton LJ, Tarnopolsky MA, Phillips SM (2002) Variability in estimating eccentric contraction-induced muscle damage and inflammation in humans. Can J Appl Physiol 27:516–526

    Article  PubMed  Google Scholar 

  • Bercoff J, Tanter M, Fink M (2004) Supersonic shear imaging: a new technique for soft tissue elasticity mapping. Ultrason Ferroelectr Freq Control IEEE Trans 51:396–409

    Article  Google Scholar 

  • Bouillard K, Hug F, Guével A, Nordez A (2012a) Shear elastic modulus can be used to estimate an index of individual muscle force during a submaximal isometric fatiguing contraction. J Appl Physiol (1985) 113:1353–1361. doi:10.1152/japplphysiol.00858.2012

    Article  Google Scholar 

  • Bouillard K, Nordez A, Hodges PW et al (2012b) Evidence of changes in load sharing during isometric elbow flexion with ramped torque. J Biomech 45:1424–1429. doi:10.1016/j.jbiomech.2012.02.020

    Article  PubMed  Google Scholar 

  • Butterfield TA, Herzog W (2005) Quantification of muscle fiber strain during in vivo repetitive stretch-shortening cycles. J Appl Physiol 99:593–602. doi:10.1152/japplphysiol.01128.2004

    Article  PubMed  Google Scholar 

  • Capetanaki Y, Bloch RJ, Kouloumenta A et al (2007) Muscle intermediate filaments and their links to membranes and membranous organelles. Exp Cell Res 313:2063–2076. doi:10.1016/j.yexcr.2007.03.033

    Article  CAS  PubMed  Google Scholar 

  • Chapman DW, Simpson JA, Iscoe S, Robins T, Nosaka K (2013) Changes in serum fast and slow skeletal troponin I concentration following maximal eccentric contractions. J Sci Med Sport 16:82–85

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Ruell PA, Ghoddusi M et al (2007) Ultrastructural changes and sarcoplasmic reticulum Ca2+ regulation in red vastus muscle following eccentric exercise in the rat: effects of eccentric exercise on SR Ca2+ regulation. Exp Physiol 92:437–447. doi:10.1113/expphysiol.2006.036442

    Article  CAS  PubMed  Google Scholar 

  • Cohen JH (1988) Statistical power for the behavioral sciences. REMEDICA Publishing, London

    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. doi:10.1016/S0021-9290(02)00430-X

    Article  PubMed  Google Scholar 

  • Eby SF, Song P, Chen S et al (2013) Validation of shear wave elastography in skeletal muscle. J Biomech 46:2381–2387. doi:10.1016/j.jbiomech.2013.07.033

    Article  PubMed  Google Scholar 

  • Eby SF, Cloud BA, Brandenburg JE et al (2015) Shear wave elastography of passive skeletal muscle stiffness: influences of sex and age throughout adulthood. Clin Biomech 30:22–27. doi:10.1016/j.clinbiomech.2014.11.011

    Article  Google Scholar 

  • Eby S, Zhao H, Song P et al (2016) Quantitative evaluation of passive muscle stiffness in chronic stroke. Am J Phys Med Rehabil 95:899–910. doi:10.1097/PHM.0000000000000516

    Article  PubMed  Google Scholar 

  • Farahmand F, Sejiavongse W, Amis AA (1998) Quantitative study of the quadriceps muscles and trochlear groove geometry related to instability of the patellofemoral joint. J Orthop Res 16:136–143

    Article  CAS  PubMed  Google Scholar 

  • Green MA, Sinkus R, Gandevia SC et al (2012) Measuring changes in muscle stiffness after eccentric exercise using elastography: measuring muscle stiffness changes after eccentric exercise using mre. NMR Biomed 25:852–858. doi:10.1002/nbm.1801

    Article  CAS  PubMed  Google Scholar 

  • Guilhem G, Doguet V, Hauraix H et al (2016) Muscle force loss and soreness subsequent to maximal eccentric contractions depend on the amount of fascicle strain in vivo. Acta Physiol 217:152–163. doi:10.1111/apha.12654

    Article  CAS  Google Scholar 

  • Herzog W (2014) Mechanisms of enhanced force production in lengthening (eccentric) muscle contractions. J Appl Physiol 116:1407–1417. doi:10.1152/japplphysiol.00069.2013

    Article  PubMed  Google Scholar 

  • Hoang PD, Herbert RD, Gandevia SC (2007) Effects of eccentric exercise on passive mechanical properties of human gastrocnemius in vivo. Med Sci Sports Exerc 39:849–857. doi:10.1249/MSS.0b013e318033499b

    Article  PubMed  Google Scholar 

  • Hopkins WG (2000) Measures of reliability in sports medicine and science. Sports Med 30:1–15

    Article  CAS  PubMed  Google Scholar 

  • Jamurtas AZ, Theocharis V, Tofas T et al (2005) Comparison between leg and arm eccentric exercises of the same relative intensity on indices of muscle damage. Eur J Appl Physiol 95:179–185. doi:10.1007/s00421-005-1345-0

    Article  PubMed  Google Scholar 

  • Johnson MA, Sideri G, Weightman D, Appleton D (1973) A comparison of fibre size, fibre type constitution and spatial fibre type distribution in normal human muscle and in muscle from cases of spinal muscular atrophy and from other neuromuscular disorders. J Neurol Sci 20:345–361

    Article  CAS  PubMed  Google Scholar 

  • Kawakami Y, Nakazawa K, Fujimoto T et al (1994) Specific tension of elbow flexor and extensor muscles based on magnetic resonance imaging. Eur J Appl Physiol 68:139–147

    Article  CAS  Google Scholar 

  • Kulig K, Powers CM, Shellock FG, Terk M (2001) The effects of eccentric velocity on activation of elbow flexors: evaluation by magnetic resonance imaging. Med Sci Sports Exerc 33:196–200

    Article  CAS  PubMed  Google Scholar 

  • Lacourpaille L, Hug F, Bouillard K et al (2012) Supersonic shear imaging provides a reliable measurement of resting muscle shear elastic modulus. Physiol Meas 33:N19–28. doi:10.1088/0967-3334/33/3/N19

    Article  PubMed  Google Scholar 

  • Lacourpaille L, Nordez A, Hug F (2013) Influence of stimulus intensity on electromechanical delay and its mechanisms. J Electromyogr Kinesiol Off J Int Soc Electrophysiol Kinesiol 23:51–55. doi:10.1016/j.jelekin.2012.06.010

    Article  Google Scholar 

  • Lacourpaille L, Nordez A, Hug F et al (2014) Time-course effect of exercise-induced muscle damage on localized muscle mechanical properties assessed using elastography. Acta Physiol 211:135–146. doi:10.1111/apha.12272

    Article  CAS  Google Scholar 

  • Lieber R, Thornell E, Friden J (1996) Muscle cytoskeletal disruption occurs within the first 15 min of cyclic eccentric contraction. J Appl Physiol 80:278–284

    Article  CAS  PubMed  Google Scholar 

  • Opar MDA, Williams MD, Shield AJ (2012) Hamstring strain injuries. Sports Med 42:209–226

    Article  PubMed  Google Scholar 

  • Paddon-Jones D, Keech A, Lonergan A, Abernethy P (2005) Differential expression of muscle damage in humans following acute fast and slow velocity eccentric exercise. J Sci Med Sport 8:255–263

    Article  CAS  PubMed  Google Scholar 

  • Paulsen G, Crameri R, Benestad HB, Fjeld JG, Morkrid L, Hallen J, Raastad T (2010) Time course of leukocyte accumulation in human muscle after eccentric exercise. Med Sci Sports Exerc 42:75–85

    Article  PubMed  Google Scholar 

  • Paulsen G, Mikkelsen UR, Raastad T, Peake JM (2012) Leucocytes, cytokines and satellite cells: what role do they play in muscle damage and regeneration following eccentric exercise. Exerc Immunol Rev 18:42–97

    PubMed  Google Scholar 

  • Prior BM, Jayaraman RC, Reid RW et al (2001) Biarticular and monoarticular muscle activation and injury in human quadriceps muscle. Eur J Appl Physiol 85:185–190. doi:10.1007/s004210100434

    Article  CAS  PubMed  Google Scholar 

  • Proske U, Morgan DL (2001) Muscle damage from eccentric exercise: mechanism, mechanical signs, adaptation and clinical applications. J Physiol 537:333–345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raastad T, Owe SG, Paulsen G et al (2010) Changes in calpain activity, muscle structure, and function after eccentric exercise. Med Sci Sports Exerc 42:86–95. doi:10.1249/MSS.0b013e3181ac7afa

    Article  PubMed  Google Scholar 

  • Salomoni S, Tucker K, Hug F et al (2016) Reduced maximal force during acute anterior knee pain is associated with deficits in voluntary muscle activation. PLoS One 11:e0161487. doi:10.1371/journal.pone.0161487

    Article  PubMed  PubMed Central  Google Scholar 

  • Stephenson D, Wendt I (1984) Length dependence of changes in sarcoplasmic calcium concentration and myofibrillar calcium sensitivity in striated muscle fibres. J Muscle Res Cell Motil 5:243–272

    Article  CAS  PubMed  Google Scholar 

  • Takahashi H, Kuno S, Miyamoto T et al (1994) Changes in magnetic resonance images in human skeletal muscle after eccentric exercise. Eur J Appl Physiol 69:408–413

    Article  CAS  Google Scholar 

  • Warren GL, Lowe DA, Armstrong RB (1999) Measurement tools used in the study of eccentric contraction-induced injury. Sports Med 27:43–59. doi:10.2165/00007256-199927010-00004

    Article  CAS  PubMed  Google Scholar 

  • Whitehead NP, Weerakkody NS, Gregory JE et al (2001) Changes in passive tension of muscle in humans and animals after eccentric exercise. J Physiol 533:593–604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This study was supported by grants from the French Ministry of Sports (Contract No. 15i19) and the Région Pays de la Loire (QUETE Project No. 2015-09035).

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Authors and Affiliations

  1. Laboratory “Movement, Interactions, Performance” (EA 4334), Faculty of Sport Sciences, University of Nantes, 25 bis boulevard Guy Mollet, BP 72206, 44322, Nantes Cedex 3, France

    Lilian Lacourpaille, Antoine Nordez, François Hug, Valentin Doguet & Ricardo Andrade

  2. Research Department, Laboratory “Sport, Expertise and Performance” (EA 7370), French Institute of Sport (INSEP), Paris, France

    Lilian Lacourpaille & Gaël Guilhem

  3. NHMRC Centre of Clinical Research Excellence in Spinal Pain, Injury and Health, School of Health and Rehabilitation Sciences, The University of Queensland, Brisbane, Australia

    François Hug

  4. Institut Universitaire de France, Paris, France

    François Hug

Authors
  1. Lilian Lacourpaille
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  2. Antoine Nordez
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  3. François Hug
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  4. Valentin Doguet
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  5. Ricardo Andrade
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  6. Gaël Guilhem
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Corresponding author

Correspondence to Lilian Lacourpaille.

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Conflict of interest

No conflicts of interest, financial or otherwise, are declared by the authors. The results of the study are presented clearly, honestly, and without fabrication, falsification, or inappropriate data manipulation. The results of the present study do not constitute endorsement by the American College of Sports Medicine.

Additional information

Communicated by Olivier Seynnes.

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Lacourpaille, L., Nordez, A., Hug, F. et al. Early detection of exercise-induced muscle damage using elastography. Eur J Appl Physiol 117, 2047–2056 (2017). https://doi.org/10.1007/s00421-017-3695-9

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  • DOI: https://doi.org/10.1007/s00421-017-3695-9

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