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Hamstring stiffness pattern during contraction in healthy individuals: analysis by ultrasound-based shear wave elastography

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Abstract

Purpose

To assess the stiffness of hamstring muscles during isometric contractions in healthy individuals, using ultrasound-based shear wave elastography to (1) determine the intra- and inter-day assessment repeatability, (2) characterize the stiffness of semitendinosus (ST) and biceps femoris long head (BFlh) along the contraction intensity, and (3) characterize stiffness distribution among the hamstring muscles and inter-limb symmetry.

Methods

Two experiments were conducted. In experiment I (n = 12), the intra-day repeatability in assessing the BFlh and ST stiffness were determined at intensities between 10–60% of maximal voluntary isometric contraction (MVIC) in a single session. In experiment II (n = 11), the stiffness of the hamstring muscles of both thighs was assessed at 20% of MVIC in the first session; and retested (for one randomly chosen thigh) in a second session. Isometric contraction of knee flexors was performed with the knee flexed at 30° and with the hip in a neutral position.

Results

Moderate-to-very-high intra- and inter-day repeatability was found (ICC = 0.69–0.93). The BFlh/ST stiffness ratio increased with contraction intensity. At 20% of MVIC, the ST showed the highest stiffness among the hamstring muscles (p < 0.02), with no differences between the remaining hamstring muscles (p > 0.474). No differences were found between limbs (p = 0.12).

Conclusions

The stiffness distribution among the hamstring muscles during submaximal isometric contractions is heterogeneous, but symmetric between limbs, and changes depending on the contraction intensity. Shear wave elastography is a reliable tool to assess the stiffness of hamstring muscles during contraction.

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Abbreviations

BFlh:

Biceps femoris long head

BFlh/ST:

Biceps femoris long head to semitendinosus ratio

BFsh:

Biceps femoris short head

d :

Cohen effect size

ICC:

Intraclass correlation coefficient

MVIC:

Maximum voluntary isometric contractions

r :

Pearson correlation coefficient

sEMG:

Surface electromyography

SEM:

Standard error of measurement

SM:

Semimembranosus

ST:

Semitendinosus

SWE:

Ultrasound-based shear wave elastography

References

  • Alfuraih AM, O’Connor P, Hensor E et al (2018) The effect of unit, depth, and probe load on the reliability of muscle shear wave elastography: variables affecting reliability of SWE. J Clin Ultrasound 46:108–115

    Article  PubMed  Google Scholar 

  • Ateş F, Hug F, Bouillard K et al (2015) Muscle shear elastic modulus is linearly related to muscle torque over the entire range of isometric contraction intensity. J Electromyogr Kinesiol 25:703–708

    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 

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

    Article  PubMed  Google Scholar 

  • Bouillard K, Jubeau M, Nordez A et al (2014) Effect of vastus lateralis fatigue on load sharing between quadriceps femoris muscles during isometric knee extensions. J Neurophysiol 111:768–776

    Article  PubMed  Google Scholar 

  • Bourne MN, Duhig SJ, Timmins RG et al (2016) Impact of the Nordic hamstring and hip extension exercises on hamstring architecture and morphology: implications for injury prevention. Br J Sports Med. https://doi.org/10.1136/bjsports-2016-096130

    Article  PubMed  Google Scholar 

  • Cagnie B, Elliott JM, O’Leary S et al (2011) Muscle functional MRI as an imaging tool to evaluate muscle activity. J Orthop Sports Phys Ther 41:896–903

    Article  PubMed  Google Scholar 

  • Campy RM, Coelho AJ, Pincivero DM (2009) EMG-torque relationship and reliability of the medial and lateral hamstring muscles. Med Sci Sports Exerc 41:2064–2071

    Article  PubMed  Google Scholar 

  • Dieterich AV, Andrade RJ, Le Sant G et al (2017) Shear wave elastography reveals different degrees of passive and active stiffness of the neck extensor muscles. Eur J Appl Physiol 117:171–178

    Article  PubMed  Google Scholar 

  • Dolman B, Verrall G, Reid I (2014) Physical principles demonstrate that the biceps femoris muscle relative to the other hamstring muscles exerts the most force: implications for hamstring muscle strain injuries. Muscles Ligaments Tendons J 4:371–377

    PubMed  PubMed Central  Google Scholar 

  • Ekstrand J, Hägglund M, Waldén M (2011) Epidemiology of muscle injuries in professional football (soccer). Am J Sports Med 39:1226–1232

    Article  PubMed  Google Scholar 

  • Ekstrand J, Jan E, Markus W, Martin H (2016) Hamstring injuries have increased by 4% annually in men’s professional football, since 2001: a 13-year longitudinal analysis of the UEFA Elite Club injury study. Br J Sports Med 50:731–737

    Article  PubMed  Google Scholar 

  • Feeley BT, Kennelly S, Barnes RP et al (2008) Epidemiology of National Football League training camp injuries from 1998 to 2007. Am J Sports Med 36:1597–1603

    Article  PubMed  Google Scholar 

  • Hallén A, Ekstrand J (2014) Return to play following muscle injuries in professional footballers. J Sports Sci 32:1229–1236

    Article  PubMed  Google Scholar 

  • Heiderscheit BC, Sherry MA, Silder A et al (2010) Hamstring strain injuries: recommendations for diagnosis, rehabilitation, and injury prevention. J Orthop Sports Phys Ther 40:67–81

    Article  PubMed  PubMed Central  Google Scholar 

  • Hug F, Tucker K, Gennisson J-L et al (2015) Elastography for muscle biomechanics: toward the estimation of individual muscle force. Exerc Sport Sci Rev 43:125–133

    Article  PubMed  Google Scholar 

  • Ichihashi N, Umegaki H, Ikezoe T et al (2016) The effects of a 4-week static stretching programme on the individual muscles comprising the hamstrings. J Sports Sci 34:2155–2159

    Article  PubMed  Google Scholar 

  • Kellis E, Katis A (2008) Reliability of EMG power-spectrum and amplitude of the semitendinosus and biceps femoris muscles during ramp isometric contractions. J Electromyogr Kinesiol 18:351–358

    Article  PubMed  Google Scholar 

  • Kot BCW, Zhang ZJ, Lee AWC et al (2012) Elastic modulus of muscle and tendon with shear wave ultrasound elastography: variations with different technical settings. PLoS One 7:e44348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumazaki T, Ehara Y, Sakai T (2012) Anatomy and physiology of hamstring injury. Int J Sports Med 33:950–954

    Article  CAS  PubMed  Google Scholar 

  • Lacourpaille L, Nordez A, Hug F (2017) The nervous system does not compensate for an acute change in the balance of passive force between synergist muscles. J Exp Biol 220:3455–3463

    Article  PubMed  Google Scholar 

  • Lapole T, Tindel J, Galy R, Nordez A (2015) Contracting biceps brachii elastic properties can be reliably characterized using supersonic shear imaging. Eur J Appl Physiol 115:497–505

    Article  PubMed  Google Scholar 

  • Le Sant G, Ates F, Brasseur J-L, Nordez A (2015) Elastography study of hamstring behaviors during passive stretching. PLoS One 10:e0139272

    Article  PubMed  PubMed Central  Google Scholar 

  • Le Sant G, Nordez A, Andrade R et al (2017) Stiffness mapping of lower leg muscles during passive dorsiflexion. J Anat 230:639–650

    Article  PubMed  PubMed Central  Google Scholar 

  • Marshall PW, Lovell R, Siegler JC (2016) Changes in passive tension of the hamstring muscles during a simulated soccer match. Int J Sports Physiol Perform 11:594–601

    Article  PubMed  Google Scholar 

  • Martinez Valdes E, Valdes EM, Negro F et al (2018) Surface EMG amplitude does not identify differences in neural drive to synergistic muscles. J Appl Physiol. https://doi.org/10.1152/japplphysiol.01115.2017

    Article  PubMed  Google Scholar 

  • McHugh MP, Connolly DA, Eston RG et al (1999) The role of passive muscle stiffness in symptoms of exercise-induced muscle damage. Am J Sports Med 27:594–599

    Article  CAS  PubMed  Google Scholar 

  • Mendez-Villanueva A, Suarez-Arrones L, Rodas G et al (2016) MRI-based regional muscle use during hamstring strengthening exercises in elite soccer players. PLoS One 11:e0161356

    Article  PubMed  PubMed Central  Google Scholar 

  • Miyamoto N, Hirata K, Kanehisa H (2017) Effects of hamstring stretching on passive muscle stiffness vary between hip flexion and knee extension maneuvers. Scand J Med Sci Sports 27:99–106

    Article  CAS  PubMed  Google Scholar 

  • Morin J-B, Gimenez P, Edouard P et al (2015) Sprint acceleration mechanics: the major role of hamstrings in horizontal force production. Front Physiol 6:404

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Raiteri BJ, Hug F, Cresswell AG, Lichtwark GA (2016) Quantification of muscle co-contraction using supersonic shear wave imaging. J Biomech 49:493–495

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Schache AG, Dorn TW, Blanch PD et al (2012) Mechanics of the human hamstring muscles during sprinting. Med Sci Sports Exerc 44:647–658

    Article  PubMed  Google Scholar 

  • Schmitt B, Tim T, McHugh M (2012) Hamstring injury rehabilitation and prevention of reinjury using lengthened state eccentric training: a new concept. Int J Sports Phys Ther 7:333–341

    PubMed  PubMed Central  Google Scholar 

  • Schuermans J, Van Tiggelen D, Danneels L, Witvrouw E (2014) Biceps femoris and semitendinosus—teammates or competitors? New insights into hamstring injury mechanisms in male football players: a muscle functional MRI study. Br J Sports Med 48:1599–1606

    Article  PubMed  Google Scholar 

  • Schuermans J, Van Tiggelen D, Danneels L, Witvrouw E (2016) Susceptibility to hamstring injuries in soccer: a prospective study using muscle functional magnetic resonance imaging. Am J Sports Med 44:1276–1285

    Article  PubMed  Google Scholar 

  • Shinohara M, Sabra K, Gennisson J-L et al (2010) Real-time visualization of muscle stiffness distribution with ultrasound shear wave imaging during muscle contraction. Muscle Nerve 42:438–441

    Article  PubMed  Google Scholar 

  • Sigrist RMS, Liau J, Kaffas AE et al (2017) Ultrasound elastography: review of techniques and clinical applications. Theranostics 7:1303–1329

    Article  PubMed  PubMed Central  Google Scholar 

  • Souron R, Bordat F, Farabet A et al (2016) Sex differences in active tibialis anterior stiffness evaluated using supersonic shear imaging. J Biomech 49:3534–3537

    Article  PubMed  Google Scholar 

  • Tsaklis P, Malliaropoulos N, Mendiguchia J et al (2015) Muscle and intensity based hamstring exercise classification in elite female track and field athletes: implications for exercise selection during rehabilitation. Open Access J Sports Med 6:209–217

    PubMed  PubMed Central  Google Scholar 

  • Umegaki H, Ikezoe T, Nakamura M et al (2015a) Acute effects of static stretching on the hamstrings using shear elastic modulus determined by ultrasound shear wave elastography: differences in flexibility between hamstring muscle components. Man Ther 20:610–613

    Article  PubMed  Google Scholar 

  • Umegaki H, Ikezoe T, Nakamura M et al (2015b) The effect of hip rotation on shear elastic modulus of the medial and lateral hamstrings during stretching. Man Ther 20:134–137

    Article  PubMed  Google Scholar 

  • Watsford ML, Murphy AJ, McLachlan KA et al (2010) A prospective study of the relationship between lower body stiffness and hamstring injury in professional Australian rules footballers. Am J Sports Med 38:2058–2064

    Article  PubMed  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 

  • Zebis MK, Skotte J, Andersen CH et al (2013) Kettlebell swing targets semitendinosus and supine leg curl targets biceps femoris: an EMG study with rehabilitation implications. Br J Sports Med 47:1192–1198

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors confirm that they have read the Journal’s position on issues involved in ethical publication and affirm that this report is consistent with those guidelines.

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Authors and Affiliations

Authors

Contributions

All authors conceived and designed the research. TF and BM conducted experiments. TN processed the data. TF and BM analyzed data. TF and BM wrote the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Sandro R. Freitas.

Ethics declarations

Conflict of interest

None of the authors has any conflict of interest to disclose. JV is funded by P20GM109090.

Informed consent

Informed consent was obtained from all individual participants included in the study. We are thankful to Mr. Vitor Meha for his great contribution in the experimental setup.

Additional information

Communicated by Olivier Seynnes.

The study protocol was approved by the Ethics Council of the Faculty of Human Kinetics, University of Lisbon. The authors certify that they have no affiliations with or financial involvement in any organization or entity with a direct financial interest in the subject matter or materials discussed in the article.

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Mendes, B., Firmino, T., Oliveira, R. et al. Hamstring stiffness pattern during contraction in healthy individuals: analysis by ultrasound-based shear wave elastography. Eur J Appl Physiol 118, 2403–2415 (2018). https://doi.org/10.1007/s00421-018-3967-z

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  • DOI: https://doi.org/10.1007/s00421-018-3967-z

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