European Journal of Applied Physiology

, Volume 118, Issue 3, pp 585–593 | Cite as

Passive stiffness of monoarticular lower leg muscles is influenced by knee joint angle

  • Filiz Ateş
  • Ricardo J. Andrade
  • Sandro R. Freitas
  • François Hug
  • Lilian Lacourpaille
  • Raphael Gross
  • Can A. Yucesoy
  • Antoine Nordez
Original Article

Abstract

Purpose

While several studies demonstrated the occurrence of intermuscular mechanical interactions, the physiological significance of these interactions remains a matter of debate. The purpose of this study was to quantify the localized changes in the shear modulus of the gastrocnemius lateralis (GL), monoarticular dorsi- and plantar-flexor muscles induced by a change in knee angle.

Method

Participants underwent slow passive ankle rotations at the following two knee positions: knee flexed at 90° and knee fully extended. Ultrasound shear wave elastography was used to assess the muscle shear modulus of the GL, soleus [both proximally (SOL-proximal) and distally (SOL distal)], peroneus longus (PERL), and tibialis anterior (TA). This was performed during two experimental sessions (experiment I: n = 11; experiment II: n = 10). The shear modulus of each muscle was compared between the two knee positions.

Results

The shear modulus was significantly higher when the knee was fully extended than when the knee was flexed (P < 0.001) for the GL (averaged increase on the whole range of motion: + 5.8 ± 1.3 kPa), SOL distal (+ 4.5 ± 1.5 kPa), PERL (+ 1.1 ± 0.7 kPa), and TA (+ 1.6 ± 1.0 kPa). In contrast, a lower SOL-proximal shear modulus (P < 0.001, − 5.9 ± 1.0 kPa) was observed.

Conclusion

As the muscle shear modulus is linearly related to passive muscle force, these results provide evidence of a non-negligible intermuscular mechanical interaction between the human lower leg muscles during passive ankle rotations. The role of these interactions in the production of coordinated movements requires further investigation.

Keywords

Ultrasound Shear modulus Shear wave elastography Intermuscular mechanical interactions Epimuscular myofascial force transmission 

Abbreviations

ANOVA

Analysis of variance

EMG

Electromyography

GL

Gastrocnemius lateralis

GM

Gastrocnemius medialis

MRI

Magnetic resonance imaging

PERL

Peroneus longus

ROI

Region of interest

ROM

Range of motion

SOL

Soleus

SSI

Supersonic shear imaging

TA

Tibialis anterior

Notes

Acknowledgements

This study was supported by grants from the European Regional development Fund (ERDF, no. 37400), the Region Pays de la Loire (QUETE project), and by the Interdisciplinary program from the University of Nantes.

Author contributions

FA, RJA, SRF, CAY, RG, FH, and AN conceived and designed research. FA, RJA, SRF, and LL conducted experiments. FA, RJA and AN analyzed data. FA and RJA wrote the manuscript. All authors read and approved the manuscript.

Compliance with ethical standards

Conflict of interest

The authors have no conflict of interest.

References

  1. Andrade RJ, Lacourpaille L, Freitas SR, McNair PJ, Nordez A (2016) Effects of hip and head position on ankle range of motion, ankle passive torque, and passive gastrocnemius tension. Scand J Med Sci Sports 26(1):41–47CrossRefPubMedGoogle Scholar
  2. Ates F, Temelli Y, Yucesoy CA (2014) Intrapoerative experiments show relevance of inter-antagonistic mechanical interaction for spastic muscle’s contribution to joint movement disorder. Clin Biomech 29(8):943–949CrossRefGoogle Scholar
  3. 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(4):396–409CrossRefPubMedGoogle Scholar
  4. Berthier C, Blaineau S (1997) Supramolecular organization of the subsarcolemmal cytoskeleton of adult skeletal muscle fibers. A review. Biol Cell 89(7):413–434CrossRefPubMedGoogle Scholar
  5. Bojsen-Moller J, Schwartz S, Kalliokoski KK, Finni T, Magnusson SP (2010) Intermuscular force transmission between human plantarflexor muscles in vivo. J Appl Physiol 109(6):1608–1618CrossRefPubMedGoogle Scholar
  6. Buchanan TS, Lloyd DG, Manal K, Besier TF (2004) Neuromusculoskeletal modeling: estimation of muscle forces and joint moments ans movements from measurements of neural command. J Appl Biomech 20(4):367–395CrossRefPubMedPubMedCentralGoogle Scholar
  7. Eby SF, Song P, Chen S, Chen Q, Greenleaf JF, An KN (2013) Validation of shear wave elastography in skeletal muscle. J Biomech 46(14):2381–2387CrossRefPubMedGoogle Scholar
  8. Finni T, Cronin NJ, Mayfield D, Lichtwark GA, Cresswell AG (2017) Effects of muscle activation on shear between human soleus and gastrocnemius muscles. Scand J Med Sci Sports 27(1):26–34CrossRefPubMedGoogle Scholar
  9. Gennisson JL, Catheline S, Chaffai S, Fink M (2003) Transient elastography in anisotropic medium: application to the measurement of slow and fast shear wave speeds in muscles. J Acoust Soc Am 114(1):536–541CrossRefPubMedGoogle Scholar
  10. Hirata K, Miyamoto-Mikami E, Kanehisa H, Miyamoto N (2016) Muscle-specific acute changes in passive stiffness of human triceps surae after stretching. Eur J Appl Physiol 116(5):911–918CrossRefPubMedGoogle Scholar
  11. Hoang PD, Gorman RB, Todd G, Gandevia SC, Herbert RD (2005) A new method for measuring passive length-tension properties of human gastrocnemius muscle in vivo. J Biomech 38(6):1333–1341CrossRefPubMedGoogle Scholar
  12. Hug F, Tucker K, Gennisson JL, Tanter M, Nordez A (2015) Elastography for muscle biomechanics: toward the estimation of individual muscle force. Exerc Sport Sci Rev 43(3):125–133CrossRefPubMedGoogle Scholar
  13. Huijing P (1999) Muscular force transmission: a unified, dual or multiple system? A review and some explorative experimental results. Arch Physiol Biochem 107(4):292–311PubMedGoogle Scholar
  14. Huijing PA (2009) Epimuscular myofascial force transmission: a historical review and implications for new research. International Society of Biomechanics Muybridge Award Lecture, Taipei, 2007. J Biomech 42(1):9–21CrossRefPubMedGoogle Scholar
  15. Huijing PA, Baan GC (2001) Extramuscular myofascial force transmission within the rat anterior distal compartment: proximo-distal differences in muscle force. Acta Physiol Scand 173(3):297–311CrossRefPubMedGoogle Scholar
  16. Huijing PA, van de Langenberg RW, Meesters JJ, Baan GC (2007) Extramuscular myofascial force transmission also occurs between synergistic muscles and antagonistic muscles. J Electromyogr Kinesiol 17(6):680–689.  https://doi.org/10.1016/j.jelekin.2007.02.005 CrossRefPubMedGoogle Scholar
  17. Huijing PA, Yaman A, Ozturk C, Yucesoy CA (2011) Effects of knee joint angle on global and local strains within human triceps surae muscle: MRI analysis indicating in vivo myofascial force transmission between synergistic muscles. Surg Radiol Anat 33(10):869–879CrossRefPubMedPubMedCentralGoogle Scholar
  18. Karakuzu A, Pamuk U, Ozturk C, Acar B, Yucesoy CA (2017) Magnetic resonance and diffusion tensor imaging analyses indicate heterogeneous strains along human medial gastrocnemius fascicles caused by submaximal plantar-flexion activity. J Biomech 57:69–78CrossRefPubMedGoogle Scholar
  19. Koo TK, Guo JY, Cohen JH, Parker KJ (2013) Relationship between shear elastic modulus and passive muscle force: an ex-vivo study. J Biomech 46(12):2053–2059.  https://doi.org/10.1016/j.jbiomech.2013.05.016 CrossRefPubMedGoogle Scholar
  20. Lacourpaille L, Hug F, Bouillard K, Hogrel JY, Nordez A (2012) Supersonic shear imaging provides a reliable measurement of resting muscle shear elastic modulus. Physiol Meas 33(3):N19–N28.  https://doi.org/10.1088/0967-3334/33/3/N19 CrossRefPubMedGoogle Scholar
  21. Le Sant G, Nordez A, Andrade R, Hug F, Freitas S, Gross R (2017) Stiffness mapping of lower leg muscles during passive dorsiflexion. J Anat 230(5):639–650CrossRefPubMedGoogle Scholar
  22. Maas H, Baan GC, Huijing PA (2001) Intermuscular interaction via myofascial force transmission: effects of tibialis anterior and extensor hallucis longus length on force transmission from rat extensor digitorum longus muscle. J Biomech 34(7):927–940CrossRefPubMedGoogle Scholar
  23. Maas H, Meijer HJ, Huijing PA (2005) Intermuscular interaction between synergists in rat originates from both intermuscular and extramuscular myofascial force transmission. Cells Tissues Organs 181(1):38–50CrossRefPubMedGoogle Scholar
  24. Maganaris CN (2004) Imaging-based estimates of moment arm length in intact human muscle-tendons. Eur J Appl Physiol 91(2–3):130–139CrossRefPubMedGoogle Scholar
  25. 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(6):978–984CrossRefPubMedGoogle Scholar
  26. McNair PJ, Dombroski EW, Hewson DJ, Stanley SN (2001) Stretching at the ankle joint: viscoelastic responses to holds and continuous passive motion. Med Sci Sports Exerc 33(3):354–358CrossRefPubMedGoogle Scholar
  27. Meijer HJ, Rijkelijkhuizen JM, Huijing PA (2007) Myofascial force transmission between antagonistic rat lower limb muscles: effects of single muscle or muscle group lengthening. J Electromyogr Kinesiol 17(6):698–707CrossRefPubMedGoogle Scholar
  28. Nordez A, Hug F (2010) Muscle shear elastic modulus measured using supersonic shear imaging is highly related to muscle activity level. J Appl Physiol (1985) 108(5):1389–1394CrossRefGoogle Scholar
  29. Nordez A, Foure A, Dombroski EW, Mariot JP, Cornu C, McNair PJ (2010) Improvements to Hoang et al.’s method for measuring passive length-tension properties of human gastrocnemius muscle in vivo. J Biomech 43(2):379–382CrossRefPubMedGoogle Scholar
  30. Pamuk U, Karakuzu A, Ozturk C, Acar B, Yucesoy CA (2016) Combined magnetic resonance and diffusion tensor imaging analyses provide a powerful tool for in vivo assessment of deformation along human muscle fibers. J Mech Behav Biomed Mat 63:207–219CrossRefGoogle Scholar
  31. Rijkelijkhuizen JM, Meijer HJ, Baan GC, Huijing PA (2007) Myofascial force transmission also occurs between antagonistic muscles located within opposite compartments of the rat lower hind limb. J Electromyogr Kinesiol 17(6):690–697CrossRefPubMedGoogle Scholar
  32. Standring S (2016) Gray’s anatomy: the anatomical basis of clinical practice. 41st edn. Elsevier Limited, New YorkGoogle Scholar
  33. Stecco C, Hammer WI (2015) Functional atlas of the human fascial system. Elsevier Ltd., EdinburghGoogle Scholar
  34. Street SF (1983) Lateral transmission of tension in frog myofibers: a myofibrillar network and transverse cytoskeletal connections are possible transmitters. J Cell Physiol 114(3):346–364CrossRefPubMedGoogle Scholar
  35. Tian M, Herbert RD, Hoang P, Gandevia SC, Bilston LE (2012) Myofascial force transmission between the human soleus and gastrocnemius muscles during passive knee motion. J Appl Physiol (1985) 113(4):517–523CrossRefGoogle Scholar
  36. Tijs C, van Dieen JH, Maas H (2015) No functionally relevant mechanical effects of epimuscular myofascial connections between rat ankle plantar flexors. J Exp Biol 218(Pt 18):2935–2941CrossRefPubMedGoogle Scholar
  37. Tijs C, van Dieen JH, Baan GC, Maas H (2016a) Synergistic co-activation increases the extent of mechanical interaction between rat ankle plantar-flexors. Front Physiol 7:414CrossRefPubMedPubMedCentralGoogle Scholar
  38. Tijs C, van Dieen JH, Maas H (2016b) Limited mechanical effects of intermuscular myofascial connections within the intact rat anterior crural compartment. J Biomech 49(13):2953–2959CrossRefPubMedGoogle Scholar
  39. Yaman A, Ozturk C, Huijing PA, Yucesoy CA (2013) Magnetic resonance imaging assessment of mechanical interactions between human lower leg muscles in vivo. J Biomech Eng 135(9):91003CrossRefPubMedGoogle Scholar
  40. Yucesoy CA (2010) Epimuscular myofascial force transmission implies novel principles for muscular mechanics. Exerc Sport Sci Rev 38:128–134CrossRefPubMedGoogle Scholar
  41. Yucesoy CA, Maas H, Koopman BH, Grootenboer HJ, Huijing PA (2006) Mechanisms causing effects of muscle position on proximo-distal muscle force differences in extra-muscular myofascial force transmission. Med Eng Phys 28(3):214–226CrossRefPubMedGoogle Scholar
  42. Yucesoy CA, Koopman BH, Grootenboer HJ, Huijing PA (2008) Extramuscular myofascial force transmission alters substantially the acute effects of surgical aponeurotomy: assessment by finite element modeling. Biomech Model Mechanobiol 7(3):175–189CrossRefPubMedGoogle Scholar
  43. Zajac FE (1989) Muscle and tendon: properties, models, scalin, and application to biomechanics and motor control. Crit Rev Biomed Eng 17(4):359–411PubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Laboratory “Movement, Interactions, Performance” (EA 4334), Faculty of Sport SciencesUniversité de Nantes, UFR STAPSNantesFrance
  2. 2.Institute of Biomedical EngineeringBogazici UniversityIstanbulTurkey
  3. 3.Universidade de Lisboa, Faculdade de Motricidade HumanaLisbonPortugal
  4. 4.Benfica LabSport Lisboa e BenficaLisbonPortugal
  5. 5.NHMRC Centre of Clinical Research Excellence in Spinal Pain, Injury and Health, School of Health and Rehabilitation SciencesThe University of QueenslandBrisbaneAustralia
  6. 6.Institut Universitaire de France (IUF)ParisFrance
  7. 7.Gait Analysis Laboratory, Physical and Rehabilitation Medicine DepartmentUniversity Hospital of NantesNantesFrance
  8. 8.Health and Rehabilitation Research Institute, Faculty of Health and Environmental SciencesAuckland University of TechnologyAucklandNew Zealand

Personalised recommendations