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Muscle and tendon stiffness assessment using the alpha method and ultrafast ultrasound

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Abstract

Purpose

The alpha method enables the dissociation of the passive (i.e., tendinous tissues) and active (i.e., fascicles) part of muscle–tendon stiffness. It is based on two main assumptions (i.e., a constant tendon stiffness and a muscle stiffness proportional to the torque produced), which have not been approved in vivo. The purpose of this study was to validate these two assumptions using ultrafast ultrasound, and to compare fascicle and tendon stiffness as determined by both methods.

Methods

Ten healthy males performed a fast-stretch experiment on the ankle plantar flexors. The mathematical model of the alpha method allowed to estimate the stiffness of muscle and tendinous tissues on the basis of the assumptions associated to the behaviors of muscle fascicles and tendinous tissues. Muscle and tendon stiffness of the gastrocnemius medialis were also calculated from ultrafast ultrasound measurements.

Results

Muscle stiffness measured by the ultrasound method increased from 217 ± 83 to 720 ± 265 N/mm with an increasing level of force (from 30 to 90 % MVC). Tendinous stiffness measured by the ultrasound method remained constant across the force level (P < 0.001). However, the stiffness values obtained with both methods were significantly different (P < 0.001).

Conclusions

In conclusion, these findings validate the two main assumptions underlying the alpha method using ultrasound. Differences in stiffness values obtained with alpha and ultrasound methods could be associated with physiological and geometrical differences between the whole plantar flexors muscles characterized by the alpha method and the gastrocnemius medialis assessed with the ultrasound method.

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Abbreviations

ANOVA:

Analysis of variance

L fh :

Horizontal fascicle length

MVC:

Maximal voluntary contraction

S :

Muscle-tendon stiffness

SEC:

Series elastic component

S muscle :

Muscle stiffness

S tendon :

Tendinous stiffness

ΔF :

Change in force

ΔL :

Muscle-tendon unit length change

ΔL fh :

Horizontal fascicle length change

ΔL tt :

Tendinous tissues length change

References

  • Albracht K, Arampatzis A, Baltzopoulos V (2008) Assessment of muscle volume and physiological cross-sectional area of the human triceps surae muscle in vivo. J Biomech 41(10):2211–2218. doi:10.1016/j.jbiomech.2008.04.020

    Article  CAS  PubMed  Google Scholar 

  • Arya S, Kulig K (2010) Tendinopathy alters mechanical and material properties of the Achilles tendon. J Appl Physiol 108:670–675. doi:10.1152/japplphysiol.00259.2009

    Article  PubMed  Google Scholar 

  • Bénard MR, Becher JG, Harlaar J, Huijing PA, Jaspers RT (2009) Anatomical information is needed in ultrasound imaging of muscle to avoid potentially substantial errors in measurement of muscle geometry. Muscle Nerve 39:652–665. doi:10.1002/mus.21287

    Article  PubMed  Google Scholar 

  • Blanpied P, Smidt GL (1992) Human plantarflexor stiffness to multiple single-stretch trials. J Biomech 25(1):29–39

  • Blanpied P, Smidt GL (1993) The difference in stiffness of the active plantarflexors between young and elderly human females. J Gerontol 48(2):M58–63

  • Carroll CC, Dickinson JM, Haus JM, Lee GA, Hollon CJ, Aagaard P, Magnusson SP, Trappe TA (2008) Influence of aging on the in vivo properties of human patellar tendon. J Appl Physiol 105(6):1907–1915. doi:10.1152/japplphysiol.00059.2008

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cook CS, McDonagh MJ (1996) Measurement of muscle and tendon stiffness in man. Eur J Appl Physiol Occup Physiol 72(4):380–382

    Article  CAS  PubMed  Google Scholar 

  • Cornu C, Almeida Silveira MI, Goubel F (1997) Influence of plyometric training on the mechanical impedance of the human ankle joint. Eur J Appl Physiol Occup Physiol 76(3):282–288

    Article  CAS  PubMed  Google Scholar 

  • Cornu C, Goubel F, Fardeau M (1998) Stiffness of knee extensors in Duchenne muscular dystrophy. Muscle Nerve 21(12):1772–1774

    Article  CAS  PubMed  Google Scholar 

  • Cronin NJ, Lichtwark G (2012) The use of ultrasound to study muscle-tendon function in human posture and locomotion. Gait Posture 37(3):305–312

    Article  PubMed  Google Scholar 

  • Cronin NJ, Carty CP, Barrett RS, Lichtwark G (2011) Automatic tracking of medial gastrocnemius fascicle length during human locomotion. J Appl Physiol 111:1491–1496. doi:10.1152/japplphysiol.00530.2011

    Article  PubMed  Google Scholar 

  • Deffieux T, Gennisson JL, Tanter M, Fink M, Nordez A (2006) Ultrafast imaging of in vivo muscle contraction using ultrasound. Appl Phys Lett 89:184107–184111. doi:10.1063/1.2378616

    Article  Google Scholar 

  • Deffieux T, Gennisson JL, Tanter M, Fink M (2008) Assessment of the mechanical properties of the musculoskeletal system using 2-D and 3-D very high frame rate ultrasound. IEEE Trans Ultrason Ferroelectr Freq Control 55:2177–2190. doi:10.1109/TUFFC.917

    Article  PubMed  Google Scholar 

  • Ettema GJ, Huijing PA (1994) Skeletal muscle stiffness in static and dynamic contractions. J Biomech 27(11):1361–1368

    Article  CAS  PubMed  Google Scholar 

  • Farcy S, Nordez A, Dorel S, Hauraix H, Portero P, Rabita G (2014) Interaction between gastrocnemius medialis fascicle and Achilles tendon compliance: a new insight on the quick-release method. J App Physiol 116(3):259–266. doi:10.1152/japplphysiol.00309.2013

    Article  Google Scholar 

  • Fletcher JR, Pfister TR, Macintosh BR (2013) Energy cost of running and Achilles tendon stiffness in man and woman trained runners. Physiol Rep 16(6):678–687. doi:10.1002/phy2.178

    Google Scholar 

  • Fouré A, Nordez A, Cornu C (2010) In vivo assessment of both active and passive parts of the plantarflexors series elastic component stiffness using the alpha method: a reliability study. Int J Sports Med 31(1):51–57. doi:10.1055/s-0029-1241210

    Article  PubMed  Google Scholar 

  • Fouré A, Nordez A, McNair P, Cornu C (2011) Effects of plyometric training on both active and passive parts of the plantarflexors series elastic component stiffness of muscle-tendon complex. Eur J Appl Physiol 111(3):539–548. doi:10.1007/s00421-010-1667-4

    Article  PubMed  Google Scholar 

  • Fouré A, Cornu C, McNair P, Nordez A (2012a) Gender differences in both active and passive parts of the plantar flexors series elastic component stiffness and geometrical parameters of the muscle-tendon complex. J Orthop Res 30(5):707–712. doi:10.1002/jor.21584

    Article  PubMed  Google Scholar 

  • Fouré A, Nordez A, Cornu C (2012b) Effects of plyometric training on passive stiffness of gastrocnemii muscles and Achilles tendon. Eur J Appl Physiol 112(2):2849–2857. doi:10.1007/s00421-011-2256-x

    Article  PubMed  Google Scholar 

  • Fouré A, Nordez A, Cornu C (2013) Effects of eccentric training on mechanical properties of the plantar flexor muscle-tendon complex. J Appl Physiol 114(5):523–537. doi:10.1152/japplphysiol.01313.2011

    Article  PubMed  Google Scholar 

  • Fukunaga T, Roy RR, Shellock FG, Hodgson JA, Edgerton VR (1996) Specific tension of human plantar flexors and dorsiflexors. J Appl Physiol 80(1):158–165

    CAS  PubMed  Google Scholar 

  • Gillett JG, Barrett RS, Lichtwark GA (2013) Reliability and accuracy of an automated tracking algorithm to measure controlled passive and active muscle fascicle length changes from ultrasound. Comput Methods Biomech Biomed Eng 16(6):678–687. doi:10.1080/10255842.2011.633516

    Article  Google Scholar 

  • Goubel F, Pertuzon E (1973) Evaluation of the elasticity of muscle in situ by the quick-release method. Arch Int Physiol Biochim 81(4):697–707

    Article  CAS  PubMed  Google Scholar 

  • Grieve D, Pheasant S, Cavanagh PR (1978) Prediction of gastrocnemius length from knee and ankle joint posture. In: Asmussen E, Jorgensen K (eds) Biomechanics VI-A. University Park Press, Baltimore, pp 405–412

    Google Scholar 

  • Hauraix H, Nordez A, Dorel S (2013) Shortening behavior of the different components of muscle-tendon unit during isokinetic plantar flexions. J Appl Physiol 115(7):1015–1024. doi:10.1152/japplphysiol.00247.2013

    Article  PubMed  Google Scholar 

  • Helland C, Bojsen-Møller J, Raastad T, Seynnes OR, Moltubakk MM, Jakobsen V, Visnes H, Bahr R (2013) Mechanical properties of the patellar tendon in elite volleyball players with and without patellar tendinopathy. Br J Sports Med 47(13):862–868. doi:10.1136/bjsports-2013-092275

    Article  PubMed  Google Scholar 

  • Kawakami Y, Ichinose Y, Fukunaga T (1998) Architectural and functional features of human triceps surae muscles during contraction. J Appl Physiol 85(2):398–404

    CAS  PubMed  Google Scholar 

  • Kongsgaard M, Nielsen CH, Hegnsvad S, Aagaard P, Magnusson SP (2011) Mechanical properties of the human Achilles tendon, in vivo. Clin Biomech 26(7):772–777. doi:10.1016/j.clinbiomech.2011.02.011

    Article  CAS  Google Scholar 

  • Kubo K, Kawakami Y, Fukunaga T (1999) Influence of elastic properties of tendon structures on jump performance in humans. J Appl Physiol 87(6):2090–2096

    CAS  PubMed  Google Scholar 

  • Kubo K, Morimoto M, Komuro T, Tsunoda N, Kanehisa H, Fukunaga T (2007) Influences of tendon stiffness, joint stiffness, and electromyographic activity on jump performances using single joint. Eur J Appl Physiol 99(3):235–243

    Article  PubMed  Google Scholar 

  • Kubo K, Tabata T, Ikebukuro T, Igarashi K, Yata H, Tsunoda N (2010) Effects of mechanical properties of muscle and tendon on performance in long distance runners. Eur J Appl Physiol 110(3):507–514. doi:10.1007/s00421-010-1528-1

    Article  PubMed  Google Scholar 

  • Lambertz D, Perot C, Kaspranski R, Goubel F (2001) Effects of long-term spaceflight on mechanical properties of muscles in humans. J Appl Physiol 90(1):179–188

    CAS  PubMed  Google Scholar 

  • Lenskjold A, Kongsgaard M, Larsen JO, Nielsen RH, Kovanen V, Aagaard P, Kjaer M, Magnusson SP (2013) The influence of physical activity during youth on structural and functional properties of the Achilles tendon. Scand J Med Sci Sports. doi:10.1111/sms.12143

    PubMed  Google Scholar 

  • Maganaris CN, Paul JP (1999) In vivo human tendon mechanical properties. J Physiol 521:307–313

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Magnusson SP, Aagaard P, Dyhre-Poulsen P, Kjaer M (2001) Load-displacement properties of the human triceps surae aponeurosis in vivo. J Physiol 531:277–288

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Magnusson SP, Narici MV, Maganaris CN, Kjaer M (2008) Human tendon behaviour and adaptation, in vivo. J Physiol 586(1):71–81

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Morgan DL (1977) Separation of active and passive components of short-range stiffness of muscle. Am J Physiol 232(1):45–49

    Google Scholar 

  • Morgan DL, Proske U, Warren D (1978) Measurements of muscle stiffness and the mechanism of elastic storage of energy in hopping kangaroos. J Physiol 282:253–261

  • Muraoka T, Muramatsu T, Fukunaga T, Kanehisa H (2004) Influence of tendon slack on electromechanical delay in the human medial gastrocnemius in vivo. J Appl Physiol 96(2):540–544

  • Nordez A, Gallot T, Catheline S, Guével A, Cornu C, Hug F (2009) Electromechanical delay revisited using very high frame rate ultrasound. J Appl Physiol 106(6):1970–1975. doi:10.1152/japplphysiol.00221.2009

    Article  PubMed  Google Scholar 

  • Pearson SJ, McMahon J (2012) Lower limb mechanical properties: determining factors and implications for performance. Sports Med 42(11):929–940. doi:10.2165/11635110-000000000-00000

    Article  PubMed  Google Scholar 

  • Peltonen J, Cronin NJ, Stenroth L, Finni T, Avela J (2013) Viscoelastic properties of the Achilles tendon in vivo. Springerplus 2(1):212

    Article  PubMed Central  PubMed  Google Scholar 

  • Proske U, Morgan DL (1987) Tendon stiffness: methods of measurement and significance for the control of movement. A review. J Biomech 20(1):75–82

    Article  CAS  PubMed  Google Scholar 

  • Rack PM, Westbury DR (1973) The short range stiffness of active mammalian muscle. J Physiol 229(1):16–17

    Google Scholar 

  • Rosager S, Aagaard P, Dyhre-Poulsen P, Neergaard K, Kjaer M, Magnusson SP (2002) Load-displacement properties of the human triceps surae aponeurosis and tendon in runners and non-runners. Scand J Med Sci Sports 12(2):90–98

    Article  CAS  PubMed  Google Scholar 

  • Seynnes OR, Bojsen-Møller J, Albracht K, Arndt A, Cronin NJ, Finni T, Magnusson SP (2015) Ultrasound-based testing of tendon mechanical properties: a critical evaluation. J Appl Physiol

  • Stenroth L, Peltonen J, Cronin NJ, Sipilä S, Finni T (2012) Age-related differences in Achilles tendon properties and triceps surae muscle architecture in vivo. J Appl Physiol 113:1537–1544. doi:10.1152/japplphysiol.00782.2012

    Article  PubMed  Google Scholar 

  • Svantesson U, Takahashi H, Carlsson U, Danielsson A, Sunnerhagen KS (2000) Muscle and tendon stiffness in patients with upper motor neuron lesion following a stroke. Eur J Appl Physiol 82(4):275–279

    Article  CAS  PubMed  Google Scholar 

  • Tanter M, Fink M (2014) Ultrafast Imaging in biomedical ultrasound. IEEE Trans Ultrason Ferroelectr Freq Control 61(1):102–119. doi:10.1109/TUFFC.2014.6689779

    Article  PubMed  Google Scholar 

  • Wilson GJ, Wood GA, Elliott BC (1991) Optimal stiffness of series elastic component in a stretch-shorten cycle activity. J Appl Physiol 70(2):825–833

    CAS  PubMed  Google Scholar 

  • Wu YK, Lien YH, Lin KH, Shih TT, Wang TG, Wang HK (2009) Relationships between three potentiation effects of plyometric training and performance. Scand J Med Sci Sports 20(1):80–86

  • Zee M, Voigt M (2001) Moment dependency of the series elastic stiffness in the human plantar flexors measured in vivo. J Biomech 34(11):1399–1406  

  • Zhao H, Ren Y, Wu Y, Liu SQ, Zhang L (2009) Ultrasonic evaluations of Achilles tendon mechanical properties poststroke. J Appl Physiol 106:843–849. doi:10.1152/japplphysiol.91212.2008

    Article  PubMed Central  PubMed  Google Scholar 

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Correspondence to Sylvain Dorel.

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Communicated by Olivier Seynnes.

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Hauraix, H., Fouré, A., Dorel, S. et al. Muscle and tendon stiffness assessment using the alpha method and ultrafast ultrasound. Eur J Appl Physiol 115, 1393–1400 (2015). https://doi.org/10.1007/s00421-015-3112-1

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  • DOI: https://doi.org/10.1007/s00421-015-3112-1

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