Muscle alterations induced by electrostimulation are lower at short quadriceps femoris length

European Journal of Applied Physiology volume 120, pages325–335(2020)Cite this article

Abstract

Purpose

This study aimed at determining through MRI investigations, force and soreness assessments whether the modulation of muscle length is a relevant strategy for minimising neuromuscular electrical stimulation (NMES)-induced muscle damage in young healthy participants.

Methods

Comparison of 2 NMES sessions (40 isometric electrically-evoked contractions of the knee extensors) was randomly performed on 1 knee flexed at 50° (short muscle length) and the contralateral at 100° (long muscle length) in a single group of healthy participants. Indirect markers of muscle damage including changes in maximal voluntary isometric contraction (MVC) force, muscle volume and transverse relaxation time (T2) were measured before, 2 days (D2), 4 days (D4) and 7 days (D7) after the NMES sessions in each limb of the ten participants.

Results

Although stimulation intensity was similar during the NMES session on both limbs, significantly lower force production was recorded at long muscle length (peak at 30 ± 5% MVC force) as compared to short muscle length (peak at 61 ± 12% MVC force). In the following days, MVC force at long muscle length was decreased from D2 to D7, whereas no significant change occurred at short muscle length. Increases in muscle volume and T2 were found at each time point in stimulated muscles at long muscle length, whereas no change was found at short muscle length.

Conclusion

For the same stimulation intensity, NMES-induced isometric contractions generate higher knee extension force output and result in lower muscle tissues alterations that could be related to a lower intramuscular shear strain when exercise is performed at short muscle length.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant access to the full article PDF.

US$ 39.95

Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3

Abbreviations

ANOVA:

Analysis of variance

D2:

Day #2

D4:

Day #4

D7:

Day #7

MRI:

Magnetic resonance imaging

MVC:

Maximal voluntary contraction

NMES:

Neuromuscular electrical stimulation

POST:

Immediately after the NMES session

PRE:

Before the NMES session

RF:

rectus femoris

SAR:

sartorius

T 2 :

Transverse relaxation time

VAS:

Visual analog scale

VI:

vastus intermedius

VL:

vastus lateralis

VM:

vastus medialis

References

  1. Aldayel A, Jubeau M, McGuigan MR, Nosaka K (2010) Less indication of muscle damage in the second than initial electrical muscle stimulation bout consisting of isometric contractions of the knee extensors. Eur J Appl Physiol 108(4):709–717. https://doi.org/10.1007/s00421-009-1278-0

    Article  PubMed  Google Scholar 

  2. Allen TJ, Jones T, Tsay A, Morgan DL, Proske U (2018) Muscle damage produced by isometric contractions in human elbow flexors. J Appl Physiol 124(2):388–399. https://doi.org/10.1152/japplphysiol.00535.2017

    Article  PubMed  Google Scholar 

  3. Armstrong RB (1984) Mechanisms of exercise-induced delayed onset muscular soreness: a brief review. Med Sci Sports Exerc 16(6):529–538

    CAS  Article  Google Scholar 

  4. Brockett CL, Morgan DL, Gregory JE, Proske U (2002) Damage to different motor units from active lengthening of the medial gastrocnemius muscle of the cat. J Appl Physiol 92(3):1104–1110. https://doi.org/10.1152/japplphysiol.00479.2001

    CAS  Article  PubMed  Google Scholar 

  5. Chen X, Sanchez GN, Schnitzer MJ, Delp SL (2016) Changes in sarcomere lengths of the human vastus lateralis muscle with knee flexion measured using in vivo microendoscopy. J Biomech 49(13):2989–2994. https://doi.org/10.1016/j.jbiomech.2016.07.013

    Article  PubMed  PubMed Central  Google Scholar 

  6. Clarkson PM, Nosaka K, Braun B (1992) Muscle function after exercise-induced muscle damage and rapid adaptation. Med Sci Sports Exerc 24(5):512–520

    CAS  PubMed  Google Scholar 

  7. Crameri RM, Aagaard P, Qvortrup K, Langberg H, Olesen J, Kjaer M (2007) Myofibre damage in human skeletal muscle: effects of electrical stimulation versus voluntary contraction. J Physiol 583(Pt 1):365–380. https://doi.org/10.1113/jphysiol.2007.128827

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. Damas F, Libardi CA, Ugrinowitsch C (2018) The development of skeletal muscle hypertrophy through resistance training: the role of muscle damage and muscle protein synthesis. Eur J Appl Physiol 118(3):485–500. https://doi.org/10.1007/s00421-017-3792-9

    CAS  Article  PubMed  Google Scholar 

  9. Doguet V, Nosaka K, Guevel A, Ishimura K, Guilhem G, Jubeau M (2019) Influence of fascicle strain and corticospinal excitability during eccentric contractions on force loss. Exp Physiol 104(10):1532–1543. https://doi.org/10.1113/EP087664

    CAS  Article  PubMed  Google Scholar 

  10. Fouré A, Nosaka K, Wegrzyk J, Duhamel G, Le Troter A, Boudinet H, Mattei JP, Vilmen C, Jubeau M, Bendahan D, Gondin J (2014) Time course of central and peripheral alterations after isometric neuromuscular electrical stimulation-induced muscle damage. PLoS ONE 9(9):e107298. https://doi.org/10.1371/journal.pone.0107298

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. Fouré A, Duhamel G, Wegrzyk J, Boudinet H, Mattei JP, Le Troter A, Bendahan D, Gondin J (2015a) Heterogeneity of muscle damage induced by electrostimulation: a multimodal MRI study. Med Sci Sports Exerc 47(1):166–175. https://doi.org/10.1249/MSS.0000000000000397

    Article  PubMed  Google Scholar 

  12. Fouré A, Le Troter A, Guye M, Mattei JP, Bendahan D, Gondin J (2015b) Localization and quantification of intramuscular damage using statistical parametric mapping and skeletal muscle parcellation. Sci Rep 5:18580. https://doi.org/10.1038/srep18580

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. Fouré A, Le Troter A, Ogier AC, Guye M, Gondin J, Bendahan D (2019) Spatial difference can occur between activated and damaged muscle areas following electrically-induced isometric contractions. J Physiol 597(16):4227–4236. https://doi.org/10.1113/JP278205

    CAS  Article  PubMed  Google Scholar 

  14. Freitas SR, Antunes A, Salmon P, Mendes B, Firmino T, Cruz-Montecinos C, Cerda M, Vaz JR (2019) Does epimuscular myofascial force transmission occur between the human quadriceps muscles in vivo during passive stretching? J Biomech 83:91–96. https://doi.org/10.1016/j.jbiomech.2018.11.026

    Article  PubMed  Google Scholar 

  15. Gregory CM, Bickel CS (2005) Recruitment patterns in human skeletal muscle during electrical stimulation. Phys Ther 85(4):358–364

    Article  Google Scholar 

  16. Gregory JE, Morgan DL, Allen TJ, Proske U (2007) The shift in muscle's length-tension relation after exercise attributed to increased series compliance. Eur J Appl Physiol 99(4):431–441. https://doi.org/10.1007/s00421-006-0363-x

    CAS  Article  PubMed  Google Scholar 

  17. Guilhem G, Doguet V, Hauraix H, Lacourpaille L, Jubeau M, Nordez A, Dorel S (2016) Muscle force loss and soreness subsequent to maximal eccentric contractions depend on the amount of fascicle strain in vivo. Acta Physiol (Oxf) 217(2):152–163. https://doi.org/10.1111/apha.12654

    CAS  Article  Google Scholar 

  18. Hedayatpour N, Falla D (2012) Non-uniform muscle adaptations to eccentric exercise and the implications for training and sport. J Electromyogr Kinesiol 22(3):329–333. https://doi.org/10.1016/j.jelekin.2011.11.010

    Article  PubMed  Google Scholar 

  19. Herbert RD, Moseley AM, Butler JE, Gandevia SC (2002) Change in length of relaxed muscle fascicles and tendons with knee and ankle movement in humans. J Physiol 539(Pt 2):637–645. https://doi.org/10.1113/jphysiol.2001.012756

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. Herzog W, Abrahamse SK, ter Keurs HE (1990) Theoretical determination of force-length relations of intact human skeletal muscles using the cross-bridge model. Pflugers Arch 416(1–2):113–119

    CAS  Article  Google Scholar 

  21. Howell JN, Chleboun G, Conatser R (1993) Muscle stiffness, strength loss, swelling and soreness following exercise-induced injury in humans. J Physiol 464:183–196

    CAS  Article  Google Scholar 

  22. Jamurtas AZ, Theocharis V, Tofas T, Tsiokanos A, Yfanti C, Paschalis V, Koutedakis Y, Nosaka K (2005) Comparison between leg and arm eccentric exercises of the same relative intensity on indices of muscle damage. Eur J Appl Physiol 95(2–3):179–185. https://doi.org/10.1007/s00421-005-1345-0

    Article  PubMed  Google Scholar 

  23. Knapik JJ, Wright JE, Mawdsley RH, Braun J (1983) Isometric, isotonic, and isokinetic torque variations in four muscle groups through a range of joint motion. Phys Ther 63(6):938–947. https://doi.org/10.1093/ptj/63.6.938

    CAS  Article  PubMed  Google Scholar 

  24. Lacourpaille L, Nordez A, Hug F, Couturier A, Dibie C, Guilhem G (2014) Time-course effect of exercise-induced muscle damage on localized muscle mechanical properties assessed using elastography. Acta Physiol (Oxf) 211(1):135–146. https://doi.org/10.1111/apha.12272

    CAS  Article  Google Scholar 

  25. Lacourpaille L, Nordez A, Hug F, Doguet V, Andrade R, Guilhem G (2017) Early detection of exercise-induced muscle damage using elastography. Eur J Appl Physiol 117(10):2047–2056. https://doi.org/10.1007/s00421-017-3695-9

    Article  PubMed  Google Scholar 

  26. Lanza MB, Balshaw TG, Folland JP (2019) Is the joint-angle specificity of isometric resistance training real? And if so, does it have a neural basis? Eur J Appl Physiol. https://doi.org/10.1007/s00421-019-04229-z

    Article  PubMed  PubMed Central  Google Scholar 

  27. Lau WY, Blazevich AJ, Newton MJ, Wu SS, Nosaka K (2015) Assessment of muscle pain induced by elbow-flexor eccentric exercise. J Athl Train 50(11):1140–1148. https://doi.org/10.4085/1062-6050-50.11.05

    Article  PubMed  PubMed Central  Google Scholar 

  28. Lieber RL, Friden J (1993) Muscle damage is not a function of muscle force but active muscle strain. J Appl Physiol 74(2):520–526

    CAS  Article  Google Scholar 

  29. Maas H, Finni T (2018) Mechanical coupling between muscle-tendon units reduces peak stresses. Exerc Sport Sci Rev 46(1):26–33. https://doi.org/10.1249/JES.0000000000000132

    Article  PubMed  Google Scholar 

  30. Mackey AL, Bojsen-Moller J, Qvortrup K, Langberg H, Suetta C, Kalliokoski KK, Kjaer M, Magnusson SP (2008) Evidence of skeletal muscle damage following electrically stimulated isometric muscle contractions in humans. J Appl Physiol 105(5):1620–1627. https://doi.org/10.1152/japplphysiol.90952.2008

    Article  PubMed  Google Scholar 

  31. Mackey AL, Brandstetter S, Schjerling P, Bojsen-Moller J, Qvortrup K, Pedersen MM, Doessing S, Kjaer M, Magnusson SP, Langberg H (2011) Sequenced response of extracellular matrix deadhesion and fibrotic regulators after muscle damage is involved in protection against future injury in human skeletal muscle. FASEB J 25(6):1943–1959. https://doi.org/10.1096/fj.10-176487

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. Maffiuletti NA (2010) Physiological and methodological considerations for the use of neuromuscular electrical stimulation. Eur J Appl Physiol 110(2):223–234. https://doi.org/10.1007/s00421-010-1502-y

    Article  PubMed  Google Scholar 

  33. Marginson V, Eston R (2001) The relationship between torque and joint angle during knee extension in boys and men. J Sports Sci 19(11):875–880. https://doi.org/10.1080/026404101753113822

    CAS  Article  PubMed  Google Scholar 

  34. Morgan DL (1990) New insights into the behavior of muscle during active lengthening. Biophys J 57(2):209–221. https://doi.org/10.1016/S0006-3495(90)82524-8

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. Morgan DL, Proske U (2004) Popping sarcomere hypothesis explains stretch-induced muscle damage. Clin Exp Pharmacol Physiol 31(8):541–545. https://doi.org/10.1111/j.1440-1681.2004.04029.x

    CAS  Article  PubMed  Google Scholar 

  36. Nosaka K, Clarkson PM (1996) Changes in indicators of inflammation after eccentric exercise of the elbow flexors. Med Sci Sports Exerc 28(8):953–961

    CAS  Article  Google Scholar 

  37. Nosaka K, Newton M, Sacco P, Chapman D, Lavender A (2005) Partial protection against muscle damage by eccentric actions at short muscle lengths. Med Sci Sports Exerc 37(5):746–753

    Article  Google Scholar 

  38. Nosaka K, Aldayel A, Jubeau M, Chen TC (2011) Muscle damage induced by electrical stimulation. Eur J Appl Physiol 111(10):2427–2437. https://doi.org/10.1007/s00421-011-2086-x

    Article  PubMed  Google Scholar 

  39. Ogier A, Sdika M, Fouré A, Le Troter A, Bendahan D (2017) Individual muscle segmentation in MR Images: a 3D propagation through 2D non-linear registration approaches. Paper presented at the 39th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC’17), Jeju Island, Korea,

  40. 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 

  41. Saka T, Akova B, Yazici Z, Sekir U, Gur H, Ozarda Y (2009) Difference in the magnitude of muscle damage between elbow flexors and knee extensors eccentric exercises. J Sports Sci Med 8(1):107–115

    PubMed  PubMed Central  Google Scholar 

  42. Stubbs PW, Walsh LD, D'Souza A, Heroux ME, Bolsterlee B, Gandevia SC, Herbert RD (2018) History-dependence of muscle slack length following contraction and stretch in the human vastus lateralis. J Physiol 596(11):2121–2129. https://doi.org/10.1113/JP275527

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. Visser JJ, Hoogkamer JE, Bobbert MF, Huijing PA (1990) Length and moment arm of human leg muscles as a function of knee and hip-joint angles. Eur J Appl Physiol Occup Physiol 61(5–6):453–460

    CAS  Article  Google Scholar 

  44. Warren GL, Ingalls CP, Shah SJ, Armstrong RB (1999) Uncoupling of in vivo torque production from EMG in mouse muscles injured by eccentric contractions. J Physiol 515(Pt 2):609–619. https://doi.org/10.1111/j.1469-7793.1999.609ac.x

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  45. Xu J, Hug F, Fu SN (2018) Stiffness of individual quadriceps muscle assessed using ultrasound shear wave elastography during passive stretching. J Sport Health Sci 7(2):245–249. https://doi.org/10.1016/j.jshs.2016.07.001

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by the Centre National de la Recherche Scientifique (CNRS UMR 7339) and the Assistance Publique des Hôpitaux de Marseille (APHM). The authors thank all the subjects who participated in the present study.

Author information

Affiliations

  1. Aix Marseille Univ, CNRS, Centre de Résonance Magnétique Biologique et Médicale (CRMBM), UMR 7339, Faculté de Médecine de la Timone, 27 boulevard Jean Moulin, 13385, Marseille, France

    Alexandre Fouré, Maxime Guye, Julien Gondin & David Bendahan

  2. APHM, Hôpital Universitaire Timone, Centre d’Exploration Métabolique par Résonance Magnétique (CEMEREM), 13005, Marseille, France

    Alexandre Fouré & Maxime Guye

  3. Université de Lyon, Université Claude Bernard Lyon 1 (UCBL1), Laboratoire Interuniversitaire de Biologie de la Motricité (LIBM), EA 7424, 27-29 Boulevard du 11 Novembre 1918, Villeurbanne, 69622, France

    Alexandre Fouré

  4. Aix Marseille Univ, Université de Toulon, CNRS, Laboratoire d’Informatique & Systèmes (LIS), UMR 7020, 13385, Marseille, France

    Augustin C. Ogier

  5. Institut NeuroMyoGène (INMG), Univ Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5310, INSERM U1217, Faculté de Médecine et de Pharmacie, 8 avenue Rockefeller, Lyon, 69008, France

    Julien Gondin

Authors
  1. Alexandre Fouré
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Augustin C. Ogier
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maxime Guye
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Julien Gondin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. David Bendahan
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AF and JG conceived and designed research. AF conducted experiments. AF and ACO analysed the data. AF, JG, DB wrote the manuscript. All authors read and approved the manuscript.

Corresponding authors

Correspondence to Alexandre Fouré or Julien Gondin.

Ethics declarations

Conflict of interest

No conflicts of interest, financial or otherwise, are declared by the authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by Olivier Seynnes.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 36 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Fouré, A., Ogier, A.C., Guye, M. et al. Muscle alterations induced by electrostimulation are lower at short quadriceps femoris length. Eur J Appl Physiol 120, 325–335 (2020). https://doi.org/10.1007/s00421-019-04277-5

Download citation

Keywords

  • MRI
  • Muscle damage
  • Acute exercise
  • Neuromuscular electrical stimulation
  • Muscle strength
  • Thigh