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.
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.
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.
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.
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Analysis of variance
Magnetic resonance imaging
Maximal voluntary contraction
Neuromuscular electrical stimulation
Immediately after the NMES session
Before the NMES session
- T 2 :
Transverse relaxation time
Visual analog scale
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
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
Armstrong RB (1984) Mechanisms of exercise-induced delayed onset muscular soreness: a brief review. Med Sci Sports Exerc 16(6):529–538
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
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
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
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
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
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
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
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
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
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
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
Gregory CM, Bickel CS (2005) Recruitment patterns in human skeletal muscle during electrical stimulation. Phys Ther 85(4):358–364
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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,
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
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
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
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
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
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
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.
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Communicated by Olivier Seynnes.
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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
- Muscle damage
- Acute exercise
- Neuromuscular electrical stimulation
- Muscle strength