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Int J Sports Med 2021; 42(07): 651-661
DOI: 10.1055/a-1270-7568
Orthopedics & Biomechanics

Achilles Tendon Adaptation to Neuromuscular Electrical Stimulation: Morphological and Mechanical Changes

Adrien Létocart
,
Jean-Francois Grosset
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Abstract

It remains unclear whether neuromuscular electrical stimulation can induce sufficient tendon stress to lead to tendon adaptations. Thus, we investigated the effect of such a training program on the triceps surae muscle following the morphological and mechanical properties of the Achilles tendon. Eight men participated in a 12-week high-frequency neuromuscular electrical stimulation training program of the triceps surae muscle under isometric conditions. Ultrasonography was used pre- and post-intervention to quantify cross-sectional area, free length, and total length of the Achilles tendon, as well as the myotendinous junction elongation during a maximal isometric ramp contraction under plantar flexion. Neuromuscular electrical stimulation training does not lead to changes in Achilles tendon free and total length, cross-sectional area, or maximal elongation capacity. However, a significant increase was evidenced in maximal tendon force post-training (+25.2%). Hence, Young’s Modulus and maximal stress were significantly greater after training (+12.4% and +23.4%, respectively). High-frequency neuromuscular electrical stimulation training induces repeated stress sufficient to lead to adaptations of mechanical properties of the Achilles tendon. Thus, this training technique may be of particular interest as a new rehabilitation method in tendinopathy management or to counteract the effect of hypo-activity.

Key words

neuromuscular electrical simulation - achilles tendon - triceps surae - training


Publication History

Received: 19 April 2020

Accepted: 18 September 2020

Article published online:
07 December 2020

© 2020. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Hortobágyi T, Maffiuletti N. a. Neural adaptations to electrical stimulation strength training. Eur J Appl Physiol 2011; 111: 2439-2449
    CrossrefPubMedGoogle Scholar
  • 2 Bohm S, Mersmann F, Arampatzis A. Human tendon adaptation in response to mechanical loading: A systematic review and meta-analysis of exercise intervention studies on healthy adults. Sports Med Open 2015; 1: 7
    CrossrefPubMedGoogle Scholar
  • 3 Arampatzis A, Karamanidis K, Mademli L. et al. Plasticity of the human tendon to short- and long-term mechanical loading. Exerc Sport Sci Rev 2009; 37: 66-72
    CrossrefPubMedGoogle Scholar
  • 4 Kubo K, Kanehisa H, Fukunaga T. et al. Effects of transient muscle contractions and stretching on the tendon structures in vivo. Acta Physiol Scand 2002; 175: 157-164
    CrossrefPubMedGoogle Scholar
  • 5 Arampatzis A, Peper A, Bierbaum S. et al. Plasticity of human Achilles tendon mechanical and morphological properties in response to cyclic strain. J Biomech 2010; 43: 3073-3079
    CrossrefPubMedGoogle Scholar
  • 6 Arampatzis A, Karamanidis K, Albracht K. Adaptational responses of the human Achilles tendon by modulation of the applied cyclic strain magnitude. J Exp Biol 2007; 210: 2743-2753
    CrossrefPubMedGoogle Scholar
  • 7 Kubo K, Morimoto M, Komuro T. et al. Effects of plyometric and weight training on muscle-tendon complex and jump performance. Med Sci Sports Exerc 2007; 39: 1801-1810
    CrossrefPubMedGoogle Scholar
  • 8 Maffiuletti NA, Pensini M, Martin A. Activation of human plantar flexor muscles increases after electromyostimulation training. J Appl Physiol (1985) 2002; 92: 1383-1392
    CrossrefPubMedGoogle Scholar
  • 9 Couppé C, Svensson RB, Silbernagel KG. et al. Eccentric or concentric exercises for the treatment of tendinopathies?. J Orthop Sports Phys Ther 2015; 45: 853-863
    CrossrefPubMedGoogle Scholar
  • 10 Gondin J, Guette M, Ballay Y. et al. Electromyostimulation training effects on neural drive and muscle architecture. Med Sci Sports Exerc 2005; 37: 1291-1299
    CrossrefPubMedGoogle Scholar
  • 11 Jubeau M, Zory R, Gondin J. et al. Late neural adaptations to electrostimulation resistance training of the plantar flexor muscles. Eur J Appl Physiol 2006; 98: 202-211
    CrossrefPubMedGoogle Scholar
  • 12 Grosset J-F, Canon F, Pérot C. et al. Changes in contractile and elastic properties of the triceps surae muscle induced by neuromuscular electrical stimulation training. Eur J Appl Physiol 2014; 114: 1403-1411
    CrossrefPubMedGoogle Scholar
  • 13 Harriss DJ, MacSween A, Atkinson G. Ethical standards in sport and exercise science research: 2020 update. Int J Sports Med 2019; 40: 813-817
    Article in Thieme ConnectPubMedGoogle Scholar
  • 14 Pearson SJ, Onambele GNL. Acute changes in knee-extensors torque, fiber pennation, and tendon characteristics. Chronobiol Int 2005; 22: 1013-1027
    CrossrefPubMedGoogle Scholar
  • 15 Onambele-Pearson NLG, Pearson SJ. Time-of-day effect on patella tendon stiffness alters vastus lateralis fascicle length but not the quadriceps force–angle relationship. J Biomech 2007; 40: 1031-1037
    CrossrefPubMedGoogle Scholar
  • 16 Gobbo M, Gaffurini P, Bissolotti L. et al. Transcutaneous neuromuscular electrical stimulation: influence of electrode positioning and stimulus amplitude settings on muscle response. Eur J Appl Physiol 2011; 111: 2451-2459
    CrossrefPubMedGoogle Scholar
  • 17 Gondin J, Brocca L, Bellinzona E. et al. Neuromuscular electrical stimulation training induces atypical adaptations of the human skeletal muscle phenotype: A functional and proteomic analysis. J Appl Physiol (1985) 2011; 110: 433-450
    CrossrefPubMedGoogle Scholar
  • 18 Lake DA. Neuromuscular Electrical Stimulation. Sports Med 1992; 13: 320-336
    CrossrefPubMedGoogle Scholar
  • 19 Berg HE, Tedner B, Tesch PA. Changes in lower limb muscle cross-sectional area and tissue fluid volume after transition from standing to supine. Acta Physiol Scand 1993; 148: 379-385
    CrossrefPubMedGoogle Scholar
  • 20 Morse CI, Thom JM, Birch KM. et al. Changes in triceps surae muscle architecture with sarcopenia. Acta Physiol Scand 2005; 183: 291-298
    CrossrefPubMedGoogle Scholar
  • 21 Kongsgaard M, Nielsen CH, Hegnsvad S. et al. Mechanical properties of the human Achilles tendon, in vivo. Clin Biomech 2011; 26: 772-777
    CrossrefPubMedGoogle Scholar
  • 22 Grosset JF, Mora I, Lambertz D. et al. Age-related changes in twitch properties of plantar flexor muscles in prepubertal children. Pediatr Res 2005; 58: 966-970
    CrossrefPubMedGoogle Scholar
  • 23 Hugon M. Methodology of the Hoffmann Reflex in Man. In: Human reflexes, pathophysiology of motor systems, methodology of human reflexes. S. Karger AG 1973; 277-293
    PubMedGoogle Scholar
  • 24 Hof AL, van den Berg J. Linearity between the weighted sum of the EMGs of the human triceps surae and the total torque. J Biomech 1977; 10: 529-539
    CrossrefPubMedGoogle Scholar
  • 25 Bojsen-Møller J, Hansen P, Aagaard P. et al. Differential displacement of the human soleus and medial gastrocnemius aponeuroses during isometric plantar flexor contractions in vivo. J Appl Physiol (1985) 2004; 97: 1908-1914
    CrossrefPubMedGoogle Scholar
  • 26 Magnusson SP, Aagaard P, Dyhre-Poulsen P. et al. Load-displacement properties of the human triceps surae aponeurosis in vivo. J Physiol 2001; 531: 277-288
    CrossrefPubMedGoogle Scholar
  • 27 Kubo K, Kawakami Y, Fukunaga T. Influence of elastic properties of tendon structures on jump performance in humans. J Appl Physiol (1985) 1999; 87: 2090-2096
    CrossrefPubMedGoogle Scholar
  • 28 Gondin J, Cozzone PJ, Bendahan D. Is high-frequency neuromuscular electrical stimulation a suitable tool for muscle performance improvement in both healthy humans and athletes?. Eur J Appl Physiol 2011; 111: 2473-2487
    CrossrefPubMedGoogle Scholar
  • 29 Maffiuletti NA. Physiological and methodological considerations for the use of neuromuscular electrical stimulation. Eur J Appl Physiol 2010; 110: 223-234
    CrossrefPubMedGoogle Scholar
  • 30 Henneman E. The size-principle: a deterministic output emerges from a set of probabilistic connections. J Exp Biol 1985; 115: 105-112
    CrossrefPubMedGoogle Scholar
  • 31 Maffiuletti Na, Minetto Ma, Farina D. et al. Electrical stimulation for neuromuscular testing and training: State-of-the art and unresolved issues. Eur J Appl Physiol 2011; 111: 2391-2397
    CrossrefPubMedGoogle Scholar
  • 32 Vaz MA, Baroni BM, Geremia JM. et al. Neuromuscular electrical stimulation (NMES) reduces structural and functional losses of quadriceps muscle and improves health status in patients with knee osteoarthritis. J Orthop Res 2013; 31: 511-516
    CrossrefPubMedGoogle Scholar
  • 33 Butterfield TA, Leonard TR, Herzog W. Differential serial sarcomere number adaptations in knee extensor muscles of rats is contraction type dependent. J Appl Physiol (1985) 2005; 99: 1352-1358
    CrossrefPubMedGoogle Scholar
  • 34 Bohm S, Mersmann F, Schroll A. et al. Insufficient accuracy of the ultrasound-based determination of Achilles tendon cross-sectional area. J Biomech 2016; 49: 2932-2937
    CrossrefPubMedGoogle Scholar
  • 35 Seynnes OR, de Boer M, Narici MV. Early skeletal muscle hypertrophy and architectural changes in response to high-intensity resistance training. J Appl Physiol (1985) 2007; 102: 368-373
    CrossrefPubMedGoogle Scholar
  • 36 Aagaard P, Simonsen EB, Andersen JL. et al. Increased rate of force development and neural drive of human skeletal muscle following resistance training. J Appl Physiol (1985) 2002; 93: 1318-1326
    CrossrefPubMedGoogle Scholar
  • 37 Kongsgaard M, Reitelseder S, Pedersen TG. et al. Region specific patellar tendon hypertrophy in humans following resistance training. Acta Physiol (Oxf) 2007; 191: 111-121
    CrossrefPubMedGoogle Scholar
  • 38 Seynnes OR, Erskine RM, Maganaris CN. et al. Training-induced changes in structural and mechanical properties of the patellar tendon are related to muscle hypertrophy but not to strength gains. J Appl Physiol (1985) 2009; 107: 523-530
    CrossrefPubMedGoogle Scholar
  • 39 Bohm S, Mersmann F, Tettke M. et al. Human Achilles tendon plasticity in response to cyclic strain: effect of rate and duration. J Exp Biol 2014; 217: 4010-4017
    PubMedGoogle Scholar
  • 40 Reeves ND, Maganaris CN, Narici MV. Effect of strength training on human patella tendon mechanical properties of older individuals. J Physiol 2003; 548: 971-981
    CrossrefPubMedGoogle Scholar
  • 41 Reeves ND, Narici MV, Maganaris CN. Strength training alters the viscoelastic properties of tendons in elderly humans. Muscle Nerve 2003; 28: 74-81
    CrossrefPubMedGoogle Scholar
  • 42 Carroll CC, Dickinson JM, LeMoine JK. et al. Influence of acetaminophen and ibuprofen on in vivo patellar tendon adaptations to knee extensor resistance exercise in older adults. J Appl Physiol (1985) 2011; 111: 508-515
    CrossrefPubMedGoogle Scholar
  • 43 Kubo K, Kanehisa H, Fukunaga T. Effects of resistance and stretching training programmes on the viscoelastic properties of human tendon structures in vivo. J Physiol 2002; 538: 219-226
    CrossrefPubMedGoogle Scholar
  • 44 Kubo K, Ikebukuro T, Yaeshima K. et al. Effects of static and dynamic training on the stiffness and blood volume of tendon in vivo. J Appl Physiol (1985) 2009; 106: 412-417
    CrossrefPubMedGoogle Scholar
  • 45 Kubo K, Komuro T, Ishiguro N. et al. Effects of low-load resistance training with vascular occlusion on the mechanical properties of muscle and tendon. J Appl Biomech 2006; 22: 112-119
    CrossrefPubMedGoogle Scholar
  • 46 McMahon GE, Morse CI, Burden A. et al. The manipulation of strain, when stress is controlled, modulates in vivo tendon mechanical properties but not systemic TGF-β1 levels. Physiol Rep 2013; 1: e00091
    CrossrefPubMedGoogle Scholar
  • 47 Onambele-Pearson GL, Pearson SJ. The magnitude and character of resistance-training-induced increase in tendon stiffness at old age is gender specific. Age (Dordr) 2012; 34: 427-438
    CrossrefPubMedGoogle Scholar