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Neuromuscular adaptations to wide-pulse high-frequency neuromuscular electrical stimulation training

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European Journal of Applied Physiology Aims and scope Submit manuscript

Abstract

Purpose

No studies have evaluated the potential benefits of wide-pulse high-frequency (WPHF) neuromuscular electrical stimulation (NMES) despite it being an interesting alternative to conventional NMES. Hence, this study evaluated neuromuscular adaptations induced by 3 weeks of WPHF NMES.

Methods

Ten young healthy individuals (training group) completed nine sessions of WPHF NMES training spread over 3 weeks, whereas seven individuals (control group) only performed the first and last sessions. Plantar flexor neuromuscular function (maximal voluntary contraction (MVC) force, voluntary activation level, H reflex, V wave, contractile properties) was evaluated before the first and last training sessions. Each training session consisted of ten 20-s WPHF NMES contractions (pulse duration: 1 ms, stimulation frequency: 100 Hz) interspaced by 40 s of recovery and delivered at an intensity set to initially evoke ~ 5% of MVC force. The averaged mean evoked forces produced during the ten WPHF NMES-evoked contractions of a given session as well as the sum of the ten contractions force time integral (total FTI) were computed.

Results

Total FTI (+ 118 ± 98%) and averaged mean evoked forces (+ 96 ± 91%) increased following the 3-week intervention (p < 0.05); no changes were observed in the control group. The intervention did not induce any change (p > 0.05) in parameters used to characterize plantar flexor neuromuscular function.

Conclusion

Three weeks of WPHF NMES increased electrically evoked forces but induced no other changes in plantar flexor neuromuscular properties. Before introducing WPHF NMES clinically, optimal training program characteristics (such as frequency, duration and intensity) remain to be identified.

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

AQAP:

Physical activity auto-questionnaire

EMG:

Electromyography

EMGmax :

Maximal electromyography activity recorded during a maximal voluntary contraction

FTI:

Force time integral

H max :

Maximal H-reflex amplitude

I Hmax :

Stimulation intensity required to evoke the maximal soleus H-reflex amplitude

I Mmax :

Stimulation intensity required to evoke maximal M-wave amplitude

IWPHF :

Stimulation intensity necessary to evoke a force corresponding to 5% of MVC force

M max :

Maximal M-wave amplitude

M sup :

Superimposed M-wave peak-to-peak amplitude

MVC:

Maximal voluntary contraction

NMES:

Neuromuscular electrical stimulation

PS10:

Supramaximal 10-Hz paired stimulation

PS100:

Supramaximal 100-Hz paired stimulation

RMSmax :

Maximal root mean square

SS:

Single stimulation

V/M sup :

Ratio between V-wave and superimposed M-wave peak-to-peak amplitudes

VAL:

Voluntary activation level

WPHF:

Wide-pulse high frequency

References

  • Aagaard P, Simonsen EB, Andersen JL, Magnusson P, Dyhre-Poulsen P (2002) Neural adaptation to resistance training: changes in evoked V-wave and H-reflex responses. J Appl Physiol 92(6):2309–2318

    Article  PubMed  Google Scholar 

  • Bergquist AJ, Clair JM, Lagerquist O, Mang CS, Okuma Y, Collins DF (2011) Neuromuscular electrical stimulation: implications of the electrically evoked sensory volley. Eur J Appl Physiol 111(10):2409–2426

    Article  CAS  PubMed  Google Scholar 

  • Bickel CS, Gregory CM, Dean JC (2011) Motor unit recruitment during neuromuscular electrical stimulation: a critical appraisal. Eur J Appl Physiol 111(10):2399–2407

    Article  PubMed  Google Scholar 

  • Burke D, Gorman E, Stokes D, Lennon O (2016) An evaluation of neuromuscular electrical stimulation in critical care using the ICF framework: a systematic review and meta-analysis. Clin Respir J 10(4):407–420

    Article  PubMed  Google Scholar 

  • Collins DF (2007) Central contributions to contractions evoked by tetanic neuromuscular electrical stimulation. Exerc Sport Sci Rev 35(3):102–109

    Article  PubMed  Google Scholar 

  • Collins DF, Burke D, Gandevia SC (2001) Large involuntary forces consistent with plateau-like behavior of human motoneurons. J Neurosci 21(11):4059–4065

    Article  CAS  PubMed  Google Scholar 

  • Collins DF, Burke D, Gandevia SC (2002) Sustained contractions produced by plateau-like behaviour in human motoneurones. J Physiol 538(Pt 1):289–301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dean JC, Yates LM, Collins DF (2007) Turning on the central contribution to contractions evoked by neuromuscular electrical stimulation. J Appl Physiol 103(1):170–176

    Article  CAS  PubMed  Google Scholar 

  • Delitto A, Strube MJ, Shulman AD, Minor SD (1992) A study of discomfort with electrical stimulation. Phys Ther 72(6):410–421

    Article  CAS  PubMed  Google Scholar 

  • Gondin J, Duclay J, Martin A (2006a) Neural drive preservation after detraining following neuromuscular electrical stimulation training. Neurosci Lett 409(3):210–214

    Article  CAS  PubMed  Google Scholar 

  • Gondin J, Duclay J, Martin A (2006b) Soleus- and gastrocnemii-evoked V-wave responses increase after neuromuscular electrical stimulation training. J Neurophysiol 95(6):3328–3335

    Article  PubMed  Google Scholar 

  • Gondin J, Guette M, Jubeau M, Ballay Y, Martin A (2006c) Central and peripheral contributions to fatigue after electrostimulation training. Med Sci Sports Exerc 38(6):1147–1156

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Grospretre S, Gueugneau N, Martin A, Lepers R (2017) Central contribution to electrically induced fatigue depends on stimulation frequency. Med Sci Sports Exerc 49(8):1530–1540

    Article  PubMed  Google Scholar 

  • Gueugneau N, Grospretre S, Stapley P, Lepers R (2017) High-frequency neuromuscular electrical stimulation modulates interhemispheric inhibition in healthy humans. J Neurophysiol 117(1):467–475

    Article  PubMed  Google Scholar 

  • Heckmann CJ, Gorassini MA, Bennett DJ (2005) Persistent inward currents in motoneuron dendrites: implications for motor output. Muscle Nerve 31(2):135–156

    Article  CAS  PubMed  Google Scholar 

  • Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G (2000) Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol 10(5):361–374

    Article  CAS  PubMed  Google Scholar 

  • Jubeau M, Zory R, Gondin J, Martin A, Maffiuletti NA (2006) Late neural adaptations to electrostimulation resistance training of the plantar flexor muscles. Eur J Appl Physiol 98(2):202–211

    Article  PubMed  Google Scholar 

  • Kiernan MC, Lin CS, Burke D (2004) Differences in activity-dependent hyperpolarization in human sensory and motor axons. J Physiol 558(Pt 1):341–349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kraemer WJ, Ratamess NA (2004) Fundamentals of resistance training: progression and exercise prescription. Med Sci Sports Exerc 36(4):674–688

    Article  PubMed  Google Scholar 

  • Maffiuletti NA (2010) Physiological and methodological considerations for the use of neuromuscular electrical stimulation. Eur J Appl Physiol 110(2):223–234

    Article  PubMed  Google Scholar 

  • Maffiuletti NA, Pensini M, Martin A (2002) Activation of human plantar flexor muscles increases after electromyostimulation training. J Appl Physiol 92(4):1383–1392

    Article  PubMed  Google Scholar 

  • Maffiuletti NA, Pensini M, Scaglioni G, Ferri A, Ballay Y, Martin A (2003) Effect of electromyostimulation training on soleus and gastrocnemii H- and T-reflex properties. Eur J Appl Physiol 90(5–6):601–607

    Article  PubMed  Google Scholar 

  • Maffiuletti NA, Roig M, Karatzanos E, Nanas S (2013) Neuromuscular electrical stimulation for preventing skeletal-muscle weakness and wasting in critically ill patients: a systematic review. BMC Med 11:137

    Article  PubMed  PubMed Central  Google Scholar 

  • Mang CS, Lagerquist O, Collins DF (2010) Changes in corticospinal excitability evoked by common peroneal nerve stimulation depend on stimulation frequency. Exp Brain Res 203(1):11–20

    Article  CAS  PubMed  Google Scholar 

  • Neyroud D, Dodd D, Gondin J, Maffiuletti NA, Kayser B, Place N (2014) Wide-pulse-high-frequency neuromuscular stimulation of triceps surae induces greater muscle fatigue compared with conventional stimulation. J Appl Physiol 116(10):1281–1289

    Article  PubMed  Google Scholar 

  • Neyroud D, Armand S, De Coulon G, Da Silva SR, Wegrzyk J, Gondin J, Kayser B, Place N (2016) Wide-pulse-high-frequency neuromuscular electrical stimulation in cerebral palsy. Clin Neurophysiol 127:1530–1539

    Article  CAS  PubMed  Google Scholar 

  • Neyroud D, Grospretre S, Gondin J, Kayser B, Place N (2018) “Test–retest reliability of wide-pulse high-frequency NMES evoked force”. Muscle Nerve 57:e70–e77

    Article  PubMed  Google Scholar 

  • Pichon F, Chatard JC, Martin A, Cometti G (1995) Electrical stimulation and swimming performance. Med Sci Sports Exerc 27(12):1671–1676

    Article  CAS  PubMed  Google Scholar 

  • Snyder-Mackler L, Delitto A, Stralka SW, Bailey SL (1994) Use of electrical stimulation to enhance recovery of quadriceps femoris muscle force production in patients following anterior cruciate ligament reconstruction. Phys Ther 74(10):901–907

    Article  CAS  PubMed  Google Scholar 

  • Strojnik V, Komi PV (1998) Neuromuscular fatigue after maximal stretch-shortening cycle exercise. J Appl Physiol 84(1):344–350

    Article  CAS  PubMed  Google Scholar 

  • Theurel J, Lepers R, Pardon L, Maffiuletti NA (2007) Differences in cardiorespiratory and neuromuscular responses between voluntary and stimulated contractions of the quadriceps femoris muscle. Respir Physiol Neurobiol 157(2–3):341–347

    Article  PubMed  Google Scholar 

  • Vanderthommen M, Duchateau J (2007) Electrical stimulation as a modality to improve performance of the neuromuscular system. Exerc Sport Sci Rev 35(4):180–185

    Article  PubMed  Google Scholar 

  • Veale JL, Mark RF, Rees S (1973) Differential sensitivity of motor and sensory fibres in human ulnar nerve. J Neurol Neurosurg Psychiatry 36(1):75–86

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vol S, Bedouet M, Gusto G, Leglu C, Beslin E, Decou P, Negre E, Planage B, Chazelle E, Mercier F, Lantieri O, Tichet J (2011) Evaluating physical activity: the AQAP questionnaire and its interpretation software. Ann Phys Rehabil Med 54(8):478–495

    Article  CAS  PubMed  Google Scholar 

  • Wegrzyk J, Foure A, Vilmen C, Ghattas B, Maffiuletti NA, Mattei JP, Place N, Bendahan D, Gondin J (2015) Extra forces induced by wide-pulse, high-frequency electrical stimulation: Occurrence, magnitude, variability and underlying mechanisms. Clin Neurophysiol 126:1400–1412

    Article  PubMed  Google Scholar 

  • Wegrzyk J, Ranjeva JP, Foure A, Kavounoudias A, Vilmen C, Mattei JP, Guye M, Maffiuletti NA, Place N, Bendahan D, Gondin J (2017) Specific brain activation patterns associated with two neuromuscular electrical stimulation protocols. Sci Rep 7(1):2742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank all the participants who took part in the experiments and Dr. Julien Gondin for his helpful comments on the manuscript.

Funding

The present work was supported by internal institutional funds.

Author information

Author notes

  1. Daria Neyroud

    Present address: Department of Physical Therapy, Institute of Myology, University of Florida, Gainesville, USA

  2. Bengt Kayser and Nicolas Place shared last authorship.

Authors and Affiliations

  1. Institute of Sport Sciences, Faculty of Biology and Medicine, University of Lausanne, Lausanne, Switzerland

    Daria Neyroud, Melina Gonzalez, Sarah Mueller, Daniel Agostino, Bengt Kayser & Nicolas Place

  2. EA4660-C3S Laboratory-Culture, Sport, Health and Society, Univ. Bourgogne Franche-Comté, Besançon, France

    Sidney Grosprêtre

  3. Human Performance Laboratory, Schulthess Clinic, Zurich, Switzerland

    Nicola A. Maffiuletti

Authors
  1. Daria Neyroud
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  2. Melina Gonzalez
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  3. Sarah Mueller
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  4. Daniel Agostino
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Contributions

DN and NP conceived and designed the experiment. DN, MG, SM, DA and NP conducted experiments. DN, MG, SM and DA took part in data analysis. All authors were involved in data interpretation. DN wrote the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Daria Neyroud.

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Conflict of interest

The authors declare no conflicts of interest.

Ethical statement

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Communicated by Philip D Chilibeck.

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Neyroud, D., Gonzalez, M., Mueller, S. et al. Neuromuscular adaptations to wide-pulse high-frequency neuromuscular electrical stimulation training. Eur J Appl Physiol 119, 1105–1116 (2019). https://doi.org/10.1007/s00421-019-04100-1

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