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Comparison of electrical nerve stimulation, electrical muscle stimulation and magnetic nerve stimulation to assess the neuromuscular function of the plantar flexor muscles

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Abstract

Introduction

As it might lead to less discomfort, magnetic nerve stimulation (MNS) is increasingly used as an alternative to electrical stimulation methods. Yet, MNS and electrical nerve stimulation (ENS) and electrical muscle stimulation (EMS) have not been formally compared for the evaluation of plantar flexor neuromuscular function.

Methods

We quantified plantar flexor neuromuscular function with ENS, EMS and MNS in 10 volunteers in fresh and fatigued muscles. Central alterations were assessed through changes in voluntary activation level (VAL) and peripheral function through changes in M-wave, twitch and doublet (PS100) amplitudes. Discomfort associated with 100-Hz paired stimuli delivered with each method was evaluated on a 10-cm visual analog scale.

Results

VAL, agonist and antagonist M-wave amplitudes and PS100 were similar between the different methods in both fresh and fatigued states. Potentiated peak twitch was lower in EMS compared to ENS, whereas no difference was found between ENS and MNS for any parameter. Discomfort associated with MNS (1.5 ± 1.4 cm) was significantly less compared to ENS (5.5 ± 1.9 cm) and EMS (4.2 ± 2.6 cm) (p < 0.05).

Conclusion

When PS100 is used to evaluate neuromuscular properties, MNS, EMS and ENS can be used interchangeably for plantar flexor neuromuscular function assessment as they provide similar evaluation of central and peripheral factors in unfatigued and fatigued states. Importantly, electrical current spread to antagonist muscles was similar between the three methods while discomfort from MNS was much less compared to ENS and EMS. MNS may be potentially employed to assess neuromuscular function of plantar flexor muscles in fragile populations.

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Abbreviations

EMG:

Electromyographic

EMS:

Electrical muscle stimulation

ENS:

Electrical nerve stimulation

GL:

Gastrocnemius lateralis

GM:

Gastrocnemius medialis

MNS:

Magnetic nerve stimulation

MVC:

Maximal voluntary contraction

PS10:

10-Hz paired stimuli

PS100:

100-Hz paired stimuli

Pt:

Peak twitch

SD:

Standard deviation

SE:

Standard error

SOL:

Soleus

TA:

Tibialis anterior

VAL:

Maximal voluntary activation level

References

  • Allen GM, Gandevia SC, McKenzie DK (1995) Reliability of measurements of muscle strength and voluntary activation using twitch interpolation. Muscle Nerve 18(6):593–600

    Article  CAS  PubMed  Google Scholar 

  • Andreassen CS, Jakobsen J, Ringgaard S, Ejskjaer N, Andersen H (2009) Accelerated atrophy of lower leg and foot muscles–a follow-up study of long-term diabetic polyneuropathy using magnetic resonance imaging (MRI). Diabetologia 52(6):1182–1191

    Article  CAS  PubMed  Google Scholar 

  • Bachasson D, Millet GY, Decorte N, Wuyam B, Levy P, Verges S (2013) Quadriceps function assessment using an incremental test and magnetic neurostimulation: a reliability study. J Electromyogr Kinesiol 23(3):649–658

    Article  PubMed  Google Scholar 

  • Barker AT (1991) An introduction to the basic principles of magnetic nerve stimulation. J Clin Neurophysiol 8(1):26–37

    Article  CAS  PubMed  Google Scholar 

  • Barker AT, Freeston IL, Jalinous R, Jarratt JA (1987) Magnetic stimulation of the human brain and peripheral nervous system: an introduction and the results of an initial clinical evaluation. Neurosurgery 20(1):100–109

    Article  CAS  PubMed  Google Scholar 

  • Brouwer B, Wheeldon R, Stradiotto-Parker N, Allum J (1998) Reflex excitability and isometric force production in cerebral palsy: the effect of serial casting. Dev Med Child Neurol 40:168–175

    Article  CAS  PubMed  Google Scholar 

  • Burke D (2002) Effects of activity on axonal excitability: implications for motor control studies. Adv Exp Med Biol 508:33–37

    PubMed  Google Scholar 

  • Button DC, Behm DG (2008) The effect of stimulus anticipation on the interpolated twitch technique. J Sports Sci Med 7:520–524

    PubMed Central  PubMed  Google Scholar 

  • Cresswell AG, Loscher WN, Thorstensson A (1995) Influence of gastrocnemius muscle length on triceps surae torque development and electromyographic activity in man. Exp Brain Res 105(2):283–290

    Article  CAS  PubMed  Google Scholar 

  • Elias LJ, Bryden MP, Bulman-Fleming MB (1998) Footedness is a better predictor than is handedness of emotional lateralization. Neuropsychologia 36(1):37–43

    Article  CAS  PubMed  Google Scholar 

  • Gandevia SC (2001) Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81(4):1725–1789

    CAS  PubMed  Google Scholar 

  • Gaudreault N, Gravel D, Nadeau S (2009) Evaluation of plantar flexion contracture contribution during the gait of children with Duchenne muscular dystrophy. J Electromyogr Kinesiol 19(3):e180–e186

    Article  PubMed  Google Scholar 

  • Han TR, Shin HI, Kim IS (2006) Magnetic stimulation of the quadriceps femoris muscle: comparison of pain with electrical stimulation. Am J Phys Med Rehabil 85(7):593–599

    Article  PubMed  Google Scholar 

  • Harris ML, Luo YM, Watson AC, Rafferty GF, Polkey MI, Green M, Moxham J (2000) Adductor pollicis twitch tension assessed by magnetic stimulation of the ulnar nerve. Am J Respir Crit Care Med 162(1):240–245

    Article  CAS  PubMed  Google Scholar 

  • Kernell D, Monster AW (1982a) Time course and properties of late adaptation in spinal motoneurones of the cat. Exp Brain Res 46(2):191–196

    Article  CAS  PubMed  Google Scholar 

  • Kernell D, Monster AW (1982b) Motoneurone properties and motor fatigue. An intracellular study of gastrocnemius motoneurones of the cat. Exp Brain Res 46(2):197–204

    Article  CAS  PubMed  Google Scholar 

  • Kremenic IJ, Glace BW, Ben-Avi SS, Nicholas SJ, McHugh MP (2009) Central fatigue after cycling evaluated using peripheral magnetic stimulation. Med Sci Sports Exerc 41(7):1461–1466

    Article  PubMed  Google Scholar 

  • Laghi F, Harrison MJ, Tobin MJ (1996) Comparison of magnetic and electrical phrenic nerve stimulation in assessment of diaphragmatic contractility. J Appl Physiol 80(5):1731–1742

    CAS  PubMed  Google Scholar 

  • Man WD, Moxham J, Polkey MI (2004) Magnetic stimulation for the measurement of respiratory and skeletal muscle function. Eur Respir J 24(5):846–860

    Article  PubMed  Google Scholar 

  • Martin V, Millet GY, Martin A, Deley G, Lattier G (2004) Assessment of low-frequency fatigue with two methods of electrical stimulation. J Appl Physiol 97(5):1923–1929

    Article  CAS  PubMed  Google Scholar 

  • Millet GY, Martin V, Martin A, Vergès S (2011) Electrical stimulation for testing neuromuscular function: from sport to pathology. Eur J Appl Physiol 111(10):2489–2500

    Article  PubMed  Google Scholar 

  • Millet GY, Bachasson D, Temesi J, Wuyam B, Feasson L, Verges S, Levy P (2012) Potential interests and limits of magnetic and electrical stimulation techniques to assess neuromuscular fatigue. Neuromuscul Disord 22(Suppl 3):S181–S186

    Article  PubMed  Google Scholar 

  • Neyroud D, Vallotton A, Millet GY, Kayser B, Place N (2014) The effect of muscle fatigue on stimulus intensity requirements for central and peripheral fatigue quantification. Eur J Appl Physiol 114(1):205–215

    Article  PubMed  Google Scholar 

  • Place N, Maffiuletti NA, Martin A, Lepers R (2007) Assessment of the reliability of central and peripheral fatigue after sustained maximal voluntary contraction of the quadriceps muscle. Muscle Nerve 35(4):486–495

    Article  PubMed  Google Scholar 

  • Place N, Duclay J, Lepers R, Martin A (2009) Unchanged H-reflex during a sustained isometric submaximal plantar flexion performed with an EMG biofeedback. J Electromyogr Kinesiol 19(6):395–402

    Article  Google Scholar 

  • Place N, Casartelli N, Glatthorn JF, Maffiuletti NA (2010) Comparison of quadriceps inactivation between nerve and muscle stimulation. Muscle Nerve 42(6):894–900

    Article  PubMed  Google Scholar 

  • Polkey MI, Kyroussis D, Hamnegard CH, Mills GH, Green M, Moxham J (1996) Quadriceps strength and fatigue assessed by magnetic stimulation of the femoral nerve in man. Muscle Nerve 19(5):549–555

    Article  CAS  PubMed  Google Scholar 

  • Polkey MI, Duguet A, Luo Y, Hughes PD, Hart N, Hamnegard CH, Green M, Similowski T, Moxham J (2000) Anterior magnetic phrenic nerve stimulation: laboratory and clinical evaluation. Intensive Care Med 26(8):1065–1075

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Falces J, Maffiuletti NA, Place N (2013a) Spatial distribution of motor units recruited during electrical stimulation of the quadriceps muscle versus the femoral nerve. Muscle Nerve 48(5):752–761

    Article  PubMed  Google Scholar 

  • Rodriguez-Falces J, Maffiuletti NA, Place N (2013b) Twitch and M-wave potentiation induced by intermittent maximal voluntary quadriceps contractions: differences between direct quadriceps and femoral nerve stimulation. Muscle Nerve 45:752–761

    Article  Google Scholar 

  • Rutherford OM, Jones DA, Newham DJ (1986) Clinical and experimental application of the percutaneous twitch superimposition technique for the study of human muscle activation. J Neurol Neurosurg Psychiatry 49(11):1288–1291

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Scaglioni G, Martin A (2009) Assessment of plantar flexors activation capacity: nerve versus muscle stimulation by single versus double pulse. Eur J Appl Physiol 106(4):563–572

    Article  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Swallow EB, Gosker HR, Ward KA, Moore AJ, Dayer MJ, Hopkinson NS, Schols AM, Moxham J, Polkey MI (2007) A novel technique for non volitional assessment of quadriceps muscle endurance in humans. J Appl Physiol 103(3):739–746

    Article  CAS  PubMed  Google Scholar 

  • Tomazin K, Verges S, Decorte N, Oulerich A, Maffiuletti NA, Millet GY (2011) Fat tissue alters quadriceps response to femoral nerve magnetic stimulation. Clin Neurophysiol 122(4):842–847

    Article  PubMed  Google Scholar 

  • Vagg R, Mogyoros I, Kiernan MC, Burke D (1998) Activity-dependent hyperpolarization of human motor axons produced by natural activity. J Physiol 507:919–925

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Verges S, Maffiuletti NA, Kerherve H, Decorte N, Wuyam B, Millet GY (2009) Comparison of electrical and magnetic stimulations to assess quadriceps muscle function. J Appl Physiol 106(2):701–710

    Article  PubMed  Google Scholar 

  • Vinci P, Perelli SL (2002) Footdrop, foot rotation, and plantar flexor failure in Charcot-Marie-Tooth disease. Arch Phys Med Rehabil 83(4):513–516

    Article  PubMed  Google Scholar 

  • Wiley ME, Damiano DL (1998) Lower-extremity strength profiles in spastic cerebral palsy. Dev Med Child Neurol 40(2):100–107

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to thank all the participants who took part in this study and Fabienne Crettaz von Roten for the helpful discussion on the statistical analyses. Daria Neyroud was supported by the Sir Jules Thorn Charitable Trust and John Temesi was supported by a doctoral research grant from the Rhône-Alpes Region.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standard

The study protocol was performed in accordance with the Declaration of Helsinki and approved by the Geneva University Hospital ethics committee (protocol 11–287). Before participation, each subject gave written informed consent. This study complied with the laws of Switzerland.

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Correspondence to Nicolas Place.

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Communicated by Toshio Moritani.

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Neyroud, D., Temesi, J., Millet, G.Y. et al. Comparison of electrical nerve stimulation, electrical muscle stimulation and magnetic nerve stimulation to assess the neuromuscular function of the plantar flexor muscles. Eur J Appl Physiol 115, 1429–1439 (2015). https://doi.org/10.1007/s00421-015-3124-x

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  • DOI: https://doi.org/10.1007/s00421-015-3124-x

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