Skip to main content

Advertisement

Log in

Is the triple stimulation technique a better quantification tool of motor dysfunction than motor evoked potentials in multiple sclerosis?

  • Original Article
  • Published:
Acta Neurologica Belgica Aims and scope Submit manuscript

Abstract

The triple stimulation technique (TST) was rarely used in multiple sclerosis (MS). This study aimed to compare TST and motor evoked potentials (MEP) for the quantification of motor dysfunction. Central motor conduction based on MEP (four limbs) and TST (upper limbs) was assessed in 28 MS patients with a median Expanded Disability Status Scale (EDSS) of 4. EDSS, timed 25-foot walk (T25FW), grasping strength and motor components of the MS functional composite were evaluated. Regression analysis was used to assess the relationship between MEP, TST and clinical findings. TST was negatively correlated with EDSS (r = − 0.74, p < 0.0001) and to a lesser extent with T25FW (r = − 0.47, p < 0.05), and grasping strength (r = − 0.43, p < 0.05). A multiple regression analysis underlined the better correlation between clinical data and TST (R2 = 0.56, p < 0.0005) than with MEP (0.03 < R2 < 0.22, p > 0.05). This study evidenced the value of TST as a quantification tool of motor dysfunction. TST appeared to reflect a global disability since it was correlated not only to hand function but also to walking capacity.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Chen R, Cros D, Curra A, Di Lazzaro V, Lefaucheur JP, Magistris MR, Mills K, Rosler KM, Triggs WJ, Ugawa Y, Ziemann U (2008) The clinical diagnostic utility of transcranial magnetic stimulation: report of an IFCN committee. Clin Neurophysiol 119(3):504–532. https://doi.org/10.1016/j.clinph.2007.10.014

    Article  PubMed  Google Scholar 

  2. Fernandez V, Valls-Sole J, Relova JL, Raguer N, Miralles F, Dinca L, Taramundi S, Costa-Frossard L, Ferrandiz M, Ramio-Torrenta L, Villoslada P, Saiz A, Calles C, Antiguedad A, Alvarez-Cermeno JC, Prieto JM, Izquierdo G, Montalban X, Fernandez O (2013) Recommendations for the clinical use of motor evoked potentials in multiple sclerosis. Neurologia 28(7):408–416. https://doi.org/10.1016/j.nrl.2012.07.007

    Article  CAS  PubMed  Google Scholar 

  3. Hutchinson M (2013) Evoked potentials are of little use in the diagnosis or monitoring of MS: commentary. Mult Scler 19(14):1824–1825. https://doi.org/10.1177/1352458513506506

    Article  PubMed  Google Scholar 

  4. Zivadinov R, Leist TP (2005) Clinical-magnetic resonance imaging correlations in multiple sclerosis. J Neuroimaging 15(4 Suppl):10S–21S. https://doi.org/10.1177/1051228405283291

    Article  PubMed  Google Scholar 

  5. Ingram DA, Thompson AJ, Swash M (1988) Central motor conduction in multiple sclerosis: evaluation of abnormalities revealed by transcutaneous magnetic stimulation of the brain. J Neurol Neurosurg Psychiatry 51(4):487–494

    Article  CAS  Google Scholar 

  6. Kandler RH, Jarratt JA, Davies-Jones GA, Gumpert EJ, Venables GS, Sagar HJ, Zeman A (1991) The role of magnetic stimulation as a quantifier of motor disability in patients with multiple sclerosis. J Neurol Sci 106(1):31–34

    Article  CAS  Google Scholar 

  7. Facchetti D, Mai R, Micheli A, Marciano N, Capra R, Gasparotti R, Poloni M (1997) Motor evoked potentials and disability in secondary progressive multiple sclerosis. Can J Neurol Sci 24(4):332–337

    Article  CAS  Google Scholar 

  8. Gagliardo A, Galli F, Grippo A, Amantini A, Martinelli C, Amato MP, Borsini W (2007) Motor evoked potentials in multiple sclerosis patients without walking limitation: amplitude vs. conduction time abnormalities. J Neurol 254(2):220–227. https://doi.org/10.1007/s00415-006-0334-5

    Article  PubMed  Google Scholar 

  9. Kale N, Agaoglu J, Onder G, Tanik O (2009) Correlation between disability and transcranial magnetic stimulation abnormalities in patients with multiple sclerosis. J Clin Neurosci 16(11):1439–1442. https://doi.org/10.1016/j.jocn.2009.03.009

    Article  CAS  PubMed  Google Scholar 

  10. Hess CW, Mills KR, Murray NM, Schriefer TN (1987) Magnetic brain stimulation: central motor conduction studies in multiple sclerosis. Ann Neurol 22(6):744–752. https://doi.org/10.1002/ana.410220611

    Article  CAS  PubMed  Google Scholar 

  11. Kalkers NF, Strijers RL, Jasperse MM, Neacsu V, Geurts JJ, Barkhof F, Polman CH, Stam CJ (2007) Motor evoked potential: a reliable and objective measure to document the functional consequences of multiple sclerosis? Relation to disability and MRI. Clin Neurophysiol 118(6):1332–1340. https://doi.org/10.1016/j.clinph.2007.02.018

    Article  CAS  PubMed  Google Scholar 

  12. Humm AM, Magistris MR, Truffert A, Hess CW, Rosler KM (2003) Central motor conduction differs between acute relapsing-remitting and chronic progressive multiple sclerosis. Clin Neurophysiol 114(11):2196–2203

    Article  CAS  Google Scholar 

  13. Humm AM, Z’Graggen WJ, Buhler R, Magistris MR, Rosler KM (2006) Quantification of central motor conduction deficits in multiple sclerosis patients before and after treatment of acute exacerbation by methylprednisolone. J Neurol Neurosurg Psychiatry 77(3):345–350. https://doi.org/10.1136/jnnp.2005.065284

    Article  CAS  PubMed  Google Scholar 

  14. Comi G, Leocani L, Medaglini S, Locatelli T, Martinelli V, Santuccio G, Rossi P (1999) Evoked potentials in diagnosis and monitoring of multiple sclerosis. Electroencephalogr Clin Neurophysiol Suppl 49:13–18

    CAS  PubMed  Google Scholar 

  15. Filippi M, Charil A, Rovaris M, Absinta M, Rocca MA (2014) Insights from magnetic resonance imaging. Handb Clin Neurol 122:115–149. https://doi.org/10.1016/B978-0-444-52001-2.00006-6

    Article  PubMed  Google Scholar 

  16. Rosler KM, Petrow E, Mathis J, Aranyi Z, Hess CW, Magistris MR (2002) Effect of discharge desynchronization on the size of motor evoked potentials: an analysis. Clin Neurophysiol 113(11):1680–1687

    Article  Google Scholar 

  17. Magistris MR, Rosler KM, Truffert A, Myers JP (1998) Transcranial stimulation excites virtually all motor neurons supplying the target muscle. A demonstration and a method improving the study of motor evoked potentials. Brain 121(Pt 3):437–450

    Article  Google Scholar 

  18. Banach M, Rakowicz M (2010) Electrophysiological diagnosis of amyotrophic lateral sclerosis. Przegl Lek 67(9):736–740

    PubMed  Google Scholar 

  19. Xu Y, Zhang S, Fan D (2015) Upper motor neuron involvement in Kennedy disease evaluated by triple stimulation technique. Zhonghua Yi Xue Za Zhi 95(19):1522–1525

    CAS  PubMed  Google Scholar 

  20. Sakuma K, Adachi Y, Fukuda H, Kai T, Nakashima K (2005) Triple stimulation technique in patients with spinocerebellar ataxia type 6. Clin Neurophysiol 116(11):2586–2591. https://doi.org/10.1016/j.clinph.2005.04.015

    Article  PubMed  Google Scholar 

  21. Eusebio A, Azulay JP, Witjas T, Rico A, Attarian S (2007) Assessment of cortico-spinal tract impairment in multiple system atrophy using transcranial magnetic stimulation. Clin Neurophysiol 118(4):815–823. https://doi.org/10.1016/j.clinph.2007.01.004

    Article  CAS  PubMed  Google Scholar 

  22. Attarian S, Franques J, Elisabeth J, Trebuchon A, Duclos Y, Wybrecht D, Verschueren A, Salort-Campana E, Pouget J (2015) Triple-stimulation technique improves the diagnosis of chronic inflammatory demyelinating polyradiculoneuropathy. Muscle Nerve 51(4):541–548. https://doi.org/10.1002/mus.24352

    Article  PubMed  Google Scholar 

  23. Taieb G, Grapperon AM, Duclos Y, Franques J, Labauge P, Renard D, Yuki N, Attarian S (2015) Proximal conduction block in the pharyngeal-cervical-brachial variant of Guillain–Barre syndrome. Muscle Nerve 52(6):1102–1106. https://doi.org/10.1002/mus.24729

    Article  CAS  PubMed  Google Scholar 

  24. Humm AM, Z’Graggen WJ, von Hornstein NE, Magistris MR, Rosler KM (2004) Assessment of central motor conduction to intrinsic hand muscles using the triple stimulation technique: normal values and repeatability. Clin Neurophysiol 115(11):2558–2566. https://doi.org/10.1016/j.clinph.2004.06.009

    Article  CAS  PubMed  Google Scholar 

  25. Hofstadt-van Oy U, Keune PM, Muenssinger J, Hagenburger D, Oschmann P (2015) Normative data and long-term test–retest reliability of the triple stimulation technique (TST) in multiple sclerosis. Clin Neurophysiol 126(2):356–364. https://doi.org/10.1016/j.clinph.2014.05.032

    Article  CAS  PubMed  Google Scholar 

  26. Rosler KM, Scheidegger O, Magistris MR (2009) Corticospinal output and loss of force during motor fatigue. Exp Brain Res 197(2):111–123. https://doi.org/10.1007/s00221-009-1897-z

    Article  PubMed  Google Scholar 

  27. Scheidegger O, Kamm CP, Humpert SJ, Rosler KM (2012) Corticospinal output during muscular fatigue differs in multiple sclerosis patients compared to healthy controls. Mult Scler 18(10):1500–1506. https://doi.org/10.1177/1352458512438722

    Article  CAS  PubMed  Google Scholar 

  28. Humm AM, Beer S, Kool J, Magistris MR, Kesselring J, Rosler KM (2004) Quantification of Uhthoff’s phenomenon in multiple sclerosis: a magnetic stimulation study. Clin Neurophysiol 115(11):2493–2501. https://doi.org/10.1016/j.clinph.2004.06.010

    Article  CAS  PubMed  Google Scholar 

  29. Firmin L, Muller S, Rosler KM (2012) The latency distribution of motor evoked potentials in patients with multiple sclerosis. Clin Neurophysiol 123(12):2414–2421. https://doi.org/10.1016/j.clinph.2012.05.008

    Article  PubMed  Google Scholar 

  30. Magistris MR, Rosler KM, Truffert A, Landis T, Hess CW (1999) A clinical study of motor evoked potentials using a triple stimulation technique. Brain 122(Pt 2):265–279

    Article  Google Scholar 

  31. Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M, Fujihara K, Havrdova E, Hutchinson M, Kappos L, Lublin FD, Montalban X, O’Connor P, Sandberg-Wollheim M, Thompson AJ, Waubant E, Weinshenker B, Wolinsky JS (2011) Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol 69(2):292–302. https://doi.org/10.1002/ana.22366

    Article  PubMed  PubMed Central  Google Scholar 

  32. Fischer JS, Jack AJ, Kniker JE, Rudick RA, Cutter G (2001) Administration and scoring manual for multiple sclerosis functional composite (MSFC) (revised). National Multiple Sclerosis Society, New York

    Google Scholar 

  33. Roberts HC, Denison HJ, Martin HJ, Patel HP, Syddall H, Cooper C, Sayer AA (2011) A review of the measurement of grip strength in clinical and epidemiological studies: towards a standardised approach. Age Ageing 40(4):423–429. https://doi.org/10.1093/ageing/afr051

    Article  PubMed  Google Scholar 

  34. Buhler R, Magistris MR, Truffert A, Hess CW, Rosler KM (2001) The triple stimulation technique to study central motor conduction to the lower limbs. Clin Neurophysiol 112(5):938–949

    Article  CAS  Google Scholar 

  35. Magistris RM (2016) The triple stimulation technique: an advanced neurophysiological method to assess motor function in multiple sclerosis. J Mult Scler 3:3. https://doi.org/10.4172/2376-0389.1000188

    Article  Google Scholar 

  36. Fuhr P, Borggrefe-Chappuis A, Schindler C, Kappos L (2001) Visual and motor evoked potentials in the course of multiple sclerosis. Brain 124(Pt 11):2162–2168

    Article  CAS  Google Scholar 

  37. Schmierer K, Irlbacher K, Grosse P, Roricht S, Meyer BU (2002) Correlates of disability in multiple sclerosis detected by transcranial magnetic stimulation. Neurology 59(8):1218–1224

    Article  CAS  Google Scholar 

  38. Leocani L, Rovaris M, Boneschi FM, Medaglini S, Rossi P, Martinelli V, Amadio S, Comi G (2006) Multimodal evoked potentials to assess the evolution of multiple sclerosis: a longitudinal study. J Neurol Neurosurg Psychiatry 77(9):1030–1035. https://doi.org/10.1136/jnnp.2005.086280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. van der Kamp W, Maertens de Noordhout A, Thompson PD, Rothwell JC, Day BL, Marsden CD (1991) Correlation of phasic muscle strength and corticomotoneuron conduction time in multiple sclerosis. Ann Neurol 29(1):6–12. https://doi.org/10.1002/ana.410290104

    Article  PubMed  Google Scholar 

  40. Rocca MA, Horsfield MA, Sala S, Copetti M, Valsasina P, Mesaros S, Martinelli V, Caputo D, Stosic-Opincal T, Drulovic J, Comi G, Filippi M (2011) A multicenter assessment of cervical cord atrophy among MS clinical phenotypes. Neurology 76(24):2096–2102. https://doi.org/10.1212/WNL.0b013e31821f46b8

    Article  CAS  PubMed  Google Scholar 

  41. Boniface SJ, Mills KR, Schubert M (1991) Responses of single spinal motoneurons to magnetic brain stimulation in healthy subjects and patients with multiple sclerosis. Brain 114(Pt 1B):643–662

    Article  Google Scholar 

  42. Giffroy X, Maes N, Albert A, Maquet P, Crielaard JM, Dive D (2016) Multimodal evoked potentials for functional quantification and prognosis in multiple sclerosis. BMC Neurol 16:83. https://doi.org/10.1186/s12883-016-0608-1

    Article  PubMed  PubMed Central  Google Scholar 

  43. Giffroy X, Maes N, Albert A, Maquet P, Crielaard JM, Dive D, Humm AM (2016) Do evoked potentials contribute to the functional follow-up and clinical prognosis of multiple sclerosis? Acta Neurol Belg. https://doi.org/10.1007/s13760-016-0650-1

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank the patients who participated in this study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xavier Giffroy.

Ethics declarations

Conflict of interest

The authors of this study declare that they have no conflict of interest.

Ethical approval

All procedures performed in this study 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.

Informed consent

All patients gave their written informed consent.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Giffroy, X., Dive, D., Kaux, JF. et al. Is the triple stimulation technique a better quantification tool of motor dysfunction than motor evoked potentials in multiple sclerosis?. Acta Neurol Belg 119, 47–54 (2019). https://doi.org/10.1007/s13760-018-1001-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13760-018-1001-1

Keywords

Navigation