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Experimental Brain Research

, Volume 234, Issue 12, pp 3447–3455 | Cite as

Placebo-controlled study of rTMS combined with Lokomat® gait training for treatment in subjects with motor incomplete spinal cord injury

  • Hatice KumruEmail author
  • Jesus Benito-Penalva
  • Josep Valls-Sole
  • Narda Murillo
  • Josep M. Tormos
  • Cecilia Flores
  • Joan Vidal
Research Article

Abstract

High-frequency rTMS combined with gait training improves lower extremity motor score (LEMS) and gait velocity in SCI subjects who are able to walk over ground. The aim of this study was to optimize the functional outcome in early phases of gait rehabilitation in SCI using rTMS as an additional treatment to physical therapy. The present study included 31 motor incomplete SCI subjects randomized to receive real or sham rTMS, just before Lokomat gait training (15 subjects for real, 16 for sham rTMS). rTMS consisted of one daily session for 20 days over vertex (at 20 Hz). The subjects were evaluated using modified Ashworth scale (MAS) for spasticity, upper and lower extremity motor score (UEMS and LEMS, respectively), ten meters walking test (10MWT) and Walking Index for SCI (WISCI-II) for gait at baseline, after last rTMS session, and during follow-up. UEMS and LEMS improved significantly after last session in both groups and during follow-up period. The improvement was greater in real than in sham rTMS group. At follow-up, 71.4 % of the subjects after real rTMS and 40 % of the subjects after sham rTMS could perform 10MWT without significant differences in gait velocity, cadence, step length and WISCI-II between both groups. We conclude that 20 sessions of daily high-frequency rTMS combined with Lokomat gait training can lead to clinical improvement of gait in motor incomplete SCI. Such combined treatment improved motor strength in lower extremity in incomplete SCI subjects and in upper extremity in those with cervical SCI.

Keywords

rTMS SCI Upper extremity Gait training Lokomat 

Notes

Acknowledgments

This research was supported in part by grants from Foundation La Marató TV3 PI110932 to HK, and PI122830 and from the Instituto de Salud Carlos III PI10/00442 to Joan Vidal.

References

  1. Barthélemy D, Grey JM, Nielsen JB, Bouyer L (2011) Involvement of the corticospinal tract in the control of human gait. Prog Brain Res 192:181–197CrossRefPubMedGoogle Scholar
  2. Belci M, Catley M, Husain M, Frankel HL, Davey NJ (2004) Magnetic brain stimulation can improve clinical outcome in incomplete spinal cord injured patients. Spinal Cord. 42:417–419CrossRefPubMedGoogle Scholar
  3. Benito J, Kumru H, Murillo N et al (2012) Motor and gait improvement in patients with incomplete spinal cord injury induced by high-frequency repetitive transcranial magnetic stimulation. Top Spinal Cord Inj Rehabil 18(2):106–112CrossRefPubMedGoogle Scholar
  4. Burns AS, Ditunno JF (2001) Establishing prognosis and maximizing functional outcomes after spinal cord injury: a review of current and future directions in rehabilitation management. Spine (Phila Pa 1976) 26:S137–S145 (Review)Google Scholar
  5. Butler AJ, Wolf SL (2007) Putting the brain on the map: use of transcranial magnetic stimulation to assess and induce cortical plasticity of upper-extremity movement. Phys Ther 87(6):719–736 (Review)Google Scholar
  6. Centonze D, Koch G, Versace V et al (2007) Repetitive transcranial magnetic stimulation of the motor cortex ameliorates spasticity in multiple sclerosis. Neurology 68:1045–1050CrossRefPubMedGoogle Scholar
  7. Cooke SF, Bliss TV (2006) Plasticity in the human central nervous system. Brain 129:1659–1673 (Review)Google Scholar
  8. Craven BC, Morris AR (2010) Modified Ashworth scale reliability for measurement of lower extremity spasticity among patients with SCI. Spinal Cord 48:207–213CrossRefPubMedGoogle Scholar
  9. Curt A, Van Hedel HJ, Klaus D, Dietz V (2008) EM-SCI Study Group. Recovery from a spinal cord injury: significance of compensation, neural plasticity, and repair. J Neurotrauma 25:677–685CrossRefPubMedGoogle Scholar
  10. Dimyan MA, Cohen LG (2010) Contribution of transcranial magnetic stimulation to the understanding of functional recovery mechanisms after stroke. Neurorehabil Neural Repair 24:125–135CrossRefPubMedGoogle Scholar
  11. Ditunno JF Jr, Barbeau H, Dobkin BH et al (2007) Validity of the walking scale for spinal cord injury and other domains of function in a multicenter clinical trial. Neurorehabil Neural Repair 21:539–550CrossRefPubMedPubMedCentralGoogle Scholar
  12. Dobkin BH (2000) Spinal and supraspinal plasticity after incomplete spinal cord injury: correlations between functional magnetic resonance imaging and engaged locomotor networks. Prog Brain Res 128:99–111CrossRefPubMedGoogle Scholar
  13. Dobkin B, Barbeau H, Deforge D et al (2007) The evolution of walking-related outcomes over the first 12 weeks of rehabilitation for incomplete traumatic spinal cord injury: the multicenter randomized Spinal Cord Injury Locomotor Trial. Neurorehabil Neural Repair 21:25–35CrossRefPubMedPubMedCentralGoogle Scholar
  14. Gomes-Osman J, Field-Fote EC (2015) Improvements in hand function in adults with chronic tetraplegia following a multiday 10-Hz repetitive transcranial magnetic stimulation intervention combined with repetitive task practice. J Neurol Phys Ther 39:23–30CrossRefPubMedPubMedCentralGoogle Scholar
  15. Hiscock A, Miller S, Rothwell J, Tallis RC, Pomeroy VM (2008) Informing dose-finding studies of repetitive transcranial magnetic stimulation to enhance motor function: a qualitative systematic review. Neurorehabil Neural Repair 22:228–249CrossRefPubMedGoogle Scholar
  16. Jorgensen HS, Nakayama H, Raaschou HO, Olsen TS (1995) Recovery of walking function in stroke patients: the Copenhagen Stroke Study. Arch Phys Med Rehabil 76:27–32CrossRefPubMedGoogle Scholar
  17. Kirshblum SC, O’Connor KC (1998) Predicting neurologic recovery in traumatic cervical spinal cord injury. Arch Phys Med Rehabil 79:1456–1466CrossRefPubMedGoogle Scholar
  18. Kirshblum SC, Burns SP, Biering-Sorensen F et al (2011) International standards for neurological classification of spinal cord injury (revised 2011). J Spinal Cord Med 34:535–546CrossRefPubMedPubMedCentralGoogle Scholar
  19. Kumru H, Murillo N, Samso JV et al (2010) Reduction of spasticity with repetitive transcranial magnetic stimulation in patients with spinal cord injury. Neurorehabil Neural Repair 24(5):435-441CrossRefPubMedPubMedCentralGoogle Scholar
  20. Kuppuswamy A, Balasubramaniam AV, Maksimovic R et al (2011) Action of 5 Hz repetitive transcranial magnetic stimulation on sensory, motor and autonomic function in human spinal cord injury. Clin Neurophysiol 122(12):2452–2461CrossRefPubMedGoogle Scholar
  21. Leuner B, Shors TJ (2004) New spines, new memories. Mol Neurobiol 29:117–130CrossRefPubMedPubMedCentralGoogle Scholar
  22. Lomarev MP, Kanchana S, Bara-Jimenez W, Iyer M, Wassermann EM, Hallett M (2006) Placebo-controlled study of rTMS for the treatment of Parkinson’s disease. Mov Disord 21:325–331CrossRefPubMedGoogle Scholar
  23. Lontis ER, Voigt M, Struijk JJ (2006) Focality assessment in transcranial magnetic stimulation with double and cone coils. J Clin Neurophysiol 23:462–471CrossRefPubMedGoogle Scholar
  24. MacKay-Lyons M (2002) Central pattern generation of locomotion: a review of the evidence. Phys Ther 82:69–83PubMedGoogle Scholar
  25. Martinez M, Delivet-Mongrain H, Leblond H, Rossignol S (2012) Incomplete spinal cord injury promotes durable functional changes within the spinal locomotor circuitry. J Neurophysiol 108:124–134CrossRefPubMedGoogle Scholar
  26. Matsuzaki M, Honkura N, Ellis-Davies GCR, Kasai H (2004) Structural basis of long-term potentiation in single dendritic spines. Nature 429:761–766CrossRefPubMedPubMedCentralGoogle Scholar
  27. Rossi S, Hallett M, Rossini PM, Pascual-Leone A (2009) Safety of TMS Consensus Group. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 120:2008–2039CrossRefPubMedPubMedCentralGoogle Scholar
  28. Rossier P, Wade DT (2001) Validity and reliability comparison of 4 mobility measures in patients presenting with neurologic impairment. Arch Phys Med Rehabil 82:9–13CrossRefPubMedGoogle Scholar
  29. Shik ML, Orlovsky GN (1976) Neurophysiology of locomotor automatism. Physiol Rev 56:465–501PubMedGoogle Scholar
  30. Siebner HR, Rothwell J (2003) Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp Brain Res 148:1–16CrossRefPubMedGoogle Scholar
  31. Takakusaki K (2008) Forebrain control of locomotor behaviors. Brain Res Rev 57:192–198CrossRefPubMedGoogle Scholar
  32. Waters R, Adkins R, Yakura J et al (1994) Prediction of ambulatory performance based on motor scores derived from standards of the American Spinal Injury Association. Arch Phys Med Rehabil 75:756–760CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Hatice Kumru
    • 1
    • 2
    • 3
    Email author
  • Jesus Benito-Penalva
    • 1
    • 2
    • 3
  • Josep Valls-Sole
    • 4
  • Narda Murillo
    • 1
    • 2
    • 3
  • Josep M. Tormos
    • 1
    • 2
    • 3
  • Cecilia Flores
    • 1
    • 2
    • 3
  • Joan Vidal
    • 1
    • 2
    • 3
  1. 1.Hospital de Neurorehabilitació, Institut Universitari de Neurorehabilitació adscrit a la UABFundación Institut GuttmannBadalonaSpain
  2. 2.Univ Autonoma de BarcelonaBellaterra, Cerdanyola del VallèsSpain
  3. 3.Fundació Institut d’Investigació en Ciències de la Salut Germans Trias i PujolBadalonaSpain
  4. 4.EMG unit, NeurologyHospital Clinic-BarcelonaBarcelonaSpain

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