Combined effects of transcranial direct current stimulation (tDCS) and transcutaneous spinal direct current stimulation (tsDCS) on robot-assisted gait training in patients with chronic stroke: A pilot, double blind, randomized controlled trial

Restorative Neurology and Neuroscience

Volumn 33, Issue 3, 2015, Pages 357-368

  Picelli, Alessandro ^a   Chemello, Elena ^a   Castellazzi, Paola ^a   Roncari, Laura ^a   Waldner, Andreas ^b   Saltuari, Leopold ^c,d   Smania, Nicola ^a,e  

^a UNIVERSITY OF VERONA   (Italy)

^b Villa Melitta Rehabilitation Clinic   (Italy)

^c Hochzirl Hospital   (Austria)

^d Research Unit for Neurorehabilitation South Tyrol   (Italy)

^e UNIVERSITY HOSPITAL OF VERONA   (Italy)

Author keywords

brain; Central nervous system; rehabilitation; spinal cord

Indexed keywords

6 MINUTE WALK TEST; ADULT; ARTICLE; CEREBROVASCULAR ACCIDENT; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; FEMALE; FOLLOW UP; FUNCTION TEST; HUMAN; MALE; NERVE STIMULATION; NON INVASIVE PROCEDURE; PILOT STUDY; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; ROBOT ASSISTED GAIT TRAINING; ROBOTIC EXOSKELETON; SPASTICITY; STROKE PATIENT; TASK PERFORMANCE; TRAINING; TRANSCRANIAL DIRECT CURRENT STIMULATION; TRANSCUTANEOUS SPINAL DIRECT CURRENT STIMULATION; TREATMENT OUTCOME; AGED; BRAIN; CONVALESCENCE; GAIT; MIDDLE AGED; PATHOPHYSIOLOGY; PHYSIOLOGY; ROBOTICS; SPINAL CORD; STROKE; TRANSCUTANEOUS ELECTRICAL NERVE STIMULATION; WALKING;

AGED; BRAIN; DOUBLE-BLIND METHOD; FEMALE; GAIT; HUMANS; MALE; MIDDLE AGED; PILOT PROJECTS; RECOVERY OF FUNCTION; ROBOTICS; SPINAL CORD; STROKE; TRANSCRANIAL DIRECT CURRENT STIMULATION; TRANSCUTANEOUS ELECTRIC NERVE STIMULATION; TREATMENT OUTCOME; WALKING;

EID: 84937400132     PISSN: 09226028     EISSN: 18783627     Source Type: Journal    
DOI: 10.3233/RNN-140474     Document Type: Article

References (60)

1. Ambrus, G. G., Al-Moyed, H., Chaieb, L., Sarp, L., Antal, A., Paulus, W. (2012). The fade-in-Short stimulation-Fade out approach to sham tDCS-Reliable at 1mA for naïve and experienced subjects, but not investigators. Brain Stimul, 5(4), 499-504.
2. Aminoff, M., Boller, F., Swaab, D. (2009). Handbook of Clinical Neurology. Oxford: Elsevier.
3. Ashworth, B. (1964). Preliminary trial carisoprodal in multiple sclerosis. Practitioner, 192, 540-542.
4. Benjamini, Y., Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc Ser B, 57, 289-300.
5. Bradnam, L. V., Stinear, C. M., Barber, P. A., Byblow, W. D. (2012). Contralesional hemisphere control of the proximal paretic upper limb following stroke. Cerebr Cortex, 22(11), 2662-2671.
6. Bocci, T., Vannini, B., Torzini, A., Mazzatenta, A., Vergari, M., Cogiamanian, F., Priori, A. &Sartucci, F. (2014). Neurosci Lett, 578, 75-79.
7. Cha, H. K., Ji, S. G., Kim, M. K., Chang, J. S. (2014). Effect of transcranial direct current stimulation of function in patients with stroke. J Phys Ther Sci, 26(3), 363-365.
8. Cogiamanian, F., Ardolino, G., Vergari, M., Ferrucci, R., Ciocca, M., Scelzo, E., Barbieri, S., Priori, A. (2012). Transcutaneous spinal direct current stimulation. Front Psychiatry, 3, 63.
9. Cogiamanian, F., Vergari, M., Pulecchi, F., Marceglia, S., Priori, A. (2008). Effect of spinal transcutaneous direct current stimulation on somatosensory evoked potentials in humans. Clin Neurophysiol, 119(11), 2636-2640.
10. Cogiamanian, F., Vergari, M., Schiaffi, E., Marceglia, S., Ardolino, G., Barbieri, S., Priori, A. (2011). Transcutaneous spinal cord direct current stimulation inhibits the lower limb nociceptive flexion reflex in human beings. Pain, 152(2), 370-375.
11. Cohen, J. (1988). Statistical power analysis for the behavioral sciences, Lawrence Erlbaum, 2nd ed. Hillsdale. NJ.
12. Demeruisse, G., Demol, O., Robaye, E. (1980). Motor evaluation in vascular emiplegia. Eur Neurol, 19(6), 382-389.
13. Di Pino, G., Pellegrino, G., Assenza, G., Capone, F., Ferreri, F., Formica, D., Ranieri, F., Tombini, M., Ziemann, U., Rothwell, J. C., Di Lazzaro, V. (2014). Modulation of brain plasticity in stroke: A novel model for neurorehabilitation. Nat Rev Neurol, 10(10), 597-608.
14. Dietz, V. (2002). Do human bipeds use quadrupedal coordination? Trends Neurosci, 25(9), 462-467.
15. Dobkin, B. H., Firestine, A., West, M., Saremi, K., Woods, R. (2004). Ankle dorsiflexion as an fMRI paradigm to assay motor control for walking during rehabilitation. Neuroimage, 23(1), 370-381.
16. Dominici, N., Yvanenko, Y. P., Cappellini, G., d'Avella, A., Mondi, V., Cicchese, M., Fabiano, A., Silei, T., Di Paolo, A., Giannini, C., Poppele, R. E., Lacquaniti, F. (2011). Locomotor primitives in newborn babies and their development. Science, 334(6058), 997-999.
17. Duque, J., Murase, N., Celnik, P., Hummel, F., Harris-Love, M., Mazzocchio, R., Olivier, E., &Cohen, L. G. (2007). Intermanual differences in movement-related interhemispheric inhibition. J Cogn Neurosci, 19(2), 204-213.
18. Elsner, B., Kugler, J., Pohl, M., Merholz, J. (2013). Transcranial direct current stimulation (tDCS) for improving function and activities of daily living in patients after stroke. Cochrane Database Syst Rev, 11, CD009645.
19. Enright, P. L. (2003). The six-minute walk test. Respir Care, 48(8), 783-785.
20. Folstein, M. F., Folstein, S. E., McHugh, P. R. (1975). Mini-mental state: A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res, 12(3), 189-198.
21. Fregni, F., Boggio, P. S., Mansur, C. G., Wagner, T., Ferreira, M. J., Lima, M. C., Rigonatti, S. P., Marcolin, M. A., Freedman, S. D., Nitsche, M. A., &Pascual-Leone, A. (2005). Transcranial direct current stimulation of the unaffected hemisphere in stroke patients. Neuroreport, 16(14), 1551-1555.
22. Geroin, C., Mazzoleni, S., Smania, N., Gandolfi, M., Bonaiuti, D., Gasperini, G., Sale, P., Munari, D., Waldner, A., Spidalieri, R., Bovolenta, F., Picelli, A., Posteraro, F., Molteni, F., Franceschini, M., Italian Robotic Neurorehabilitation Research Group. (2013). Systematic review of outcome measures of walking training using electromechanical and robotic devices in patients with stroke. J Rehabil Med, 45(10), 987-996.
23. Geroin, C., Picelli, A., Munari, D., Waldner, A., Tomelleri, C., Smania, N. (2011). Combined transcranial direct current stimulation and robot-assisted gait training in patients with chronic stroke:Apreliminary comparison. Clin Rehabil, 25(6), 537-548.
24. Go, A. S., Mozaffarian, D., Roger, V. L., Benjamin, E. J., Berry, J. D., Blaha, M. J., Dai, S., Ford, E. S., Fox, C. S., Franco, S., Fullerton, H. J., Gillespie, C., Hailpern, S. M., Heit, J. A., Howard, V. J., Huffman, M. D., Judd, S. E., Kissela, B. M., Kittner, S. J., Lackland, D. T., Lichtman, J. H., Lisabeth, L. D., Mackey, R. H., Magid, D. J., Marcus, G. M., Marelli, A., Matchar, D. B., McGuire, D. K., Mohler, E. R., Moy, C. S., Mussolino, M. E., Neumar, R. W., Nichol, G., Pandey, D. K., Paynter, N. P., Reeves, M. J., Sorlie, P. D., Stein, J., Towfighi, A., Turan, T. N., Virani, S. S., Wong, N. D., Woo, D., Turner, M. B. (2014). Heart disease and stroke statistics-2014 update: A report from the American Heart Association. Circulation, 129(3), e28-e292.
25. Heide, A. C., Winkler, T., Helms, H. J., Nitsche, M. A., Trenkwalder, C., Paulus, W., Bachmann, C. G. (2014). Effects of transcutaneous spinal direct current stimulation in idiopathic restless legs patients. Brain Stimul, 7(5), 636-642.
26. Hesse, S., Tomelleri, C., Bardeleben, A., Werner, C., Waldner, A. (2012). Robot-assisted practice of gait and stair climbing in nonambulatory stroke patients. J Rehabil Res Dev, 49(4), 613-622.
27. Holden, M. K., Gill, K. M., Magliozzi, M. R. (1986). Gait assessment for neurologically impaired patients. Standards for outcome assessment. Phys Ther, 66(10), 1530-1539.
28. Hubli, M., Dietz, V., Schrafl-Altermatt, M., Bolliger, M. (2013). Modulation of spinal neuronal excitability by spinal direct currents and locomotion after spinal cord injury. Clin Neurophysiol, 124(6), 1187-1195.
29. Jayaram, G., &Stinear, J. W. (2009). The effects ofTranscranial stimulation on paretic lower limb motor excitability duringwalking. J Clin Neurophysiol, 26(4), 272-279.
30. Kitano, K., Koceja, D. M. (2009). Spinal reflex in human lower leg muscles evoked by transcutaneous spinal cord stimulation. J Neurosci Methods, 180(1), 111-115.
31. Kuys, S. S., Brauer, S. G., Ada, L. (2011). Test-retest reliability of the GAITRite system in people with stroke undergoing rehabilitation. Disabil Rehabil, 33(19-20), 1848-1853.
32. Lacquaniti, F., Ivanenko, Y. P., &Zago, M. (2012a). Patterned control of human locomotion. J Physiol, 590(10), 2189-2199.
33. Lacquaniti, F., Ivanenko, Y. P., Zago, M. (2012b). Development of human locomotion. Curr Opin Neurobiol, 22(5), 822-828.
34. Lamy, J. C., Ho, C., Badel, A., Arrigo, R. T., Boakye, M. (2012). Modulation of soleus H reflex by spinal DC stimulation in humans. J Neurophysiol, 108(3), 906-914.
35. Lefaucheur, J. P. (2009). Methods of therapeutic cortical stimulation. Neurophysiol Clin, 39(1), 1-14.
36. Liebetanz, D., Koch, R., Mayenfels, S., Konig, F., Paulus, W., Nitsche, M. A. (2009). Safety limits of cathodal transcranial direct current stimulation in rats. Clin Neurophysiol, 120(6), 1161-1167.
37. Mehrholz, J., Elsner, B., Werner, C., Kugler, J., Pohl, M. (2013). Electromechanical-assisted training for walking after stroke. Cochrane Database Syst Rev, 7, CD006185.
38. Mehrholz, J., Werner, C., Kugler, J., Pohl, M. (2007). Electromechanical-assisted training for walking after stroke. Cochrane Database Syst Rev, 4, CD006185.
39. Moreno-Duarte, I., Morse, L. R., Alam, M., Bikson, M., Zafonte, R., Fregni, F. (2014). Targeted therapies using electrical and magnetic neural stimulation for the treatment of chronic pain in spinal cord injury. Neuroimage, 85(3), 1003-1013.
40. Nitsche, M. A., Paulus, W. (2000). Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol, 527(3), 633-639.
41. Nitsche, M. A., Liebantz, D., Lang, N., Antal, A., Tergau, F., Paulus, W. (2003). Safety criteria for transcranial direct current stimulation (tDCS) in humans. Clin Neurophysiol, 114(11), 2220-2222.
42. Parazzini, M., Fiocchi, S., Liorni, I., Rossi, E., Cogiamanian, F., Vergari, M., Priori, A., Ravazzani, P. (2014). Modeling the current density generated by transcutaneous spinal direct current stimulation (tsDCS). Clin Neurophysiol, S1388-2457(14), 00173-00174.
43. Patrick, E., Ada, L. (2006). The Tardieu scale differentiates contracture from spasticity whereas the Ashworth scale is confounded by it. Clin Rehabil, 20(2), 173-182.
44. Perera, S., Mody, S. H., Woodman, R. C., Studenski, S. A. (2006). Meaningful change and responsiveness in common physical performance measures in older adults. J Am Geriatr Soc, 54(5), 743-749.
45. Petersen, T. H., Kliim-Due, M., Farmer, S. F., Nielsen, J. B. (2010). Childhood development of common drive to a human leg muscle during ankle dorsiflexion and gait. J Physiol, 588(22), 4387-4400.
46. Picelli, A., Bonetti, P., Fontana, C., Barausse, M., Dambruoso, F., Gajofatto, F., Girardi, P., Manca, M., Gimigliano, R., Smania, N. (2012). Is spastic muscle echo intensity related to the response to botulinum toxin type A in patients with stroke? A cohort study. Arch Phys Med Rehabil, 93(7), 1253-1258.
47. Picelli, A., Tamburin, S., Cavazza, S., Scampoli, C., Manca, M., Cosma, M., Berto, G., Vallies, G., Roncari, L., Melotti, C., Santilli, V., Smania, N. (2014). Relationship between ultrasonographic, electromyographic, and clinical parameters in adult stroke patients with spastic equinus: An observational study. Arch Phys Med Rehabil, 95(8), 1564-1570.
48. Priori, A., Ciocca, M., Parazzini, M., Vergari, M., Ferrucci, R. (2014). Transcranial cerebellar direct current stimulation and transcutaneous spinal cord direct current stimulation as innovative tools for neuroscientists. J Physiol, 592(16), 3345-3369.
49. Radman, T., Datta, A., Ramos, R. L., Brumberg, J. C., Bikson, M. (2009a). One-dimensional representation of a neuron in a uniform electric field. Conf Proc IEEE Eng Med Biol Soc, 2009, 6481-6484.
50. Radman, T., Ramos, R. L., Brumberg, J. C., Bikson, M. (2009b). Role of cortical cell type and morphology in sub-and suprathreshold uniform electric field stimulation. Brain Stimul, 2(4), 215-228.
51. Roche, N., Lackmy, A., Achache, V., Bussel, B., Katz, R. (2012). Effects of anodal tDCS on lumbar propriospinal system in healthy subjects. Clin Neurophysiol, 123(5), 1027-1034.
52. Sohn, M. K., Jee, S. J., Kim, Y. W. (2013). Effect of transcranial direct current stimulation on postural stability and lower extremity strength in hemiplegic stroke patients. Ann Rehabil Med, 37(6), 759-765.
53. Tahtis, V., Kaski, D., Seemungal, B. M. (2014). The effect of single session bi-cephalic transcranial direct current stimulation on gait performance in sub-acute stroke: A pilot study. Restor Neurol Neurosci, 32(4), 527-532.
54. Tanaka, S., Takeda, K., Otaka, Y., Kita, K., Osu, R., Honda, M., Sadato, N., Hanakawa, T., Watanabe, K. (2011). Single session of transcranial direct current stimulation transiently increases knee extensor force in patients with hemiparetic stroke. Neurorehabil Neural Repair, 25(6), 565-569.
55. Toshev, P. K., Guleyupoglu, B., &Bikson, M. (2014). Informing dose design by modeling transcutaneous spinal direct current stimulation. Clin Neurophysiol, S1388-2457(14), 00174-00176.
56. Traversa, R., Cicinelli, P., Pasqualetti, P., Filippi, M., &Rossini, P. M. (1998). Follow-up of interhemispheric differences of motor evoked potentials from the "affected" and "unaffected" hemisphere in human stroke. Brain Res, 803(1-2), 1-8.
57. Truini, A., Vergari, M., Biasiotta, A., La Cesa, S., Gabriele, M., Di Stefano, G., Cambieri, C., Cruccu, G., Inghilleri, M., Priori, A. (2011). Transcutaneous spinal direct current stimulation inhibits nociceptive spinal pathway conduction and increases pain tolerance in humans. Eur J Pain, 15(10), 1023-1027.
58. Veerbeek, J. M., Kwakkel, G., van Wegen, E. E., Ket, J. C., Heymans, M. W. (2011). Early prediction of outcome of activities of daily living after stroke: A systematic review. Stroke, 42(5), 1482-1488.
59. Winkler, T., Hering, P., Straube, A. (2010). Spinal DC stimulation in humans modulates post-activation depression of the H-reflex depending on current polarity. Clin Neurophysiol, 121(6), 957-961.
60. Yang, J. F., &Gorassini, M. (2006). Spinal and brain control of human walking: Implications for retraining ofwalking. Neuroscientist, 12(5), 379-389.