A randomized sham-controlled trial on the effects of dual-tDCS "during" physical therapy on lower limb performance in sub-acute stroke and a comparison to the previous study using a "before" stimulation protocol

Wanalee Klomjai, Benchaporn Aneksan, Wanalee Klomjai, Benchaporn Aneksan

Abstract

Background: Dual-transcranial direct current stimulation (tDCS) has been used to rebalance the cortical excitability of both hemispheres following unilateral-stroke. Our previous study showed a positive effect from a single-session of dual-tDCS applied before physical therapy (PT) on lower limb performance. However, it is still undetermined if other timings of brain stimulation (i.e., during motor practice) induce better effects. The objective of this study was to examine the effect of a single-session of dual-tDCS "during" PT on lower limb performance in sub-acute stroke and then compare the results with our previous data using a "before" stimulation paradigm.

Method: For the current "during" protocol, 19 participants were participated in a randomized sham-controlled crossover trial. Dual-tDCS over the M1 of both cortices (2 mA) was applied during the first 20 min of PT. The Timed Up and Go and Five-Times-Sit-To-Stand tests were assessed at pre- and post-intervention and 1-week follow-up. Then, data from the current study were compared with those of the previous "before" study performed in a different group of 19 subjects. Both studies were compared by the difference of mean changes from the baseline.

Results: Dual-tDCS "during" PT and the sham group did not significantly improve lower limb performance. By comparing with the previous data, performance in the "before" group was significantly greater than in the "during" and sham groups at post-intervention, while at follow-up the "before" group had better improvement than sham, but not greater than the "during" group.

Conclusion: A single-session of dual-tDCS during PT induced no additional advantage on lower limb performance. The "before" group seemed to induce better acute effects; however, the benefits of the after-effects on motor learning for both stimulation protocols were probably not different. Trial registration Current randomized controlled trials was prospectively registered at the clinicaltrials.gov, registration number: NCT04051671. The date of registration was 09/08/2019.

Keywords: Dual-tDCS; Lower limb; Physical therapy; Stroke; Timing effect.

Conflict of interest statement

The authors declare that they have no competing interests.

© 2022. The Author(s).

Figures

Fig. 1
Fig. 1
Flowchart of study procedure of the present study
Fig. 2
Fig. 2
The column graph represents mean differences from baseline (PRE–POST) and (PRE–F/U) of FTSTS for each group. Vertical bars represent the standard error of the mean. Asterisks represent significant differences of P < 0.05 (*)
Fig. 3
Fig. 3
The column graph represents mean differences from baseline (PRE–POST) and (PRE–F/U) of TUG for each group. Vertical bars represent the standard error of the mean. ‬‬‬Asterisks represent significant differences of P < 0.05 (*)

References

    1. Stoykov ME, Madhavan S. Motor priming in neurorehabilitation. J Neurol Phys Ther. 2015;39(1):33–42. doi: 10.1097/NPT.0000000000000065.
    1. Nitsche MA, Paulus W. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol. 2000;527(Pt 3):633–639. doi: 10.1111/j.1469-7793.2000.t01-1-00633.x.
    1. Liebetanz D, Nitsche MA, Tergau F, Paulus W. Pharmacological approach to the mechanisms of transcranial DC-stimulation-induced after-effects of human motor cortex excitability. Brain. 2002;125(Pt 10):2238–2247. doi: 10.1093/brain/awf238.
    1. Delvaux V, Alagona G, Gérard P, De Pasqua V, Pennisi G, de Noordhout AM. Post-stroke reorganization of hand motor area: a 1-year prospective follow-up with focal transcranial magnetic stimulation. Clin Neurophysiol. 2003;114(7):1217–1225. doi: 10.1016/S1388-2457(03)00070-1.
    1. Traversa R, Cicinelli P, Pasqualetti P, Filippi M, Rossini PM. Follow-up of interhemispheric differences of motor evoked potentials from the “affected” and “unaffected” hemispheres in human stroke. Brain Res. 1998;803(1–2):1–8. doi: 10.1016/S0006-8993(98)00505-8.
    1. Orrù G, Conversano C, Hitchcott PK, Gemignani A. Motor stroke recovery after tDCS: a systematic review. Rev Neurosci. 2020;31(2):201–218. doi: 10.1515/revneuro-2019-0047.
    1. Lindenberg R, Nachtigall L, Meinzer M, Sieg MM, Flöel A. Differential effects of dual and unihemispheric motor cortex stimulation in older adults. J Neurosci. 2013;33(21):9176–9183. doi: 10.1523/JNEUROSCI.0055-13.2013.
    1. Klomjai W, Aneksan B, Pheungphrarattanatrai A, Chantanachai T, Choowong N, Bunleukhet S, et al. Effect of single-session dual-tDCS before physical therapy on lower-limb performance in sub-acute stroke patients: A randomized sham-controlled crossover study. Ann Phys Rehabil Med. 2018;61(5):286–291. doi: 10.1016/j.rehab.2018.04.005.
    1. Lindenberg R, Renga V, Zhu LL, Nair D, Schlaug G. Bihemispheric brain stimulation facilitates motor recovery in chronic stroke patients. Neurology. 2010;75(24):2176–2184. doi: 10.1212/WNL.0b013e318202013a.
    1. Waters-Metenier S, Husain M, Wiestler T, Diedrichsen J. Bihemispheric transcranial direct current stimulation enhances effector-independent representations of motor synergy and sequence learning. J Neurosci. 2014;34(3):1037–1050. doi: 10.1523/JNEUROSCI.2282-13.2014.
    1. Lefebvre S, Laloux P, Peeters A, Desfontaines P, Jamart J, Vandermeeren Y. Dual-tDCS enhances online motor skill learning and long-term retention in chronic stroke patients. Front Hum Neurosci. 2012;6:343.
    1. Lefebvre S, Thonnard J-L, Laloux P, Peeters A, Jamart J, Vandermeeren Y. Single session of dual-tDCS transiently improves precision grip and dexterity of the paretic hand after stroke. Neurorehabil Neural Repair. 2014;28(2):100–110. doi: 10.1177/1545968313478485.
    1. Feng W, Kautz SA, Schlaug G, Meinzer C, George MS, Chhatbar PY. Transcranial direct current stimulation for poststroke motor recovery: challenges and opportunities. PM R. 2018;10(9 Suppl 2):S157–S164. doi: 10.1016/j.pmrj.2018.04.012.
    1. Chhatbar PY, Ramakrishnan V, Kautz S, George MS, Adams RJ, Feng W. Transcranial direct current stimulation post-stroke upper extremity motor recovery studies exhibit a dose-response relationship. Brain Stimul. 2016;9(1):16–26. doi: 10.1016/j.brs.2015.09.002.
    1. Kang N, Summers JJ, Cauraugh JH. Transcranial direct current stimulation facilitates motor learning post-stroke: a systematic review and meta-analysis. J Neurol Neurosurg Psychiatry. 2016;87(4):345–355. doi: 10.1136/jnnp-2015-311242.
    1. Cabral ME, Baltar A, Borba R, Galvão S, Santos L, Fregni F, et al. Transcranial direct current stimulation: before, during, or after motor training? NeuroReport. 2015;26(11):618–622. doi: 10.1097/WNR.0000000000000397.
    1. Sriraman A, Oishi T, Madhavan S. Timing-dependent priming effects of tDCS on ankle motor skill learning. Brain Res. 2014;18(1581):23–29. doi: 10.1016/j.brainres.2014.07.021.
    1. Stagg CJ, Jayaram G, Pastor D, Kincses ZT, Matthews PM, Johansen-Berg H. Polarity and timing-dependent effects of transcranial direct current stimulation in explicit motor learning. Neuropsychologia. 2011;49(5):800–804. doi: 10.1016/j.neuropsychologia.2011.02.009.
    1. Jin M, Zhang Z, Bai Z, Fong KNK. Timing-dependent interaction effects of tDCS with mirror therapy on upper extremity motor recovery in patients with chronic stroke: a randomized controlled pilot study. J Neurol Sci. 2019;405:116436. doi: 10.1016/j.jns.2019.116436.
    1. Lefebvre S, Liew S-L. Anatomical parameters of tDCS to modulate the motor system after stroke: a review. Front Neurol. 2017;8:29. doi: 10.3389/fneur.2017.00029.
    1. Bai X, Guo Z, He L, Ren L, McClure MA, Mu Q. Different therapeutic effects of transcranial direct current stimulation on upper and lower limb recovery of stroke patients with motor dysfunction: a meta-analysis. Neural Plast. 2019 [cited 2020 Jul 16]; 2019. .
    1. Klomjai W, Lackmy-Vallée A, Roche N, Pradat-Diehl P, Marchand-Pauvert V, Katz R. Repetitive transcranial magnetic stimulation and transcranial direct current stimulation in motor rehabilitation after stroke: an update. Ann Phys Rehabil Med. 2015;58(4):220–224. doi: 10.1016/j.rehab.2015.05.006.
    1. Márquez-Ruiz J, Leal-Campanario R, Sánchez-Campusano R, Molaee-Ardekani B, Wendling F, Miranda PC, et al. Transcranial direct-current stimulation modulates synaptic mechanisms involved in associative learning in behaving rabbits. Proc Natl Acad Sci USA. 2012;109(17):6710–6715. doi: 10.1073/pnas.1121147109.
    1. Ammann C, Spampinato D, Márquez-Ruiz J. Modulating motor learning through transcranial direct-current stimulation: an integrative view. Front Psychol. 2016;23(7):1981.
    1. Hummel F, Celnik P, Giraux P, Floel A, Wu W-H, Gerloff C, et al. Effects of non-invasive cortical stimulation on skilled motor function in chronic stroke. Brain. 2005;128(3):490–499. doi: 10.1093/brain/awh369.
    1. Ng SS, Hui-Chan CW. The timed up & go test: its reliability and association with lower-limb impairments and locomotor capacities in people with chronic stroke. Arch Phys Med Rehabil. 2005;86(8):1641–1647. doi: 10.1016/j.apmr.2005.01.011.
    1. Mong Y, Teo TW, Ng SS. 5-repetition sit-to-stand test in subjects with chronic stroke: reliability and validity. Arch Phys Med Rehabil. 2010;91(3):407–413. doi: 10.1016/j.apmr.2009.10.030.
    1. Persson CU, Hansson P-O, Sunnerhagen KS. Clinical tests performed in acute stroke identify the risk of falling during the first year: postural stroke study in Gothenburg (POSTGOT) J Rehabil Med. 2011;43(4):348–353. doi: 10.2340/16501977-0677.
    1. Andersson AG, Kamwendo K, Seiger A, Appelros P. How to identify potential fallers in a stroke unit: validity indexes of 4 test methods. J Rehabil Med. 2006;38(3):186–191. doi: 10.1080/16501970500478023.
    1. Alghadir AH, Al-Eisa ES, Anwer S, Sarkar B. Reliability, validity, and responsiveness of three scales for measuring balance in patients with chronic stroke. BMC Neurol. 2018;18(1):141. doi: 10.1186/s12883-018-1146-9.
    1. de Melo TA, Duarte ACM, Bezerra TS, França F, Soares NS, Brito D. The five times sit-to-stand test: safety and reliability with older intensive care unit patients at discharge. Rev Bras Ter Intensiva. 2019;31(1):27–33. doi: 10.5935/0103-507X.20190006.
    1. Kwong PWH, Ng SSM, Chung RCK, Ng GYF. Foot placement and arm position affect the five times sit-to-stand test time of individuals with chronic stroke. Biomed Res Int. 2014 [cited 2020 Nov 14]; 2014. .
    1. Sage M, Middleton LE, Tang A, Sibley KM, Brooks D, McIlroy W. Validity of rating of perceived exertion ranges in individuals in the subacute stage of stroke recovery. Top Stroke Rehabil. 2013;20(6):519–527. doi: 10.1310/tsr2006-519.
    1. Chang MC, Kim DY, Park DH. Enhancement of cortical excitability and lower limb motor function in patients with stroke by transcranial direct current stimulation. Brain Stimul. 2015;8(3):561–566. doi: 10.1016/j.brs.2015.01.411.
    1. Tazoe T, Endoh T, Kitamura T, Ogata T. Polarity specific effects of transcranial direct current stimulation on interhemispheric inhibition. PLoS ONE. 2014;9(12):e114244. doi: 10.1371/journal.pone.0114244.
    1. Andrade SM, Ferreira JJA, Rufino TS, Medeiros G, Brito JD, da Silva MA, et al. Effects of different montages of transcranial direct current stimulation on the risk of falls and lower limb function after stroke. Neurol Res. 2017;39(12):1037–1043. doi: 10.1080/01616412.2017.1371473.
    1. Clark B, Whitall J, Kwakkel G, Mehrholz J, Ewings S, Burridge J. Time spent in rehabilitation and effect on measures of activity after stroke. Cochrane Database Syst Rev. 2017 [cited 2020 Jul 18];2017(3). .
    1. Miyaguchi S, Onishi H, Kojima S, Sugawara K, Tsubaki A, Kirimoto H, et al. Corticomotor excitability induced by anodal transcranial direct current stimulation with and without non-exhaustive movement. Brain Res. 2013;5(1529):83–91. doi: 10.1016/j.brainres.2013.07.026.
    1. Chye L, Nosaka K, Murray L, Edwards D, Thickbroom G. Corticomotor excitability of wrist flexor and extensor muscles during active and passive movement. Hum Mov Sci. 2010;29(4):494–501. doi: 10.1016/j.humov.2010.03.003.
    1. Coxon JP, Stinear JW, Byblow WD. Amplitude of muscle stretch modulates corticomotor gain during passive movement. Brain Res. 2005;1031(1):109–117. doi: 10.1016/j.brainres.2004.10.062.
    1. Lewis GN, Byblow WD, Carson RG. Phasic modulation of corticomotor excitability during passive movement of the upper limb: effects of movement frequency and muscle specificity. Brain Res. 2001;900(2):282–294. doi: 10.1016/S0006-8993(01)02369-1.
    1. Wiethoff S, Hamada M, Rothwell JC. Variability in response to transcranial direct current stimulation of the motor cortex. Brain Stimul. 2014;7(3):468–475. doi: 10.1016/j.brs.2014.02.003.
    1. Madhavan S, Weber KA, Stinear JW. Non-invasive brain stimulation enhances fine motor control of the hemiparetic ankle: implications for rehabilitation. Exp Brain Res. 2011;209(1):9–17. doi: 10.1007/s00221-010-2511-0.
    1. Madhavan S, Sriraman A, Freels S. Reliability and variability of tDCS induced changes in the lower limb motor cortex. Brain Sci. 2016;6(3):26. doi: 10.3390/brainsci6030026.
    1. van Asseldonk EHF, Boonstra TA. Transcranial direct current stimulation of the leg motor cortex enhances coordinated motor output during walking with a large inter-individual variability. Brain Stimul. 2016;9(2):182–190. doi: 10.1016/j.brs.2015.10.001.
    1. Rudroff T, Workman CD, Fietsam AC, Kamholz J. Response variability in transcranial direct current stimulation: why sex matters. Front Psychiatry. 2020;11:585. doi: 10.3389/fpsyt.2020.00585.
    1. Inghilleri M, Conte A, Currà A, Frasca V, Lorenzano C, Berardelli A. Ovarian hormones and cortical excitability. An rTMS study in humans. Clin Neurophysiol. 2004;115(5):1063–1068. doi: 10.1016/j.clinph.2003.12.003.
    1. Smith MJ, Adams LF, Schmidt PJ, Rubinow DR, Wassermann EM. Effects of ovarian hormones on human cortical excitability. Ann Neurol. 2002;51(5):599–603. doi: 10.1002/ana.10180.
    1. Smith MJ, Keel JC, Greenberg BD, Adams LF, Schmidt PJ, Rubinow DA, et al. Menstrual cycle effects on cortical excitability. Neurology. 1999;53(9):2069–2072. doi: 10.1212/WNL.53.9.2069.
    1. Antal A, Chaieb L, Moliadze V, Monte-Silva K, Poreisz C, Thirugnanasambandam N, et al. Brain-derived neurotrophic factor (BDNF) gene polymorphisms shape cortical plasticity in humans. Brain Stimul. 2010;3(4):230–237. doi: 10.1016/j.brs.2009.12.003.
    1. Mosayebi-Samani M, Jamil A, Salvador R, Ruffini G, Haueisen J, Nitsche MA. The impact of individual electrical fields and anatomical factors on the neurophysiological outcomes of tDCS: a TMS-MEP and MRI study. Brain Stimul. 2021;14(2):316–326. doi: 10.1016/j.brs.2021.01.016.
    1. Hummel FC, Voller B, Celnik P, Floel A, Giraux P, Gerloff C, et al. Effects of brain polarization on reaction times and pinch force in chronic stroke. BMC Neurosci. 2006;3(7):73. doi: 10.1186/1471-2202-7-73.
    1. Hesse S, Waldner A, Mehrholz J, Tomelleri C, Pohl M, Werner C. Combined transcranial direct current stimulation and robot-assisted arm training in subacute stroke patients: an exploratory, randomized multicenter trial. Neurorehabil Neural Repair. 2011;25(9):838–846. doi: 10.1177/1545968311413906.
    1. Tahtis V, Kaski D, Seemungal BM. The effect of single session bi-cephalic transcranial direct current stimulation on gait performance in sub-acute stroke: a pilot study. Restor Neurol Neurosci. 2014;32(4):527–532.
    1. Patrick L, Knoefel F, Gaskowski P, Rexroth D. Medical comorbidity and rehabilitation efficiency in geriatric inpatients. J Am Geriatr Soc. 2001;49(11):1471–1477. doi: 10.1046/j.1532-5415.2001.4911239.x.
    1. Atalay A, Turhan N. Determinants of length of stay in stroke patients: a geriatric rehabilitation unit experience. Int J Rehabil Res. 2009;32(1):48–52. doi: 10.1097/MRR.0b013e32830d3689.
    1. Simić-Panić D, Bošković K, Milićević M, Žikić TR, Cvjetković Bošnjak M, Tomašević-Todorović S, et al. The impact of comorbidity on rehabilitation outcome after ischemic stroke. Acta Clin Croat. 2018;57(1):5–15. doi: 10.20471/acc.2018.57.01.01.
    1. Turhan N, Atalay A, Muderrisoglu H. Predictors of functional outcome in first-ever ischemic stroke: a special interest to ischemic subtypes, comorbidity and age. NeuroRehabilitation. 2009;24(4):321–326. doi: 10.3233/NRE-2009-0485.
    1. Frazer AK, Howatson G, Ahtiainen JP, Avela J, Rantalainen T, Kidgell DJ. Priming the motor cortex with anodal transcranial direct current stimulation affects the acute inhibitory corticospinal responses to strength training. J Strength Cond Res. 2019;33(2):307–317. doi: 10.1519/JSC.0000000000002959.
    1. Ziemann U, Siebner HR. Modifying motor learning through gating and homeostatic metaplasticity. Brain Stimul. 2008;1(1):60–66. doi: 10.1016/j.brs.2007.08.003.
    1. Giacobbe V, Krebs HI, Volpe BT, Pascual-Leone A, Rykman A, Zeiarati G, et al. Transcranial direct current stimulation (tDCS) and robotic practice in chronic stroke: the dimension of timing. NeuroRehabilitation. 2013;33(1):49–56. doi: 10.3233/NRE-130927.
    1. Shah B, Nguyen TT, Madhavan S. Polarity independent effects of cerebellar tDCS on short term ankle visuomotor learning. Brain Stimul. 2013;6(6):966–968. doi: 10.1016/j.brs.2013.04.008.
    1. Olesen J. Calcium entry blockers in the treatment of vertigo. Ann N Y Acad Sci. 1988;522:690–697. doi: 10.1111/j.1749-6632.1988.tb33414.x.
    1. Spierings EL. Clinical and experimental evidence for a role of calcium entry blockers in the treatment of migraine. Ann N Y Acad Sci. 1988;522:676–689. doi: 10.1111/j.1749-6632.1988.tb33413.x.
    1. Greenberg DA. Calcium channels and calcium channel antagonists. Ann Neurol. 1987;21(4):317–330. doi: 10.1002/ana.410210402.
    1. Nitsche MA, Fricke K, Henschke U, Schlitterlau A, Liebetanz D, Lang N, et al. Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans. J Physiol (Lond) 2003;553(Pt 1):293–301. doi: 10.1113/jphysiol.2003.049916.
    1. Johnson R, Dludla P, Mabhida S, Benjeddou M, Louw J, February F. Pharmacogenomics of amlodipine and hydrochlorothiazide therapy and the quest for improved control of hypertension: a mini review. Heart Fail Rev. 2019;24(3):343–357. doi: 10.1007/s10741-018-09765-y.

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