Skip to main content

Advertisement

SpringerLink
Log in

Transcranial direct current stimulation for post-stroke dysphagia: a systematic review and meta-analysis of randomized controlled trials

  • Original Communication
  • Published:
Journal of Neurology Aims and scope Submit manuscript

Abstract

Background

Transcranial direct current stimulation (tDCS) has been investigated as a tool for dysphagia recovery after stroke in several single-center randomized controlled trials (RCT).

Objective

The aim of this investigation was to quantitatively evaluate the effect of tDCS on dysphagia recovery after a stroke utilizing a systematic review and meta-analysis.

Methods

Major databases were searched through October 2019 using a pre-defined set of criteria. Any RCT investigating the efficacy of tDCS in post-stroke dysphagia using a standardized dysphagia scale as outcome measure was included. Studies were assessed for risk of bias and quality using the Physiotherapy Evidence Database (PEDro) scale. Effect sizes were calculated from extracted data and entered into a random effects analysis to obtain pooled estimates of the effect.

Results

Seven RCTs with a total sample size of 217 patients fulfilled the criteria and were included in the analysis. The overall results revealed a small but statistically significant pooled effect size (0.31; CI 0.03, 0.59; p = 0.03). The subgroup which explored the stimulation intensity yielded a moderately significant effect size for the low-intensity stimulation group (g = 0.44; CI = 0.08, 0.81 vs. g = 0.15, CI − 0.30, 0.61). For the other subgroup analyses, neither comparisons of affected vs. unaffected hemisphere or acute vs. chronic stroke phase revealed a significant result.

Conclusion

This meta-analysis demonstrates a modest but significant beneficial effect of tDCS on improving post-stroke dysphagia. Whether benefits from this intervention are more pronounced in certain patient subgroups and with specific stimulation protocols requires further investigation.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Ahn YH, Sohn HJ, Park JS, Ahn TG, Shin YB, Park M, Ko SH, Shin YI (2017) Effect of bihemispheric anodal transcranial direct current stimulation for dysphagia in chronic stroke patients: a randomized clinical trial. J Rehabil Med 49:30–35

    PubMed  Google Scholar 

  2. Altman KW, Yu GP, Schaefer SD (2010) Consequence of dysphagia in the hospitalized patient: impact on prognosis and hospital resources. Arch Otolaryngol-Head Neck Surg 136:784–789

    PubMed  Google Scholar 

  3. Ammann C, Lindquist MA, Celnik PA (2017) Response variability of different anodal transcranial direct current stimulation intensities across multiple sessions. Brain Stimul 10:757–763

    PubMed  PubMed Central  Google Scholar 

  4. Arnold M, Liesirova K, Broeg-Morvay A, Meisterernst J, Schlager M, Mono ML, El-Koussy M, Kagi G, Jung S, Sarikaya H (2016) Dysphagia in acute stroke: incidence, burden and impact on clinical outcome. PLoS ONE 11:e0148424

    PubMed  PubMed Central  Google Scholar 

  5. Baker JM, Rorden C, Fridriksson J (2010) Using transcranial direct-current stimulation to treat stroke patients with aphasia. Stroke J Cereb Circ 41:1229–1236

    Google Scholar 

  6. Bastani A, Jaberzadeh S (2012) Does anodal transcranial direct current stimulation enhance excitability of the motor cortex and motor function in healthy individuals and subjects with stroke: a systematic review and meta-analysis. Clin Neurophysiol Off J Int Fed Clin Neurophysiol 123:644–657

    CAS  Google Scholar 

  7. Bath PM, Bath FJ, Smithard DG (2000) Interventions for dysphagia in acute stroke. Cochrane Database Syst Rev 2:CD000323

    Google Scholar 

  8. Bath PM, Lee HS, Everton LF (2018) Swallowing therapy for dysphagia in acute and subacute stroke. Cochrane Database Syst Rev 10:CD000323

    PubMed  Google Scholar 

  9. Bath PM, Scutt P, Love J, Clave P, Cohen D, Dziewas R, Iversen HK, Ledl C, Ragab S, Soda H, Warusevitane A, Woisard V, Hamdy S, Swallowing Treatment Using Pharyngeal Electrical Stimulation Trial I (2016) Pharyngeal electrical stimulation for treatment of dysphagia in subacute stroke: a randomized controlled trial. Stroke J Cereb Circ 47:1562–1570

    Google Scholar 

  10. Batsikadze G, Moliadze V, Paulus W, Kuo MF, Nitsche MA (2013) Partially non-linear stimulation intensity-dependent effects of direct current stimulation on motor cortex excitability in humans. J Physiol 591:1987–2000

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Bulow M, Speyer R, Baijens L, Woisard V, Ekberg O (2008) Neuromuscular electrical stimulation (NMES) in stroke patients with oral and pharyngeal dysfunction. Dysphagia 23:302–309

    PubMed  Google Scholar 

  12. Butler AJ, Shuster M, O’Hara E, Hurley K, Middlebrooks D, Guilkey K (2013) A meta-analysis of the efficacy of anodal transcranial direct current stimulation for upper limb motor recovery in stroke survivors. J Hand Therapy: Off J Am Soc Hand Therapists 26:162–170 (quiz 171)

    Google Scholar 

  13. Carnaby G, Hankey GJ, Pizzi J (2006) Behavioural intervention for dysphagia in acute stroke: a randomised controlled trial. Lancet Neurol 5:31–37

    PubMed  Google Scholar 

  14. Chen H, Manning AK, Dupuis J (2012) A method of moments estimator for random effect multivariate meta-analysis. Biometrics 68:1278–1284

    PubMed  PubMed Central  Google Scholar 

  15. de Lama Lazzara G, Lazarus C, Logemann JA (1986) Impact of thermal stimulation on the triggering of the swallowing reflex. Dysphagia 1:73–77

    Google Scholar 

  16. Dziewas R, Stellato R, van der Tweel I, Walther E, Werner CJ, Braun T, Citerio G, Jandl M, Friedrichs M, Notzel K, Vosko MR, Mistry S, Hamdy S, McGowan S, Warnecke T, Zwittag P, Bath PM, Investigators P-T (2018) Pharyngeal electrical stimulation for early decannulation in tracheotomised patients with neurogenic dysphagia after stroke (PHAST-TRAC): a prospective, single-blinded, randomised trial. Lancet Neurol 17:849–859

    PubMed  Google Scholar 

  17. Dziewas R, Warnecke T, Olenberg S, Teismann I, Zimmermann J, Kramer C, Ritter M, Ringelstein EB, Schabitz WR (2008) Towards a basic endoscopic assessment of swallowing in acute stroke—development and evaluation of a simple dysphagia score. Cerebrovasc Dis 26:41–47

    PubMed  Google Scholar 

  18. Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Elmstahl S, Bulow M, Ekberg O, Petersson M, Tegner H (1999) Treatment of dysphagia improves nutritional conditions in stroke patients. Dysphagia 14:61–66

    CAS  PubMed  Google Scholar 

  20. Elsner B, Kugler J, Pohl M, Mehrholz J (2019) Transcranial direct current stimulation (tDCS) for improving aphasia in adults with aphasia after stroke. Cochrane Database Syst Rev 5:CD009760

    PubMed  Google Scholar 

  21. Esmaeilpour Z, Marangolo P, Hampstead BM, Bestmann S, Galletta E, Knotkova H, Bikson M (2018) Incomplete evidence that increasing current intensity of tDCS boosts outcomes. Brain Stimul 11:310–321

    PubMed  Google Scholar 

  22. Feng WW, Bowden MG, Kautz S (2013) Review of transcranial direct current stimulation in poststroke recovery. Top Stroke Rehabil 20:68–77

    PubMed  Google Scholar 

  23. Foley NC, Teasell RW, Bhogal SK, Speechley MR (2003) Stroke rehabilitation evidence-based review: methodology. Top Stroke Rehabil 10:1–7

    PubMed  Google Scholar 

  24. Galovic M, Stauber AJ, Leisi N, Krammer W, Brugger F, Vehoff J, Balcerak P, Muller A, Muller M, Rosenfeld J, Polymeris A, Thilemann S, De Marchis GM, Niemann T, Leifke M, Lyrer P, Saladin P, Kahles T, Nedeltchev K, Sarikaya H, Jung S, Fischer U, Manno C, Cereda CW, Sander JW, Tettenborn B, Weder BJ, Stoeckli SJ, Arnold M, Kagi G (2019) Development and validation of a prognostic model of swallowing recovery and enteral tube feeding after ischemic stroke. JAMA Neurol 76:561–570

    PubMed  PubMed Central  Google Scholar 

  25. Hamdy S, Aziz Q, Rothwell JC, Crone R, Hughes D, Tallis RC, Thompson DG (1997) Explaining oropharyngeal dysphagia after unilateral hemispheric stroke. Lancet 350:686–692

    CAS  PubMed  Google Scholar 

  26. Hamdy S, Aziz Q, Rothwell JC, Power M, Singh KD, Nicholson DA, Tallis RC, Thompson DG (1998) Recovery of swallowing after dysphagic stroke relates to functional reorganization in the intact motor cortex. Gastroenterology 115:1104–1112

    CAS  PubMed  Google Scholar 

  27. Hamdy S, Aziz Q, Rothwell JC, Singh KD, Barlow J, Hughes DG, Tallis RC, Thompson DG (1996) The cortical topography of human swallowing musculature in health and disease. Nat Med 2:1217–1224

    CAS  PubMed  Google Scholar 

  28. Hamdy S, Rothwell JC, Aziz Q, Thompson DG (2000) Organization and reorganization of human swallowing motor cortex: implications for recovery after stroke. Clin Sci 99:151–157

    CAS  Google Scholar 

  29. Han TR, Paik NJ, Park JW (2001) Quantifying swallowing function after stroke: a functional dysphagia scale based on videofluoroscopic studies. Arch Phys Med Rehabil 82:677–682

    CAS  PubMed  Google Scholar 

  30. Hedges LV, Olkin I (1985) Statistical methods for meta-analysis. Academic Press, Orlando

    Google Scholar 

  31. Hummel F, Celnik P, Giraux P, Floel A, Wu WH, Gerloff C, Cohen LG (2005) Effects of non-invasive cortical stimulation on skilled motor function in chronic stroke. Brain: J Neurol 128:490–499

    Google Scholar 

  32. Iyer MB, Mattu U, Grafman J, Lomarev M, Sato S, Wassermann EM (2005) Safety and cognitive effect of frontal DC brain polarization in healthy individuals. Neurology 64:872–875

    CAS  PubMed  Google Scholar 

  33. Jamil A, Batsikadze G, Kuo HI, Labruna L, Hasan A, Paulus W, Nitsche MA (2017) Systematic evaluation of the impact of stimulation intensity on neuroplastic after-effects induced by transcranial direct current stimulation. J Physiol 595:1273–1288

    CAS  PubMed  Google Scholar 

  34. Jefferson S, Mistry S, Singh S, Rothwell J, Hamdy S (2009) Characterizing the application of transcranial direct current stimulation in human pharyngeal motor cortex. Am J Physiol Gastrointest Liver Physiol 297:G1035–G1040

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Ko MH, Han SH, Park SH, Seo JH, Kim YH (2008) Improvement of visual scanning after DC brain polarization of parietal cortex in stroke patients with spatial neglect. Neurosci Lett 448(2):171–174

    CAS  PubMed  Google Scholar 

  36. Krause FF, Muller K, Zillmann D, Jansen J, Schowalter M, Rosenauer A (2013) Comparison of intensity and absolute contrast of simulated and experimental high-resolution transmission electron microscopy images for different multislice simulation methods. Ultramicroscopy 134:94–101

    CAS  PubMed  Google Scholar 

  37. Kumar S, Wagner CW, Frayne C, Zhu L, Selim M, Feng W, Schlaug G (2011) Noninvasive brain stimulation may improve stroke-related dysphagia: a pilot study. Stroke; a journal of cerebral circulation 42:1035–1040

    PubMed Central  Google Scholar 

  38. Kumar SM, Langmore S, Massaro J, Palmisano J, Wang N, Searls DE, Lioutas V, Pisegna J, Wagner C, Schlaug G (under review) Fostering eating after stroke with transcranial direct current stimulation (FEASt): a randomized controlled trial of non-invasive brain stimulation for dysphagia recovery. JAMA Neurol

  39. Kusumaningsih W, Lestari NI, Harris S, Tamin S, Werdhani RA (2019) The effectivity of pharyngeal strengthening exercise, hyolaryngeal complex range of motion exercise, and swallowing practice in swallowing function of ischemic stroke patients with neurogenic dysphagia. J Exerc Rehabil 15:769–774

    PubMed  PubMed Central  Google Scholar 

  40. Liao X, Xing G, Guo Z, Jin Y, Tang Q, He B, McClure MA, Liu H, Chen H, Mu Q (2017) Repetitive transcranial magnetic stimulation as an alternative therapy for dysphagia after stroke: a systematic review and meta-analysis. Clin Rehabil 31:289–298

    PubMed  Google Scholar 

  41. Lindenberg R, Renga V, Zhu LL, Nair D, Schlaug G (2010) Bihemispheric brain stimulation facilitates motor recovery in chronic stroke patients. Neurology 75:2176–2184

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Maher CG, Sherrington C, Herbert RD, Moseley AM, Elkins M (2003) Reliability of the PEDro scale for rating quality of randomized controlled trials. Phys Ther 83:713–721

    PubMed  Google Scholar 

  43. Mann G, Hankey GJ, Cameron D (1999) Swallowing function after stroke: prognosis and prognostic factors at 6 months. Stroke J Cereb Circ 30:744–748

    CAS  Google Scholar 

  44. Martino R, Foley N, Bhogal S, Diamant N, Speechley M, Teasell R (2005) Dysphagia after stroke: incidence, diagnosis, and pulmonary complications. Stroke J Cereb Circ 36:2756–2763

    Google Scholar 

  45. Meron D, Hedger N, Garner M, Baldwin DS (2015) Transcranial direct current stimulation (tDCS) in the treatment of depression: systematic review and meta-analysis of efficacy and tolerability. Neurosci Biobehav Rev 57:46–62

    PubMed  Google Scholar 

  46. Mondino M, Bennabi D, Poulet E, Galvao F, Brunelin J, Haffen E (2014) Can transcranial direct current stimulation (tDCS) alleviate symptoms and improve cognition in psychiatric disorders? World J Biol Psychiatry: Off J World Fed Soc Biol Psychiatry 15:261–275

    Google Scholar 

  47. Monte-Silva K, Kuo MF, Hessenthaler S, Fresnoza S, Liebetanz D, Paulus W, Nitsche MA (2013) Induction of late LTP-like plasticity in the human motor cortex by repeated non-invasive brain stimulation. Brain Stimul 6:424–432

    PubMed  Google Scholar 

  48. Moseley AM, Herbert RD, Sherrington C, Maher CG (2002) Evidence for physiotherapy practice: a survey of the Physiotherapy Evidence Database (PEDro). Aust J Physiother 48:43–49

    PubMed  Google Scholar 

  49. Nitsche MA, Boggio PS, Fregni F, Pascual-Leone A (2009) Treatment of depression with transcranial direct current stimulation (tDCS): a review. Exp Neurol 219:14–19

    PubMed  Google Scholar 

  50. Nitsche MA, Paulus W (2000) Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol 527(Pt 3):633–639

    CAS  PubMed  PubMed Central  Google Scholar 

  51. O’Neil KH, Purdy M, Falk J, Gallo L (1999) The dysphagia outcome and severity scale. Dysphagia 14:139–145

    PubMed  Google Scholar 

  52. Pingue V, Priori A, Malovini A, Pistarini C (2018) Dual transcranial direct current stimulation for poststroke dysphagia: a randomized controlled trial. Neurorehabil Neural Repair 32:635–644

    PubMed  Google Scholar 

  53. Pisegna JM, Kaneoka A, Pearson WG Jr, Kumar S, Langmore SE (2016) Effects of non-invasive brain stimulation on post-stroke dysphagia: a systematic review and meta-analysis of randomized controlled trials. Clin Neurophysiol: Off J Int Fed Clin Neurophysiol 127:956–968

    Google Scholar 

  54. Poreisz C, Boros K, Antal A, Paulus W (2007) Safety aspects of transcranial direct current stimulation concerning healthy subjects and patients. Brain Res Bull 72:208–214

    PubMed  Google Scholar 

  55. Pozo K, Goda Y (2010) Unraveling mechanisms of homeostatic synaptic plasticity. Neuron 66:337–351

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Review Manager (RevMan) [Computer Program] (2014) Version 5.3. In: The Nordic Cochrane Centre, The Cochrane Collaboration, Copenhagen, Denmark

  57. Rioult-Pedotti MS, Donoghue JP, Dunaevsky A (2007) Plasticity of the synaptic modification range. J Neurophysiol 98:3688–3695

    PubMed  Google Scholar 

  58. Rosenbek JC, Robbins JA, Roecker EB, Coyle JL, Wood JL (1996) A penetration-aspiration scale. Dysphagia 11:93–98

    CAS  PubMed  Google Scholar 

  59. Schlaug G, Renga V, Nair D (2008) Transcranial direct current stimulation in stroke recovery. Arch Neurol 65:1571–1576

    PubMed  PubMed Central  Google Scholar 

  60. Shigematsu T, Fujishima I, Ohno K (2013) Transcranial direct current stimulation improves swallowing function in stroke patients. Neurorehabil Neural Repair 27:363–369

    PubMed  Google Scholar 

  61. Simons A, Hamdy S (2017) The use of brain stimulation in dysphagia management. Dysphagia 32:209–215

    PubMed  PubMed Central  Google Scholar 

  62. Singh S, Hamdy S (2006) Dysphagia in stroke patients. Postgrad Med J 82:383–391

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Smithard DG, O’Neill PA, Martin DF, England R (1997) Aspiration following stroke: is it related to the side of the stroke? Clinical rehabilitation 11:73–76

    CAS  PubMed  Google Scholar 

  64. Suntrup-Krueger S, Ringmaier C, Muhle P, Wollbrink A, Kemmling A, Hanning U, Claus I, Warnecke T, Teismann I, Pantev C, Dziewas R (2018) Randomized trial of transcranial direct current stimulation for poststroke dysphagia. Ann Neurol 83:328–340

    PubMed  Google Scholar 

  65. Takeuchi N, Izumi S (2012) Noninvasive brain stimulation for motor recovery after stroke: mechanisms and future views. Stroke Res Treat 2012:584727

    PubMed  PubMed Central  Google Scholar 

  66. Thomson-Reuters Endnote. endnote.com

  67. Vose A, Nonnenmacher J, Singer ML, Gonzalez-Fernandez M (2014) Dysphagia management in acute and sub-acute stroke. Curr Phys Med Rehabil Rep 2:197–206

    PubMed  PubMed Central  Google Scholar 

  68. Warnecke T, Ritter MA, Kroger B, Oelenberg S, Teismann I, Heuschmann PU, Ringelstein EB, Nabavi DG, Dziewas R (2009) Fiberoptic endoscopic dysphagia severity scale predicts outcome after acute stroke. Cerebrovasc Dis 28:283–289

    PubMed  Google Scholar 

  69. Yang EJ, Baek SR, Shin J, Lim JY, Jang HJ, Kim YK, Paik NJ (2012) Effects of transcranial direct current stimulation (tDCS) on post-stroke dysphagia. Restor Neurol Neurosci 30:303–311

    CAS  PubMed  Google Scholar 

  70. Yang SN, Pyun SB, Kim HJ, Ahn HS, Rhyu BJ (2015) Effectiveness of non-invasive brain stimulation in dysphagia subsequent to stroke: a systemic review and meta-analysis. Dysphagia 30:383–391

    PubMed  Google Scholar 

Download references

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Author information

Authors and Affiliations

  1. Department of Neurology, Stroke Division, Beth Israel Deaconess Medical Center and Harvard Medical School, Palmer 127, 330 Brookline Ave, Boston, MA, 02215, USA

    Sarah Marchina, Courtney McVey, Jeffrey Wang & Sandeep Kumar

  2. Department of Otolaryngology- Head and Neck Surgery Department, Boston University Medical Center, Boston, MA, USA

    Jessica M. Pisegna & Susan E. Langmore

  3. Department of Biostatistics, School of Public Health, Boston University, Boston, MA, USA

    Joseph M. Massaro

Authors
  1. Sarah Marchina
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jessica M. Pisegna
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Joseph M. Massaro
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Susan E. Langmore
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Courtney McVey
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jeffrey Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sandeep Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sarah Marchina.

Ethics declarations

Conflicts of interest

The authors declare that that research was conducted in the absence of any commercial or financial relationships that could be construed as potential conflict of interest.

Ethical standard statement

All procedures performed in studies involving human participants 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.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Marchina, S., Pisegna, J., Massaro, J.M. et al. Transcranial direct current stimulation for post-stroke dysphagia: a systematic review and meta-analysis of randomized controlled trials. J Neurol 268, 293–304 (2021). https://doi.org/10.1007/s00415-020-10142-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00415-020-10142-9

Keywords

Search

Navigation