Novel TMS for Stroke and Depression (NoTSAD): Accelerated Repetitive Transcranial Magnetic Stimulation as a Safe and Effective Treatment for Post-stroke Depression

Jessica Frey, Umer Najib, Christa Lilly, Amelia Adcock, Jessica Frey, Umer Najib, Christa Lilly, Amelia Adcock

Abstract

Background: Post-stroke depression (PSD) affects up to 50% of stroke survivors, reducing quality of life, and increasing adverse outcomes. Conventional therapies to treat PSD may not be effective for some patients. Repetitive transcranial magnetic stimulation (rTMS) is well-established as an effective treatment for Major Depressive Disorder (MDD) and some small trials have shown that rTMS may be effective for chronic PSD; however, no trials have evaluated an accelerated rTMS protocol in a subacute stroke population. We hypothesized that an accelerated rTMS protocol will be a safe and viable option to treat PSD symptoms. Methods: Patients (N = 6) with radiographic evidence of ischemic stroke within the last 2 weeks to 6 months with Hamilton Depression Rating Scale (HAMD-17) scores >7 were recruited for an open label study using an accelerated rTMS protocol as follows: High-frequency (20-Hz) rTMS at 110% resting motor threshold (RMT) was applied to the left dorsolateral prefrontal cortex (DLPFC) during five sessions per day over four consecutive days for a total of 20 sessions. Safety assessment and adverse events were documented based on the patients' responses following each day of stimulation. Before and after the 4-days neurostimulation protocol, outcome measures were obtained for the HAMD, modified Rankin Scale (mRS), functional independence measures (FIM), and National Institutes of Health Stroke Scales (NIHSS). These same measures were obtained at 3-months follow up. Results: HAMD significantly decreased (Wilcoxon p = 0.03) from M = 15.5 (2.81)-4.17 (0.98) following rTMS, a difference which persisted at the 3-months follow-up (p = 0.03). No statistically significant difference in FIM, mRS, or NIHSS were observed. No significant adverse events related to the treatment were observed and patients tolerated the stimulation protocol well overall. Conclusions: This pilot study indicates that an accelerated rTMS protocol is a safe and viable option, and may be an effective alternative or adjunctive therapy for patients suffering from PSD. Future randomized, controlled studies are needed to confirm these preliminary findings. Clinical Trial Registration: https://ichgcp.net/clinical-trials-registry/NCT04093843.

Keywords: accelerated TMS; ischemic stroke; neurorehabilitation; neurostimulation; post-stroke depression; stroke recovery; transcranial magnetic stimulation.

Copyright © 2020 Frey, Najib, Lilly and Adcock.

Figures

Figure 1
Figure 1
HAMD scores in our six patients before the TMS sessions (baseline), immediately after completing the full 4-days neurostimulation protocol, and at their 3-months follow-up appointment.

References

    1. Villa RF, Ferrari F, Moretti A. Post-stroke depression: mechanisms and pharmacological treatment. Pharmacol Ther. (2018) 184:131–44. 10.1016/j.pharmthera.2017.11.005
    1. Bartoli F, Lillia N, Lax A, Crocamo C, Mantero V, Carrà G, et al. . Depression after stroke and risk of mortality: a systematic review and meta-analysis. Stroke Res Treat. (2013) 2013:862978. 10.1155/2013/862978
    1. Paolucci S. Epidemiology and treatment of post-stroke depression. Neuropsychiatr Dis Treat. (2008) 4:145–54. 10.2147/NDT.S2017
    1. Espárrago Llorca G, Castilla-Guerra L, Fernández Moreno MC, Ruiz Doblado S, Jiménez Hernández MD. Post-stroke depression: an update. Neurologia. (2015) 30:23–31. 10.1016/j.nrleng.2012.06.006
    1. Al-Harbi KS. Treatment-resistant depression: therapeutic trends, challenges, and future directions. Patient Prefer Adherence. (2012) 6:369–88. 10.2147/PPA.S29716
    1. Robinson RG, Jorge RE. Post-stroke depression: a review. Am J Psychiatry. (2016) 173:221–31. 10.1176/appi.ajp.2015.15030363
    1. Xu XM, Zou DZ, Shen LY, Liu Y, Zhou XY, Pu JC, et al. . Efficacy and feasibility of antidepressant treatment in patients with post-stroke depression. Medicine (Baltimore). (2016) 95:e5349. 10.1097/MD.0000000000005349
    1. O'Reardon JP, Solvason HB, Janicak PG, Sampson S, Isenberg KE, Nahas Z, et al. . Efficacy and safety of transcranial magnetic stimulation in the acute treatment of major depression: a multisite randomized controlled trial. Biol Psychiatry. (2007) 62:1208–16. 10.1016/j.biopsych.2007.01.018
    1. Jorge RE, Robinson RG, Tateno A, Narushima K, Acion L, Moser D, et al. . Repetitive transcranial magnetic stimulation as treatment of poststroke depression: a preliminary study. Biol Psych. (2004) 55:398–405. 10.1016/j.biopsych.2003.08.017
    1. Shen X, Liu M, Cheng Y, Jia C, Pan X, Gou Q, et al. . Repetitive transcranial magnetic stimulation for the treatment of post-stroke depression: a systematic review and meta-analysis of randomized controlled clinical trials. J Affect Disord. (2017) 211:65–74. 10.1016/j.jad.2016.12.058
    1. Baeken C, Marinazzo D, Wu GR, Van Schuerbeek P, De Mey J, Marchetti I, et al. Accelerated HF-rTMS in treatment-resistant unipolar depression: insights from subgenual anterior cingulate functional connectivity. World J Biol Psych. (2014) 12:2014 10.3109/15622975.2013.872295
    1. Herremans SC, Van Schuerbeek P, De Raedt R, Matthys F, Buyl R, De Mey J, et al. The impact of accelerated prefrontal high-frequency repetitive transcranial magnetic stimulation (rTMS) on cue-reactivity: an fMRI study on craving in recently detoxified alcohol-dependent patients. PLoS ONE. (2015) 10:2015 10.1371/journal.pone.0136182
    1. Holtzheimer PE, McDonald WM, Mufti M, Kelley ME, Quinn S, Corso G, et al. . Accelerated repetitive transcranial magnetic stimulation (aTMS) for treatment-resistant depression. Depr Anx. (2010). 27:960–3. 10.1002/da.20731
    1. Fitzgerald PB, Hoy KE, Elliot D, Susan McQueen RN, Wambeek LE, Daskalakis ZJ. Accelerated repetitive transcranial magnetic stimulation in the treatment of depression. Neuropsychopharmacology. (2018) 43:1565–72. 10.1038/s41386-018-0009-9
    1. Coleman ER, Moudgal R, Lang K, Hyacinth HI, Awosika OO, Kissela BM, et al. . Early rehabilitation after stroke: a narrative review. Curr Atheroscler Rep. (2017) 19:59. 10.1007/s11883-017-0686-6
    1. Wu CM, McLaughlin K, Lorenzetti DL, Hill MD, Manns BJ, Ghali WA. Early risk of stroke after transient ischemic attack: a systematic review and meta-analysis. JAMA Internal Med. (2007) 167:2417–22. 10.1001/archinte.167.22.2417
    1. McGirr A, Van den Eynde F, Tovar-Perdomo S, Fleck MP, Berlim MT. Effectiveness and acceptability of accelerated repetitive transcranial magnetic stimulation (rTMS) for treatment-resistant major depressive disorder: an open label trial. J Affect Disord. (2015) 173:216–20. 10.1016/j.jad.2014.10.068
    1. Baeken C, Vanderhasselt MA, Remue J, Herremans S, Vanderbruggen N, Zeeuws D, et al. . Intensive HF-rTMS treatment in refractory medication-resistant unipolar depressed patients. J Affect Disord. (2013) 151:625–31. 10.1016/j.jad.2013.07.008
    1. Gu SY, Chang MC. The effects of 10-Hz repetitive transcranial magnetic stimulation on depression in chronic stroke patients. Brain Stimul. (2017) 10:270–4. 10.1016/j.brs.2016.10.010
    1. Kim BR, Kim DY, Chun MH, Yi JH, Kwon JS. Effect of repetitive transcranial magnetic stimulation on cognition and mood in stroke patients: a double-blind, sham-controlled trial. Am J Phys Med Rehabil. (2018) 89:362–8. 10.1097/PHM.0b013e3181d8a5b1
    1. Kim KU, Kim SH, An TG. The effects of repetitive transcranial magnetic stimulation (rTMS) on depression, visual perception, and activities of daily living in stroke patients. J Physical Ther Sci. (2017) 29:1036–9. 10.1589/jpts.29.1036
    1. Slotema CW, Blom JD, Hoek HW, Sommer IE. Should we expand the toolbox of psychiatric treatment methods to include Repetitive Transcranial Magnetic Stimulation (rTMS)? A meta-analysis of the efficacy of rTMS in psychiatric disorders. J Clin Psychiatry. (2010) 71:873–84. 10.4088/JCP.08m04872gre
    1. Duan X, Yao G, Liu Z, Cui R, Yang W. Mechanisms of transcranial magnetic stimulation treating on post-stroke depression. Front Neurol. (2018) 12:215. 10.3389/fnhum.2018.00215
    1. Currier MB, Murray GB, Welch CC. Electroconvulsive therapy for post-stroke depressed geriatric patients. J Neuropsychiatry Clin Neurosci. (1992) 4:140–4. 10.1176/jnp.4.2.140
    1. Wassermann EM, Zimmermann T. Transcranial magnetic brain stimulation: therapeutic promises and scientific gaps. Pharmacol Ther. (2012) 133:98–107. 10.1016/j.pharmthera.2011.09.003
    1. Paus T, Castro-Alamancos MA, Petrides M. Cortico-cortical connectivity of the human mid-dorsolateral frontal cortex and its modulation by repetitive transcranial magnetic stimulation. Eur J Neurosci. (2001) 14:1405–11. 10.1046/j.0953-816x.2001.01757.x
    1. Dubin MJ, Mao X, Banerjee S, Goodman Z, Lapidus KA, Kang G, et al. . Elevated prefrontal cortex GABA in patients with major depressive disorder after TMS treatment measured with proton magnetic resonance spectroscopy. J Psychiatry Neurosci. (2016) 41:E37–45. 10.1503/jpn.150223
    1. Nordmann G, Azorina V, Langguth B, Schecklmann M. A systematic review of non-motor rTMS induced motor cortex plasticity. Front Hum Neurosci. (2015) 9:416. 10.3389/fnhum.2015.00416
    1. Autry AE, Monteggia LM. Brain-derived neurotrophic factor and neuropsychiatric disorders. Pharmacol Rev. (2012) 64:238–58. 10.1124/pr.111.005108
    1. Chang WH, Shin MA, Lee A, Kim H, Kim YH. Relationship between serum BDNF levels and depressive mood in subacute stroke patients: a preliminary study. Int J Mol Sci. (2018) 19:3131. 10.3390/ijms19103131
    1. Li Y, Peng C, Guo X, You JJ, Yadav HP. Expression of brain-derived neurotrophic factor and tyrosine kinase b in cerebellum of poststroke depression rat model. Chin Med J. (2015) 128:2926–31. 10.4103/0366-6999.168058
    1. Na KS, Won E, Kang J, Chang HS, Yoon HK, Tae WS, et al. . Brain-derived neurotrophic factor promoter methylation and cortical thickness in recurrent major depressive disorder. Sci Rep. (2016) 6:21089. 10.1038/srep21089
    1. Phillips C. Brain-derived neurotrophic factor, depression, and physical activity: making the neuroplastic connection. Neural Plast. (2017) 2017:7260130. 10.1155/2017/7260130
    1. Yang XR, Kirton A, Wilkes TC, Pradhan S, Liu I, Jaworska N, et al. . Glutamate alterations associated with transcranial magnetic stimulation in youth depression: a case series. J ECT. (2014) 30:242–7. 10.1097/YCT.0000000000000094
    1. Strafella AP, Paus T, Fraraccio M, Dagher A. Striatal dopamine release induced by repetitive transcranial magnetic stimulation of the human motor cortex. Brain. (2003) 126:2609–15. 10.1093/brain/awg268
    1. Cho SS, Strafella AP. rTMS of the left dorsolateral prefrontal cortex modulates dopamine release in the ipsilateral anterior cingulate cortex and orbitofrontal cortex. PLoS ONE. (2009) 4:e6725–25. 10.1371/journal.pone.0006725
    1. Etiévant A, Manta S, Latapy C, Magno LA, Fecteau S, Beaulieu JM. Repetitive transcranial magnetic stimulation induces long-lasting changes in protein expression and histone acetylation. Scient Rep. (2015) 5:16873. 10.1038/srep16873
    1. Chervyakov AV, Chernyavsky AY, Sinitsyn DO, Piradov MA. Possible mechanisms underlying the therapeutic effects of transcranial magnetic stimulation. Front Hum Neurosci. (2015) 9:303. 10.3389/fnhum.2015.00303
    1. Hosomi K, Morris S, Sakamoto T, Taguchi J, Maruo T, Kageyama Y, et al. . Daily repetitive transcranial magnetic stimulation for poststroke upper limb paresis in the subacute period. J Stroke Cerebrovasc Dis. (2016) 25:1655–64. 10.1016/j.jstrokecerebrovasdis.2016.02.024
    1. Guo Z, Jin Y, Peng H, Xing G, Liao X, Wang Y, et al. . Ipsilesional high frequency repetitive transcranial magnetic stimulation add-on therapy improved diffusion parameters of stroke patients with motor dysfunction: a preliminary DTI study. Neural Plasticity. (2016) 2016:11. 10.1155/2016/6238575
    1. Guan YZ, Li J, Zhang XW, Wu S, Du H, Cui LY, et al. . Effectiveness of repetitive transcranial magnetic stimulation (rTMS) after acute stroke: a one year longitudinal randomized trial. CNS Neurosci Therap. (2017) 23:940–6. 10.1111/cns.12762
    1. Conforto AB, Anjos SM, Saposnik G, Mello EA, Nagaya EM, Santos W, et al. . Transcranial magnetic stimulation in mild to severe hemiparesis early after stroke: a proof of principle and novel approach to improve motor function. J Neurol. (2012) 259:1399–405. 10.1007/s00415-011-6364-7
    1. Rossini D, Magri L, Lucca A, Giordani S, Smeraldi E, Zanardi R. Does rTMS hasten the response to escitalopram, sertraline, or venlafaxine in patients with major depressive disorder? A double-blind, randomized, sham-controlled trial. J Clin Psychiatry. (2005) 66:1569–75. 10.4088/JCP.v66n1212
    1. Taylor R, Galvez V, Loo C. Transcranial magnetic stimulation (TMS) safety considerations and recommendations. Transcran Magnet Stimul. (2014) 89:15–30. 10.1007/978-1-4939-0879-0_2

Source: PubMed

Спонсоры и соавторы

Заболевания

Медикаментозные вмешательства

Подписаться