Neurostimulation for cognitive rehabilitation in stroke (NeuroCog): study protocol for a randomized controlled trial

Suellen Marinho Andrade, Bernardino Fernández-Calvo, Paulo Sérgio Boggio, Eliane Araújo de Oliveira, Lilze Franklim Gomes, José Eudes Gomes Pinheiro Júnior, Rafaela Martins Rodrigues, Natália Leandro de Almeida, Gioconda Marla de Siqueira Moreira, Nelson Torro Alves, Suellen Marinho Andrade, Bernardino Fernández-Calvo, Paulo Sérgio Boggio, Eliane Araújo de Oliveira, Lilze Franklim Gomes, José Eudes Gomes Pinheiro Júnior, Rafaela Martins Rodrigues, Natália Leandro de Almeida, Gioconda Marla de Siqueira Moreira, Nelson Torro Alves

Abstract

Background: Stroke patients may present severe cognitive impairments, primarily related to executive functions. Transcranial direct current stimulation has shown promising results, with neuromodulatory and neuroplastic effects. This study is a double-blind, sham-controlled clinical trial aiming to compare the long-term effects of stimulation in two different cognitive regions after a stroke.

Methods/design: Sixty patients who suffer from chronic strokes will be randomized into one of four groups: dorsolateral prefrontal cortex, cingulo-opercular network, motor primary cortex and sham stimulation. Each group will receive transcranial direct current stimulation at an intensity of 2 mA for 20 minutes daily for 10 consecutive days. Patients will be assessed with a Dysexecutive Questionnaire, Semantic Fluency Test, categorical verbal fluency and Go-no go tests, Wechsler Adult Intelligence Scale, Rey Auditory-Verbal Learning Test, Letter Comparison and Pattern Comparison Tasks at baseline and after their tenth stimulation session. Those who achieve clinical improvement with neurostimulation will be invited to receive treatment for 12 months as part of a follow-up study.

Discussion: Long-term stimulation could be analyzed in regard to possible adaptive changes on plasticity after structural brain damage and if these changes are different in terms of clinical improvement when applied to two important cognitive centers.

Trials registration: Clinicaltrials.gov, NCT02315807 . 9 December 2014.

Figures

Fig. 1
Fig. 1
Flow chart of study. ASB: Assessment of Stroke and other Brain Damage; CES-D: Center for Epidemiological Studies-Depression; CON: cingulo-opercular network; DEX: Dysexecutive Questionnaire; dlPFC: dorsolateral prefrontal cortex; FAS: Semantic Fluency Test; DRS-2: Dementia Rating Scale-2; LCPCT: Letter Comparison and Pattern Comparison Tasks; M1: primary motor cortex; MOCA: Montreal Cognitive Assessment; NIHSS: National Institute of Health Stroke Scale; OLT: Object Learning Test; RAVLT: Rey Auditory-Verbal Learning Test; tDCS: transcranial direct current stimulation; TMT: Trail Making Test; WAIS: Wechsler Adult Intelligence Scale

References

    1. Khedr EM, Shawky OA, El-Hammady DH, Rothwell JC, Darwish ES, Mostafa OM, et al. Effect of anodal versus cathodal transcranial direct current stimulation on stroke rehabilitation: a pilot randomized controlled trial. Neurorehabil Neural Repair. 2013;27:592–601. doi: 10.1177/1545968313484808.
    1. Chung CSY, Pollock A, Campbell T, Durward BR, Hagen S. Cognitive rehabilitation for executive dysfunction in adults with stroke or other adult non-progressive acquired brain damage. Cochrane Database Syst Rev. 2013;4:CD008391.
    1. Thibaut A, Chatelle C, Gosseries O, Laureys S, Bruno M-A. Transcranial direct current stimulation: a new tool for neurostimulation. Rev Neurol (Paris) 2013;169:108–20. doi: 10.1016/j.neurol.2012.05.008.
    1. Nahas Z, Kozel FA, Li X, Anderson B, George MS. Left prefrontal transcranial magnetic stimulation (TMS) treatment of depression in bipolar affective disorder: a pilot study of acute safety and efficacy. Bipolar Disord. 2003;5:40–7. doi: 10.1034/j.1399-5618.2003.00011.x.
    1. Brunoni AR, Nitsche MA, Bolognini N, Bikson M, Wagner T, Merabet L, et al. Clinical research with transcranial direct current stimulation (tDCS): challenges and future directions. Brain Stimul. 2012;5:175–95. doi: 10.1016/j.brs.2011.03.002.
    1. Cocchi L, Zalesky A, Fornito A, Mattingley JB. Dynamic cooperation and competition between brain systems during cognitive control. Trends Cogn Sci. 2013;17:493–501. doi: 10.1016/j.tics.2013.08.006.
    1. Beeli G, Koeneke S, Gasser K, Jancke L. Brain stimulation modulates driving behavior. Behav Brain Funct. 2008;4:34. doi: 10.1186/1744-9081-4-34.
    1. Power JD, Cohen AL, Nelson SM, Wig GS, Barnes KA, Church JA, et al. Functional network organization of the human brain. Neuron. 2011;72:665–78. doi: 10.1016/j.neuron.2011.09.006.
    1. Zanto TP, Gazzaley A. Fronto-parietal network: flexible hub of cognitive control. Trends Cogn Sci. 2013;17:602–3. doi: 10.1016/j.tics.2013.10.001.
    1. Cocchi L, Halford GS, Zalesky A, Harding IH, Ramm BJ, Cutmore T, et al. Complexity in relational processing predicts changes in functional brain network dynamics. Cereb Cortex. 2014;24:2283–96. doi: 10.1093/cercor/bht075.
    1. Dosenbach NUF, Fair DA, Cohen AL, Schlaggar BL, Petersen SE. A dual-networks architecture of top-down control. Trends Cogn Sci (Regul Ed) 2008;12:99–105. doi: 10.1016/j.tics.2008.01.001.
    1. Nomura EM, Gratton C, Visser RM, Kayser A, Perez F, D’Esposito M. Double dissociation of two cognitive control networks in patients with focal brain lesions. Proc Natl Acad Sci U S A. 2010;107:12017–22. doi: 10.1073/pnas.1002431107.
    1. De Bruijn MAAM, Synhaeve NE, van Rijsbergen MWA, de Leeuw F-E, Jansen BPW, de Kort PLM. Long-term cognitive outcome of ischaemic stroke in young adults. Cerebrovasc Dis. 2014;37:376–81. doi: 10.1159/000362592.
    1. Wyrwich KW, Tierney WM, Wolinsky FD. Further evidence supporting an SEM-based criterion for identifying meaningful intra-individual changes in health-related quality of life. J Clin Epidemiol. 1999;52:861–73. doi: 10.1016/S0895-4356(99)00071-2.
    1. Valiengo L, Benseñor IM, Goulart AC, de Oliveira JF, Zanao TA, Boggio PS, et al. The sertraline versus electrical current therapy for treating depression clinical study (select-TDCS): results of the crossover and follow-up phases. Depress Anxiety. 2013;30:646–53. doi: 10.1002/da.22079.
    1. Fertonani A, Ferrari C, Mninussi C. What do you feel if I apply transcranial electric stimulation? Safety, sensations and secondary induced effects. Clin Neurophysiol. 2015; doi: 10.1016/j.clinph.2015.03.015. [Epub ahead of print].
    1. Nitsche MA, Liebetanz D, Lang N, Antal A, Tergau F, Paulus W. Safety criteria for transcranial direct current stimulation (tDCS) in humans. Clin Neurophysiol. 2003;114(11):2220–2. doi: 10.1016/S1388-2457(03)00235-9.
    1. Chan A-W, Tetzlaff JM, Altman DG, Laupacis A, Gøtzsche PC, Krleža-Jerić K, et al. SPIRIT 2013 Statement: Defining standard protocol items for clinical trials. Ann Intern Med. 2013;158:200–7. doi: 10.7326/0003-4819-158-3-201302050-00583.
    1. Elsner B, Kugler J, Pohl M, Mehrholz J. Transcranial direct current stimulation (tDCS) for improving function and activities of daily living in patients after stroke. Cochrane Database Syst Rev. 2013;11:CD009645.
    1. Winkens I, Van Heugten CM, Wade DT, Habets EJ, Fasotti L. Efficacy of time pressure management in stroke patients with slowed information processing: a randomized controlled trial. Arch Phys Med Rehabil. 2009;90:1672–9. doi: 10.1016/j.apmr.2009.04.016.
    1. Fure B, Bruun Wyller T, Engedal K, Thommessen B. Cognitive impairments in acute lacunar stroke. Acta Neurol Scand. 2006;114:17–22. doi: 10.1111/j.1600-0404.2006.00603.x.
    1. Kendrick DC. The Kendrick Battery of tests: theoretical assumptions and clinical uses. Br J Soc Clin Psychol. 1972;11:373–86. doi: 10.1111/j.2044-8260.1972.tb00828.x.
    1. Reitan RM. The relation of the trail making test to organic brain damage. J Consult Psychol. 1955;19:393–4. doi: 10.1037/h0044509.
    1. Bernspång B, Fugl-Meyer AR, Viitanen M. Perceptual function in the elderly and after stroke. Scand J Caring Sci. 1988;2:75–9. doi: 10.1111/j.1471-6712.1988.tb00349.x.
    1. Brott T, Adams HP, Olinger CP, Marler JR, Barsan WG, Biller J, et al. Measurements of acute cerebral infarction: a clinical examination scale. Stroke. 1989;20:864–70. doi: 10.1161/01.STR.20.7.864.
    1. American Psychiatric Association . Diagnostic and statistical manual of mental disorders. Washington: American Psychiatric Association; 1987.
    1. Nasreddine ZS, Phillips NA, Bédirian V, Charbonneau S, Whitehead V, Collin I, et al. The montreal cognitive assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc. 2005;53:695–9. doi: 10.1111/j.1532-5415.2005.53221.x.
    1. Mattis S. Dementia rating scale. Professional manual. Florida: Psychological Assessment Resources; 1988.
    1. Radloff LS. The CES-D scale: a self-report depression scale for research in the general population. Appl Psychol Meas. 1977;1:385–401. doi: 10.1177/014662167700100306.
    1. Foerster A, Rocha S, Wiesiolek C, Chagas AP, Machado G, Silva E, et al. Site-specific effects of mental practice combined with transcranial direct current stimulation on motor learning. Eur J Neurosci. 2013;37:786–94. doi: 10.1111/ejn.12079.
    1. Monti A, Cogiamanian F, Marceglia S, Ferrucci R, Mameli F, Mrakic-Sposta S, et al. Improved naming after transcranial direct current stimulation in aphasia. J Neurol Neurosurg Psychiatr. 2008;79:451–3. doi: 10.1136/jnnp.2007.135277.
    1. Cattaneo Z, Pisoni A, Papagno C. Transcranial direct current stimulation over Broca’s region improves phonemic and semantic fluency in healthy individuals. Neuroscience. 2011;183:64–70. doi: 10.1016/j.neuroscience.2011.03.058.
    1. Boggio PS, Ferrucci R, Rigonatti SP, Covre P, Nitsche M, Pascual-Leone A, et al. Effects of transcranial direct current stimulation on working memory in patients with Parkinson’s disease. J Neurol Sci. 2006;249:31–8. doi: 10.1016/j.jns.2006.05.062.
    1. Wilson BA, Alderman N, Burgess PW. Behavioural assessment of the dysexecutive syndrome. Bury St. Edmund: Thames Valley Test Company; 1996.
    1. Emmanouel A, Mouza E, Kessels RPC, Fasotti L. Validity of the Dysexecutive Questionnaire (DEX). Ratings by patients with brain injury and their therapists. Brain Inj. 2014;28:1581–9. doi: 10.3109/02699052.2014.942371.
    1. Troyer AK. Normative data for clustering and switching on verbal fluency tasks. J Clin Exp Neuropsychol. 2000;22:370–8. doi: 10.1076/1380-3395(200006)22:3;1-V;FT370.
    1. Rubia K, Russell T, Overmeyer S, Brammer MJ, Bullmore ET, Sharma T, et al. Mapping motor inhibition: conjunctive brain activations across different versions of go/no-go and stop tasks. Neuroimage. 2001;13:250–61. doi: 10.1006/nimg.2000.0685.
    1. Wechsler D. Wechsler adult intelligence scale-III. Nova York: Psychological Corporation; 1997.
    1. Rey A. L’Examen clinique en psychologie. Paris: Press Universitaire de France; 1958.
    1. Salthouse TA, Kersten AW. Decomposing adult age differences in symbol arithmetic. Mem Cognit. 1993;21:699–710. doi: 10.3758/BF03197200.
    1. Manly T, Hawkins K, Evans J, Woldt K, Robertson IH. Rehabilitation of executive function: facilitation of effective goal management on complex tasks using periodic auditory alerts. Neuropsychologia. 2002;40:271–81. doi: 10.1016/S0028-3932(01)00094-X.
    1. Levine B, Stuss DT, Winocur G, Binns MA, Fahy L, Mandic M, et al. Cognitive rehabilitation in the elderly: effects on strategic behavior in relation to goal management. J Int Neuropsychol Soc. 2007;13:143–52. doi: 10.1017/S1355617707070178.
    1. Schweizer TA, Levine B, Rewilak D, O’Connor C, Turner G, Alexander MP, et al. Rehabilitation of executive functioning after focal damage to the cerebellum. Neurorehabil Neural Repair. 2008;22:72–7. doi: 10.1177/1545968307305303.
    1. Rolls ET, Hornak J, Wade D, McGrath J. Emotion-related learning in patients with social and emotional changes associated with frontal lobe damage. J Neurol Neurosurg Psychiatr. 1994;57:1518–24. doi: 10.1136/jnnp.57.12.1518.
    1. Rogers RD, Owen AM, Middleton HC, Williams EJ, Pickard JD, Sahakian BJ, et al. Choosing between small, likely rewards and large, unlikely rewards activates inferior and orbital prefrontal cortex. J Neurosci. 1999;19:9029–38.
    1. Brunoni AR, Valiengo L, Baccaro A, Zanão TA, de Oliveira JF, Goulart A, et al. The sertraline vs. electrical current therapy for treating depression clinical study: results from a factorial, randomized, controlled trial. JAMA Psychiatry. 2013;70:383–91. doi: 10.1001/2013.jamapsychiatry.32.

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