Functional MRI-guided repetitive transcranial magnetic stimulation in cognitive impairment in cerebral small vessel disease
- Authors: Lagoda D.Y.1, Bakulin I.S.1, Poydasheva A.G.1, Sinitsyn D.O.1, Zabirova A.K.1, Gadzhieva Z.S.1, Zabitova M.R.1, Shamtieva K.V.1, Dobrynina L.A.1, Suponeva N.A.1, Piradov M.A.1
-
Affiliations:
- Research Center of Neurology
- Issue: Vol 18, No 2 (2024)
- Pages: 24-33
- Section: Original articles
- URL: https://journals.rcsi.science/2075-5473/article/view/262416
- DOI: https://doi.org/10.17816/ACEN.1087
- ID: 262416
Cite item
Abstract
Introduction. Cerebral small vessel disease (CSVD) is one of the leading causes of vascular and mixed cognitive impairment (CI). Treatment options for CSVD-associated CI are limited. Repetitive transcranial magnetic stimulation (rTMS) is a promising non-drug treatment option.
The aim of the study was to evaluate the effects of 10 rTMS sessions of the left dorsolateral prefrontal cortex (DLPFC) on cognitive functions in CSVD patients.
Materials and methods. The study included 30 patients with CSVD and moderate CI randomized to the active (DLPFC stimulation; n = 20) and control (vertex stimulation; n = 10) groups. Both groups received 10 sessions of high-frequency rTMS. The DLPFC target was selected based on the individual paradigm fMRI data with a focus on executive functions. Cognitive function was assessed using the Montreal Cognitive Assessment Scale (MoCA), the Trail Making Test (TMT), the Tower of London Test, and the Rey–Osterrieth Complex Figure Test before, immediately after, and 3 months after the stimulation. Adverse events were assessed using standardized questionnaires.
Results. The active group showed a significantly better effect compared to the control group according to MoCA, TMT A and B, The Tower of London Test, delayed recall on the Rey–Osterrieth Complex Figure Test immediately after the stimulation and MoCA, TMT A and B and The Tower of London 3 months after the stimulation. Adverse events in the study were mild and did not affect treatment adherence.
Conclusion. rTMS is a promising, safe, and well-tolerated treatment option for mild cognitive impairment in CSVD. However, additional research is needed to make recommendations for its clinical use.
Full Text
##article.viewOnOriginalSite##About the authors
Dmitry Yu. Lagoda
Research Center of Neurology
Author for correspondence.
Email: lagoda.d@neurology.ru
ORCID iD: 0000-0002-9267-8315
Cand. Sci. (Med.), researcher, Noninvasive neuromo- dulation group, Institute of Neurorehabilitation and Rehabilitation Medicine, Research Center of Neurology
Russian Federation, MoscowIlya S. Bakulin
Research Center of Neurology
Email: bakulinilya@gmail.com
ORCID iD: 0000-0003-0716-3737
Cand. Sci. (Med.), senior researcher, Head, Noninvasive neuromodulation group, Institute of Neurorehabilitation and Rehabilitation Medicine, Research Center of Neurology
Russian Federation, MoscowAlexandra G. Poydasheva
Research Center of Neurology
Email: alexandra.poydasheva@gmail.com
ORCID iD: 0000-0003-1841-1177
Cand. Sci. (Med.), researcher, Noninvasive neuromodulation group, Institute of Neurorehabilitation and Rehabilitation Medicine, Research Center of Neurology
Russian Federation, MoscowDmitry O. Sinitsyn
Research Center of Neurology
Email: d_sinitsyn@mail.ru
ORCID iD: 0000-0001-9951-9803
Cand. Sci. (Physics and Math.), researcher, Institute of neurorehabilitation and rehabilitation medicine, Research Center of Neurology
Russian Federation, MoscowAlfiia K. Zabirova
Research Center of Neurology
Email: alfijasabirowa@gmail.com
ORCID iD: 0000-0001-8544-3107
postgraduate student, neurologist, Research Center of Neurology
Russian Federation, MoscowZukhra S. Gadzhieva
Research Center of Neurology
Email: zuhradoc@mail.ru
ORCID iD: 0000-0001-7498-4063
Cand. Sci. (Med.), neurologist, 3rd Neurological department, Institute of Clinical and Preventive Neurology, Research Center of Neurology
Russian Federation, MoscowMaryam R. Zabitova
Research Center of Neurology
Email: gadjieva@neurology.ru
ORCID iD: 0000-0003-2523-333X
Cand. Sci. (Med.), researcher, 3rd Neurological department, Institute of Clinical and Preventive Neurology, Research Center of Neurology
Russian Federation, MoscowKamila V. Shamtieva
Research Center of Neurology
Email: kamila.shamt@gmail.com
ORCID iD: 0000-0002-6995-1352
Cand. Sci. (Med.), researcher, 3rd Neurological department, Institute of Clinical and Preventive Neurology, Research Center of Neurology
Russian Federation, MoscowLarisa A. Dobrynina
Research Center of Neurology
Email: dobrla@mail.ru
ORCID iD: 0000-0001-9929-2725
D. Sci. (Med.), chief researcher, Head, 3rd Neurological department, Institute of Clinical and Preventive Neurology, Research Center of Neurology
Russian Federation, MoscowNatalia A. Suponeva
Research Center of Neurology
Email: nasu2709@mail.ru
ORCID iD: 0000-0003-3956-6362
D. Sci. (Med.), Corresponding Member of the Russian Academy of Sciences, Director, Institute of Neurorehabilitation and Resto- rative Technologies, Research Center of Neurology
Russian Federation, MoscowMichael A. Piradov
Research Center of Neurology
Email: mpi711@gmail.com
ORCID iD: 0000-0002-6338-0392
D. Sci. (Med.), Academician of the Russian Academy of Sciences, Director, Research Center of Neurology
Russian Federation, MoscowReferences
- Wallin A., Nordlund A., Jonsson M. et al. The Gothenburg MCI study: design and distribution of Alzheimer's disease and subcortical vascular disease diagnoses from baseline to 6-year follow-up. J. Cereb. Blood Flow Metab. 2016;36(1):114–131. doi: 10.1038/jcbfm.2015.147
- Pantoni L. Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol. 2010;9(7):689–701. doi: 10.1016/S1474-4422(10)70104-6
- van der Flier W.M., Skoog I., Schneider J.A. et al. Vascular cognitive impairment. Nat. Rev. Dis. Primers. 2018;4:18003. doi: 10.1038/nrdp.2018.3
- Ritter A., Pillai J.A. Treatment of vascular cognitive impairment. Curr. Treat. Options Neurol. 2015;17(8):367. doi: 10.1007/s11940-015-0367-0
- Petersen R.C. Clinical practice. Mild cognitive impairment. N. Engl. J. Med. 2011;364(23):2227–2234. doi: 10.1056/NEJMcp0910237
- Ward A., Arrighi H.M., Michels S., Cedarbaum J.M. Mild cognitive impairment: disparity of incidence and prevalence estimates. Alzheimers Dement. 2012;8(1):14–21. doi: 10.1016/j.jalz.2011.01.002
- Hussenoeder F.S., Conrad I., Roehr S. et al. Mild cognitive impairment and quality of life in the oldest old: a closer look. Qual. Life Res. 2020;29(6):1675–1683. doi: 10.1007/s11136-020-02425-5
- Lefaucheur J.P., Aleman A., Baeken C. et al. Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS): аn update (2014-2018). Clin. Neurophysiol. 2020;131(2):474–528. doi: 10.1016/j.clinph.2019.11.002
- Chervyakov A.V., Chernyavsky A.Y., Sinitsyn D.O., Piradov M.A. Possible mechanisms underlying the therapeutic effects of transcranial magnetic stimulation. Front. Hum. Neurosci. 2015;9:303. doi: 10.3389/fnhum.2015.00303
- Lin Y., Jiang W.J., Shan P.Y. et al. The role of repetitive transcranial magnetic stimulation (rTMS) in the treatment of cognitive impairment in patients with Alzheimer's disease: A systematic review and meta-analysis. J. Neurol. Sci. 2019;398:184–191. doi: 10.1016/j.jns.2019.01.038
- Drumond Marra H.L., Myczkowski M.L., Maia Memória C. et al. Transcranial magnetic stimulation to address mild cognitive impairment in the elderly: a randomized controlled study. Behav. Neurol. 2015;2015:287843. doi: 10.1155/2015/287843
- Rektorova I., Megova S., Bares M., Rektor I. Cognitive functioning after repetitive transcranial magnetic stimulation in patients with cerebrovascular disease without dementia: a pilot study of seven patients. J. Neurol. Sci. 2005;229-230:157–161. doi: 10.1016/j.jns.2004.11.021
- Sedlackova S., Rektorová I., Fanfrdlová Z., Rektor I. Neurocognitive effects of repetitive transcranial magnetic stimulation in patients with cerebrovascular disease without dementia. J. Psychophysiol. 2008;22(1):14–19. doi: 10.1027/0269-8803.22.1.14
- Лагода Д.Ю., Добрынина Л.А., Супонева Н.А. и др. Ритмическая транскраниальная магнитная стимуляция в терапии умеренных когнитивных расстройств при церебральной микроангиопатии. Анналы клинической и экспериментальной неврологии. 2021;15(4):5–14. doi: 10.54101/ACEN.2021.4.1
- Modak A., Fitzgerald P.B. Personalising transcranial magnetic stimulation for depression using neuroimaging: а systematic review. World J. Biol. Psychiatry. 2021;22(9):647–669. doi: 10.1080/15622975.2021.1907710
- Barbour T., Lee E., Ellard K., Camprodon J. Individualized TMS target selection for MDD: сlinical outcomes, mechanisms of action and predictors of response. Brain Stimul. 2019;12(2):516. doi: 10.1186/s12888-020-03030-z
- Cash R.F.H., Weigand A., Zalesky A. et al. Using brain imaging to improve spatial targeting of transcranial magnetic stimulation for depression. Biological Psychiatry. 2020;7:S0006-3223(20)31668-1. doi: 10.1016/j.biopsych.2020.05.033
- Пойдашева А.Г., Синицын Д.О., Бакулин И.С. и др. Определение мишени для транскраниальной магнитной стимуляции у пациентов с резистентным к фармакотерапии депрессивным эпизодом на основе индивидуальных параметров функциональной магнитно-резонансной томографии покоя (пилотное слепое контролируемое исследование). Неврология, нейропсихиатрия, психосоматика. 2019;11(4):44–50. doi: 10.14412/2074-2711-2019-4-44-50
- Cole E.J., Phillips A.L., Bentzley B.S. et al. Stanford Neuromodulation Therapy (SNT): a double-blind randomized controlled trial. Am. J. Psychiatry. 2021;appiajp202120101429. doi: 10.1176/appi.ajp.2021.20101429
- Beynel L., Appelbaum L.G., Luber B. et al. Effects of online repetitive transcranial magnetic stimulation (rTMS) on cognitive processing: A meta-analysis and recommendations for future studies. Neurosci. Biobehav. Rev. 2019;107:47–58. doi: 10.1016/j.neubiorev.2019.08.018
- Szaflarski J.P., Vannest J., Wu S.W. et al. Excitatory repetitive transcranial magnetic stimulation induces improvements in chronic post-stroke aphasia. Med. Sci. Monit. 2011;17(3):CR132–CR 139. doi: 10.12659/msm.881446
- Wardlaw J.M., Smith E.E., Biessels G.J. et al. Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol. 2013;12(8):822–838. doi: 10.1016/S1474-4422(13)70124-8
- Sachdev P., Kalaria R., O'Brien J. et al. Diagnostic criteria for vascular cognitive disorders: a VASCOG statement. Alzheimer Dis. Assoc. Disord. 2014;28(3):206–218. doi: 10.1097/WAD.0000000000000034
- Salvadori E., Poggesi A., Pracucci G. et al. Development and psychometric properties of a neuropsychological battery for mild cognitive impairment with small vessel disease: the VMCI-Tuscany Study. J. Alzheimers Dis. 2015;43(4):1313–1323. doi: 10.3233/JAD-141449
- Lezak M.D., Howieson D.B., Loring D.W., Fischer J.S. Neuropsychological assessment. N.Y., 2012:499–504.
- Gadzhieva Z., Kremneva E., Morozova S. et al. fMRI of healthy elderly during Stroop test and the serial count test: Comparative analysis. J. Alzheimers Dis. Parkinsonism. 2018;8:52. doi: 10.4172/2161-0460-C1-037
- Rossini P.M., Barker A.T., Berardelli A. et al. Noninvasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr. Clin. Neurophysiol. 1994;91:79–92. doi: 10.1016/0013-4694(94)90029-9
- Ter Telgte A., van Leijsen E.M.C., Wiegertjes K. et al. Cerebral small vessel disease: from a focal to a global perspective. Nat. Rev. Neurol. 2018;14(7):387–398. doi: 10.1038/s41582-018-0014-y
- Dey A.K., Stamenova V., Turner G. et al. Pathoconnectomics of cognitive impairment in small vessel disease: а systematic review. Alzheimers Dement. 2016;12(7):831–845. doi: 10.1016/j.jalz.2016.01.007
- Guse B., Falkai P., Wobrock T. Cognitive effects of high-frequency repetitive transcranial magnetic stimulation: a systematic review. J. Neural. Transm (Vienna). 2010;117(1):105–122. doi: 10.1007/s00702-009-0333-7
- Pisella L. Visual perception is dependent on visuospatial working memory and thus on the posterior parietal cortex. Ann. Phys. Rehabil. Med. 2017;60(3):141–147. doi: 10.1016/j.rehab.2016.01.002
- Rosen A.C. Targeting location relates to treatment response in active but not sham rTMS stimulation. Brain Stimul. 2021;14(3):703–709. doi: 10.1016/j.brs.2021.04.010
- Sack A.T., Cohen Kadosh R., Schuhmann T. et al. Optimizing functional accuracy of TMS in cognitive studies: a comparison of methods. J. Cogn. Neurosci. 2009;21(2):207–221. doi: 10.1162/jocn.2009.21126
- Bakulin I., Zabirova A., Lagoda D. et al. Combining HF rTMS over the left DLPFC with concurrent cognitive activity for the offline modulation of working memory in healthy volunteers: a proof-of-concept study. Brain Sci. 2020;10(2):83. doi: 10.3390/brainsci10020083
- Добрынина Л.А., Гаджиева З.Ш., Морозова С.Н. и др. Управляющие функции мозга: функциональная магнитно-резонансная томография с использованием теста Струпа и теста серийного счета про себя у здоровых добровольцев. Журнал неврологии и психиатрии им. С.С. Корсакова. 2018;118(11):64–71. doi: 10.17116/jnevro201811811164
- Elliott M.L., Knodt A.R., Ireland D. et al. What is the test-retest reliability of common task-functional MRI measures? New empirical evidence and a meta-analysis. Psychol Sci. 2020;31(7):792–806. doi: 10.1177/0956797620916786
- Sabbagh M., Sadowsky C., Tousi B. et al. Effects of a combined transcranial magnetic stimulation (TMS) and cognitive training intervention in patients with Alzheimer's disease. Alzheimers Dement. 2020;16(4):641–650. doi: 10.1016/j.jalz.2019.08.197
- Hodaj H., Alibeu J.P., Payen J.F., Lefaucheur J.P. Treatment of chronic facial pain including cluster headache by repetitive transcranial magnetic stimulation of the motor cortex with maintenance sessions: a naturalistic study. Brain Stimul. 2015;8(4):801–807. doi: 10.1016/j.brs.2015.01.416
- Chang J., Chu Y., Ren Y. et al. Maintenance treatment of transcranial magnetic stimulation (TMS) for treatment-resistant depression patients responding to acute TMS treatment. Int. J. Physiol. Pathophysiol. Pharmacol. 2020;12(5):128–133.
- Sathappan A.V., Luber B.M., Lisanby S.H. The dynamic duo: combining noninvasive brain stimulation with cognitive interventions. Prog. Neuropsychopharmacol. Biol. Psychiatry. 2019;89:347–360. doi: 10.1016/j.pnpbp.2018.10.006
- Rossi S., Hallett M., Rossini P.M., Pascual-Leone A. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin. Neurophysiol. 2009;120(12):2008–2039. doi: 10.1016/j.clinph.2009.08.016
- Pizem D., Novakova L., Gajdos M., Rektorova I. Is the vertex a good control stimulation site? Theta burst stimulation in healthy controls. J. Neural. Transm (Vienna). 2022;129(3):319–329. doi: 10.1007/s00702-022-02466-9