Repetitive transcranial magnetic stimulation in the treatment of mild cognitive impairment due to cerebral small vessel disease

Cover Page

Cite item

Full Text

Abstract

Introduction. Mild cognitive impairment (MCI) negatively affects patients’ quality of life and is a risk factor for dementia. One of the main causes of MCI is cerebral small vessel disease (CSVD). The previously established link between decreased activity in the supplementary motor area (SMA) and cognitive impairment in patients with CSVD makes it possible to consider repetitive transcranial magnetic stimulation (rTMS) of the SMA with functional magnetic resonance imaging (fMRI)-assisted positioning as a promising method for treating MCI caused by CSVD.

The aim of the study was to evaluate the efficacy and tolerability of fMRI-guided rTMS of the SMA in patients with MCI caused by CSVD.

Materials and methods. Twenty patients were randomly assigned to the intervention (SMA stimulation; n = 10) and the control (vertex stimulation; n = 10) groups. All patients underwent 10 sessions of high-frequency rTMS. The MoCA scale, trail making test, Tower of London test, and copying and delayed recall in the Rey–Osterrieth complex figure test were used to assess treatment effect. Testing was conducted before, immediately after and 3 months post rTMS.

Results. The intervention group demonstrated a significant improvement in the MoCA, the Tower of London test and delayed recall in the Rey–Osterrieth complex figure test immediately after rTMS. Statistically significant improvement in the MoCA and the Tower of London test results was maintained after 3 months. No statistically significant improvements were found in the control group. Groups were comparable in the incidence of headache during and in the 24-hour period after the stimulation session, and in unpleasant sensations during the session.

Conclusion. fMRI-guided rTMS of the SMA is an effective and promising treatment method for MCI caused by CSVD, with effects lasting three or more months, and good tolerability.

About the authors

Dmitry Yu. Lagoda

Research Center of Neurology

Author for correspondence.
Email: lagoda.d@neurology.ru
ORCID iD: 0000-0002-9267-8315

junior researcher, Department of neurorehabilitation and physiotherapy

Russian Federation, Moscow

Larisa A. Dobrynina

Research Center of Neurology

Email: lagoda.d@neurology.ru
ORCID iD: 0000-0001-9929-2725

D. Sci. (Med.), Head, 3rd Neurological department

Russian Federation, Moscow

Natalya A. Suponeva

Research Center of Neurology

Email: lagoda.d@neurology.ru
ORCID iD: 0000-0003-3956-6362

D. Sci. (Med.), Professor, Corresponding Member of the Russian Academy of Sciences, principal researcher, Department of neurorehabilitation and physiotherapy

Russian Federation, Moscow

Ilya S. Bakulin

Research Center of Neurology

Email: lagoda.d@neurology.ru
ORCID iD: 0000-0003-0716-3737

Cand. Sci. (Med.), researcher, Department of neurorehabilitation and physiotherapy

Russian Federation, Moscow

Alexandra G. Poydasheva

Research Center of Neurology

Email: lagoda.d@neurology.ru
ORCID iD: 0000-0003-1841-1177

junior researcher, neurologist, Department of neurorehabilitation and physiotherapy

Russian Federation, Moscow

Mariia M. Tsypushtanova

Research Center of Neurology

Email: lagoda.d@neurology.ru
ORCID iD: 0000-0002-4231-3895

postgraduate student, 3rd Neurological department

Russian Federation, Moscow

Albert S. Kadykov

Research Center of Neurology

Email: lagoda.d@neurology.ru
ORCID iD: 0000-0001-7491-7215

D. Sci. (Med.), Professor, senior researcher, 3rd Neurological department

Russian Federation, Moscow

Mikhail A. Piradov

Research Center of Neurology

Email: lagoda.d@neurology.ru
ORCID iD: 0000-0002-6338-0392

D. Sci. (Med.), Professor, Academician of the Russian Academy of Sciences, Director

Russian Federation, Moscow

References

  1. 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. PMID: 22265588.
  2. 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. PMID: 31993915.
  3. Wallin A., Nordlund A., Jonsson M. et al. The Gothenburg MCI study: design and distribution ofAlzheimer’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. PMID: 26174331.
  4. 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. PMID: 29446769.
  5. Lefaucheur J.P., Aleman A., Baeken C. et al. Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS): an update (2014-2018). Clin Neurophysiol. 2020;131(2):474-528. DOI: 10.1016/j. clinph.2019.11.002. Erratum in: Clin Neurophysiol. 2020;131(5):1168-1169. PMID: 31901449.
  6. Drumond Marra H.L., Myczkowski M.L., Maia Memoria C. et al. Trans- cranial magnetic stimulation to address mild cognitive impairment in the elderly: a randomized controlled study. Behav Neurol. 2015;2015:287843. doi: 10.1155/2015/287843. PMID: 26160997.
  7. Boggio P.S., Fregni F., Bermpohl F. et al. Effect of repetitive TMS and fluoxetine on cognitive function in patients with Parkinson’s disease and concurrent depression. Mov Disord. 2005;20(9):1178-1184. doi: 10.1002/mds.20508. PMID: 15895421.
  8. 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. PMID: 19859782.
  9. 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 PMID: 15760635.
  10. Sedlackova S., Rektorova I., Fanfrdlova 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.
  11. Gadzhiyeva Z.Sh. Neuropsychological profile and structural and functional mechanisms of cognitive impairment in cerebral microangiopathy: diss. Cand. Sci. (Med.). Moscow, 2018. 163 p. (in Russ.)
  12. Weilke F., Spiegel S., Boecker H. et al. Time-resolved fMRI of activation patterns in M1 and SMA during complex voluntary movement. J Neurophysiol. 2001;85:1858-1863. doi: 10.1152/jn.2001.85.5.1858. PMID: 11353002.
  13. Chassagnon S., Minotti L., Kremer S. et al. Somatosensory, motor, and reaching/grasping responses to direct electrical stimulation of the human cingulate motor areas. J Neurosurg. 2008;109(4):593-604. DOI: 10.3171/ JNS/2008/109/10/0593. PMID: 18826345.
  14. Canas A., Juncadella M., Lau R. et al. Working memory deficits after lesions involving the supplementary motor area. Front Psychol. 2018;9:765. doi: 10.3389/fpsyg.2018.00765. PMID: 29875717.
  15. van den Heuvel O.A., Groenewegen H.J., Barkhof F. et al. Frontostriatal system in planning complexity: a parametric functional magnetic resonance version of Tower of London task. Neuroimage. 2003;18(2):367-374. DOI: 10.1016/ s1053-8119(02)00010-1. PMID: 12595190.
  16. Beynel L., Appelbaum L.G., Luber B. et al. Effects of online repetitive trans- cranial 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. PMID: 31473301.
  17. 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. PMID: 32033106.
  18. Ramos Nunez A.I., Yue Q., Pasalar S., Martin R.C. The role of left vs. right superior temporal gyrus in speech perception: an fMRI-guided TMS study. Brain Lang. 2020;209:104838. doi: 10.1016/j.bandl.2020.104838. PMID: 32801090.
  19. 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):CR132-9. doi: 10.12659/msm.881446. PMID: 21358599.
  20. Chou Y.H., Ton That V., Chen A.Y. et al. TMS-induced seizure cases stratified by population, stimulation protocol, and stimulation site: a systematic literature search. Clin Neurophysiol. 2020;131(5):1019-1020. DOI: 10.1016/j. clinph.2020.02.008. PMID: 32193163.
  21. Rossi S., Antal A., Bestmann S. et al. Safety and recommendations for TMS use in healthy subjects and patient populations, with updates on training, ethical and regulatory issues: expert guidelines. Clin Neurophysiol. 2021;132(1):269- 306. doi: 10.1016/j.clinph.2020.10.003. PMID: 33243615.
  22. Bakulin I.S., Poydasheva A.G., Lagoda D.Yu. et al. Safety and tolerability of different protocols of high-frequency rhythmic transcranial magnetic stimulation. Ul’yanovskiy mediko-biologicheskiy zhurnal. 2019;(1):26-37. doi: 10.34014/2227-1848-2019-1-26-37. (in Russ.)
  23. 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. PMID: 24632990.
  24. 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. PMID: 23867200.
  25. Nasreddine Z.S., Phillips N.A., Bedirian V. et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc. 2005;53(4):695-699. doi: 10.1111/j.1532-5415.2005.53221.x. PMID: 15817019.
  26. Lezak M.D., Howieson D.B., Loring D.W., Fischer J.S. Neuropsychological assessment. N.Y.: Oxford University Press, 2012.
  27. Dobrynina L.A., Gadzhiyeva Z.Sh., Morozova S.N. et al. Executive functions: fMRI of healthy volunteers during Stroop test and the serial count test. Zhurnal nevrologii i psikhiatrii im. S.S. Korsakova. 2018;118(11):64-71. doi: 10.17116/jnevro201811811164. (in Russ.)
  28. Dobrynina L.A., Gadzhiyeva Z.Sh., Morozova S.N. et al. Method of detecting activation zones for assessment of brain control functions: Patent Russia No. 2688993, 2018. (in Russ.)
  29. Tymowski M., Kaspera W., Metta-Pieszka J. et al. Neuropsychological assessment of patients undergoing surgery due to low-grade glioma involving the supplementary motor area. Clin Neurol Neurosurg. 2018;175:1-8. DOI: 10.1016/j. clineuro.2018.09.036. PMID: 30292977.
  30. Leek E.C., Yuen K.S., Johnston S.J. Domain general sequence operations contribute to Pre-SMA involvement in visuo-spatial processing. Front Hum Neurosci. 2016;10:9. doi: 10.3389/fnhum.2016.00009. PMID: 26858623.
  31. Serra L., Gabrielli G.B., Tuzzi E. et al. Damage to the frontal aslant tract accounts for visuo-constructive deficits in Alzheimer’s disease. J Alzheimers Dis. 2017;60(3):1015-1024. doi: 10.3233/JAD-170638. PMID: 28984608.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Fig. 1. A flowchart of patient selection for the study.

Download (171KB)
Indexing metadata
3. Fig.2. Comparison of the MoCA test results in the intervention and control groups, before and after stimulation. А - active group; В - control group; Т0 — before stimulation; Т1 - immediately after stimulation; Т2 - 3 months after stimulation.

Download (43KB)
Indexing metadata
4. Fig.3. Comparison of the Tower of London test results in the intervention and control groups, before and after stimulation. А - intervention group; В - control group; Т0 - before stimulation; Т1 - immediately after stimulation; Т2 - 3 months after stimulation

Download (46KB)
Indexing metadata

Copyright (c) 2021 Lagoda D.Y., Dobrynina L.A., Suponeva N.A., Bakulin I.S., Poydasheva A.G., Tsypushtanova M.M., Kadykov A.S., Piradov M.A.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies