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Effects of repetitive transcranial magnetic stimulation on cerebral glucose metabolism

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Abstract

Objective

To investigate the mechanisms underlying the effect of repetitive transcranial magnetic stimulation (rTMS) on post-stroke hemiplegia, we assessed alterations in cerebral glucose metabolism.

Methods

Five post-stroke hemiplegic patients (three targeted for upper limb impairment and two targeted for lower limb impairment) aged 62.6 ± 6.1 years (mean ± standard deviation) with a duration since stroke onset of 3.5 ± 3.8 years participated in this preliminary study. Cerebral glucose metabolism was measured twice—before and after rTMS with intensive rehabilitation—using positron emission tomography with [18F]fluorodeoxyglucose. The Asymmetry Index (AI) was calculated to assess laterality of metabolism between the lesional and contralesional motor areas. The alteration rates of AI (%ΔAI) were compared between participants in whom rTMS was effective and ineffective.

Results

Two of the three upper-limb-targeted patients and one of the two lower-limb-targeted patients showed motor function improvements following rTMS treatment. All three patients who responded to rTMS had improved laterality of cerebral glucose metabolism in motor areas, commonly in the precentral gyrus, with an %ΔAI of approximately 10%. In contrast, the two patients who did not respond to rTMS had no improvements in laterality.

Conclusions

These results suggest for the first time that improved glucose metabolism is associated with improved motor function after a combination of rTMS and intensive rehabilitation.

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Data availability

Anonymized data are available by request to the corresponding author.

Code availability

Not applicable.

References

  1. Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, Cohen LG (1997) Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48:1398–1403

    Article  CAS  Google Scholar 

  2. Maeda F, Keenan JP, Tormos JM, Topka H, Pascual-Leone A (2000) Modulation of corticospinal excitability by repetitive transcranial magnetic stimulation. Clin Neurophysiol 111:800–805

    Article  CAS  Google Scholar 

  3. Wu T, Sommer M, Tergau F, Paulus W (2000) Lasting influence of repetitive transcranial magnetic stimulation on intracortical excitability in human subjects. Neurosci Lett 287:37–40

    Article  CAS  Google Scholar 

  4. Mansur CG, Fregni F, Boggio PS, Riberto M, Gallucci-Neto J, Santos CM, Wagner T, Rigonatti SP, Marcolin MA, Pascual-Leone A (2005) A sham stimulation-controlled trial of rTMS of the unaffected hemisphere in stroke patients. Neurology 64:1802–1804

    Article  CAS  Google Scholar 

  5. Takeuchi N, Chuma T, Matsuo Y, Watanabe I, Ikoma K (2005) Repetitive transcranial magnetic stimulation of contralesional primary motor cortex improves hand function after stroke. Stroke 36:2681–2686

    Article  Google Scholar 

  6. Fregni F, Boggio PS, Valle AC, Rocha RR, Duarte J, Ferreira MJ, Wagner T, Fecteau S, Rigonatti SP, Riberto M, Freedman SD, Pascual-Leone A (2006) A sham-controlled trial of a 5-day course of repetitive transcranial magnetic stimulation of the unaffected hemisphere in stroke patients. Stroke 37:2115–2122

    Article  Google Scholar 

  7. Lefaucheur JP, André-Obadia N, Antal A, Ayache SS, Baeken C, Benninger DH, Cantello RM, Cincotta M, de Carvalho M, De Ridder D, Devanne H, Di Lazzaro V, Filipović SR, Hummel FC, Jääskeläinen SK, Kimiskidis VK, Koch G, Langguth B, Nyffeler T, Oliviero A, Padberg F, Poulet E, Rossi S, Rossini PM, Rothwell JC, Schönfeldt-Lecuona C, Siebner HR, Slotema CW, Stagg CJ, Valls-Sole J, Ziemann U, Paulus W, Garcia-Larrea L (2014) Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS). Clin Neurophysiol 125:2150–2206

    Article  Google Scholar 

  8. Wassermann EM (1998) Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5–7, 1996. Electroencephalogr Clin Neurophysiol 108:1–16

    Article  CAS  Google Scholar 

  9. Kakuda W, Abo M, Shimizu M, Sasanuma J, Okamoto T, Yokoi A, Taguchi K, Mitani S, Harashima H, Urushidani N, Urashima M, Investigators NEURO (2012) A multi-center study on low-frequency rTMS combined with intensive occupational therapy for upper limb hemiparesis in post-stroke patients. J Neuroeng Rehabil 9:4–14

    Article  Google Scholar 

  10. Kakuda W, Abo M, Nakayama Y, Kiyama A, Yoshida H (2013) High-frequency rTMS using a double cone coil for gait disturbance. Acta Neurol Scand 128:100–106

    Article  CAS  Google Scholar 

  11. Fugl-Meyer AR, Jääskö L, Leyman I, Olsson S, Steglind S (1975) The post-stroke hemiplegic patient. 1. A method for evaluation of physical performance. Scand J Rehabil Med 7:13–31

    CAS  PubMed  Google Scholar 

  12. Podsiadlo D, Richardson S (1991) The timed “Up & Go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc 39:142–148

    Article  CAS  Google Scholar 

  13. Takekawa T, Kakuda W, Uchiyama M, Ikegaya M, Abo M (2014) Brain perfusion and upper limb motor function: a pilot study on the correlation between evolution of asymmetry in cerebral blood flow and improvement in Fugl-Meyer Assessment score after rTMS in chronic post-stroke patients. J Neuroradiol 41:177–183

    Article  Google Scholar 

  14. Könönen M, Kuikka JT, Husso-Saastamoinen M, Vanninen E, Vanninen R, Soimakallio S, Mervaala E, Sivenius J, Pitkänen K, Tarkka IM (2005) Increased perfusion in motor areas after constraint-induced movement therapy in chronic stroke: a single-photon emission computerized tomography study. J Cereb Blood Flow Metab 25:1668–1674

    Article  Google Scholar 

  15. Colamussi P, Giganti M, Cittanti C, Dovigo L, Trotta F, Tola MR, Tamarozzi R, Lucignani G, Piffanelli A (1995) Brain single-photon emission tomography with 99mTc-HMPAO in neuropsychiatric systemic lupus erythematosus; relations with EEG and MRI findings and clinical manifestations. Eur J Nucl Med 22:17–24

    Article  CAS  Google Scholar 

  16. Siebner HR, Peller M, Willoch F, Minoshima S, Boecker H, Auer C, Drzezga A, Conrad B, Bartenstein P (2000) Lasting cortical activation after repetitive TMS of the motor cortex: a glucose metabolic study. Neurology 54:956–963

    Article  CAS  Google Scholar 

  17. Murase N, Duque J, Mazzocchio R, Cohen LG (2004) Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol 55:400–409

    Article  Google Scholar 

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Acknowledgements

We are grateful to the late Dr. Michitaka Matsubara, former Director of Department of Planning and Research, Nagoya City Rehabilitation Center, for his kind suggestions during his lifetime.

Funding

This study was funded by The Rehabilitation Research Fund of Social Welfare Corporation Nagoya City Rehabilitation Agency.

Author information

Authors and Affiliations

  1. Department of Neurology, Nagoya City Rehabilitation Center, 1-2, Mikan-yama, Yatomi-cho, Mizuho, Nagoya, 467-8622, Japan

    Yoshihiko Horimoto, Chikako Sato, Aki Inagaki, Toshihisa Tajima, Hiroaki Hibino & Hidehiro Kabasawa

  2. Department of Radiology, Nagoya City Rehabilitation Center, Nagoya, Japan

    Emi Hayashi & Akihiko Iida

  3. Department of Physical Therapy, Nagoya City Rehabilitation Center, Nagoya, Japan

    Takuma Nozue & Marina Funaki

  4. Department of Occupational Therapy, Nagoya City Rehabilitation Center, Nagoya, Japan

    Suguru Morita

  5. Department of Nursing, Nagoya City Rehabilitation Center, Nagoya, Japan

    Yasuko Kondo

  6. Department of Neurosurgery, Nagoya City Rehabilitation Center, Nagoya, Japan

    Kazuo Yamada

Authors
  1. Yoshihiko Horimoto
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  2. Chikako Sato
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  3. Aki Inagaki
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  4. Emi Hayashi
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  5. Takuma Nozue
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  7. Yasuko Kondo
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  8. Marina Funaki
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  10. Toshihisa Tajima
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  11. Hiroaki Hibino
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  12. Kazuo Yamada
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  13. Hidehiro Kabasawa
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Contributions

All authors have read the manuscript and have approved this submission

Yoshihiko Horimoto recruitment of patients, performing TMS

Chikako Sato recruitment of patients, performing TMS

Aki Inagaki recruitment of patients, performing TMS

Emi Hayashi scanning and analyzing of images

Takuma Nozue assessment of impairment, performing rehabilitation

Suguru Morita assessment of impairment, performing rehabilitation

Yasuko Kondo performing TMS

Marina Funaki recruitment of patients, assessment of impairment

Akihiko Iida scanning and analyzing of images

Toshihisa Tajima recruitment of patients

Hiroaki Hibino recruitment of patients

Kazuo Yamada recruitment of patients

Hidehiro Kabasawa recruitment of patients

Corresponding author

Correspondence to Yoshihiko Horimoto.

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Conflict of interest

The authors declare no competing interests.

Ethics approval

This study was approved by The Ethics Committee of Nagoya City Rehabilitation Center.

Consent to participate

All participants gave written informed consent to participate.

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All authors have read and agree with the contents of the manuscript for publication.

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Horimoto, Y., Sato, C., Inagaki, A. et al. Effects of repetitive transcranial magnetic stimulation on cerebral glucose metabolism. Neurol Sci 43, 1879–1883 (2022). https://doi.org/10.1007/s10072-021-05539-x

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  • DOI: https://doi.org/10.1007/s10072-021-05539-x

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