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Published in: Neurological Sciences 3/2022

01-03-2022 | Stroke | Original Article

Effects of repetitive transcranial magnetic stimulation on cerebral glucose metabolism

Authors: Yoshihiko Horimoto, Chikako Sato, Aki Inagaki, Emi Hayashi, Takuma Nozue, Suguru Morita, Yasuko Kondo, Marina Funaki, Akihiko Iida, Toshihisa Tajima, Hiroaki Hibino, Kazuo Yamada, Hidehiro Kabasawa

Published in: Neurological Sciences | Issue 3/2022

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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.
Literature
1.
go back to reference 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 48:1398–1403CrossRef 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 48:1398–1403CrossRef
2.
go back to reference Maeda F, Keenan JP, Tormos JM, Topka H, Pascual-Leone A (2000) Modulation of corticospinal excitability by repetitive transcranial magnetic stimulation. Clin Neurophysiol 111:800–805CrossRef Maeda F, Keenan JP, Tormos JM, Topka H, Pascual-Leone A (2000) Modulation of corticospinal excitability by repetitive transcranial magnetic stimulation. Clin Neurophysiol 111:800–805CrossRef
3.
go back to reference Wu T, Sommer M, Tergau F, Paulus W (2000) Lasting influence of repetitive transcranial magnetic stimulation on intracortical excitability in human subjects. Neurosci Lett 287:37–40CrossRef Wu T, Sommer M, Tergau F, Paulus W (2000) Lasting influence of repetitive transcranial magnetic stimulation on intracortical excitability in human subjects. Neurosci Lett 287:37–40CrossRef
4.
go back to reference 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 64:1802–1804CrossRef 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 64:1802–1804CrossRef
5.
go back to reference 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 36:2681–2686CrossRef 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 36:2681–2686CrossRef
6.
go back to reference 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 37:2115–2122CrossRef 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 37:2115–2122CrossRef
7.
go back to reference 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 125:2150–2206CrossRef 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 125:2150–2206CrossRef
8.
go back to reference 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 108:1–16CrossRef 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 108:1–16CrossRef
9.
go back to reference 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 9:4–14CrossRef 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 9:4–14CrossRef
10.
go back to reference 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 128:100–106CrossRef 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 128:100–106CrossRef
11.
go back to reference 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 7:13–31PubMed 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 7:13–31PubMed
12.
go back to reference Podsiadlo D, Richardson S (1991) The timed “Up & Go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc 39:142–148CrossRef Podsiadlo D, Richardson S (1991) The timed “Up & Go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc 39:142–148CrossRef
13.
go back to reference 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 41:177–183CrossRef 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 41:177–183CrossRef
14.
go back to reference 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 25:1668–1674CrossRef 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 25:1668–1674CrossRef
15.
go back to reference 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 22:17–24CrossRef 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 22:17–24CrossRef
16.
go back to reference 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 54:956–963CrossRef 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 54:956–963CrossRef
17.
go back to reference Murase N, Duque J, Mazzocchio R, Cohen LG (2004) Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol 55:400–409CrossRef Murase N, Duque J, Mazzocchio R, Cohen LG (2004) Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol 55:400–409CrossRef
Metadata
Title
Effects of repetitive transcranial magnetic stimulation on cerebral glucose metabolism
Authors
Yoshihiko Horimoto
Chikako Sato
Aki Inagaki
Emi Hayashi
Takuma Nozue
Suguru Morita
Yasuko Kondo
Marina Funaki
Akihiko Iida
Toshihisa Tajima
Hiroaki Hibino
Kazuo Yamada
Hidehiro Kabasawa
Publication date
01-03-2022
Publisher
Springer International Publishing
Published in
Neurological Sciences / Issue 3/2022
Print ISSN: 1590-1874
Electronic ISSN: 1590-3478
DOI
https://doi.org/10.1007/s10072-021-05539-x

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