A Literature Review of the Efficacy of Repetitive Transcranial Magnetic Stimulation on Epilepsy
Iranian Journal of Child Neurology,
Vol. 17 No. 1 (2023),
3 January 2023
,
Page 9-28
https://doi.org/10.22037/ijcn.v17i2.38752
Abstract
Repetitive transcranial magnetic stimulation (rTMS), often recognized as a safe and tolerable method with promising therapeutic potential for the treatment of a variety of neurological disorders, has been extensively studied by medical engineering scientists in recent decades. Epilepsy has always been one of the vital foci in the
therapeutic role of rTMS, especially its low-frequency type. However, various reports, clinical trials, and review articles published in recent years have yielded conflicting results regarding the efficacy and sideeffects of rTMS in patients.
In this review article, reviewing studies published from January 2000 to October 2021, we examined the efficacy and side effects of rTMS with a specific look at its therapeutic applications in epilepsy. Our study indicates promising results in the clinical application of this technique for patients with epilepsy. Among other things, it has the ability to reduce interictal epileptic abnormalities, does not interfere with neuropsychological function in normal people, does not worsen cognitive function and even improves Stroop function, rarely has serious side effects such as seizures and psychotic symptoms, has low risk in children as adults, and has potential for improving suicidalideation.
Despite some limitations in this study, including the small number of studies performed and the heterogeneity among studies, this review article suggests significant rtMS potentials in improving the complications of epilepsy. Our review also showed that the reported side effects of using this technique are not very common. Therefore we can recommend further use of this technique as a promising tool in clinical research.
- Repetitive transcranial magnetic stimulation
- rTMS
- Epilepsy
- Seizure
How to Cite
References
2. Fisher RS, Acevedo C, Arzimanoglou A, Bogacz A, Cross JH, Elger CE, et al. ILAE official report: a practical clinical definition of epilepsy. Epilepsia. 2014;55(4):475-82. https://doi.org/10.1111/epi.12550
3. Epilepsy 2019 [Available from: https://www.who.int/en/news-room/fact-sheets/detail/epilepsy].
4. Stokes T. Clinical guidelines and evidence review for the epilepsies: diagnosis and management in adults and children in primary and secondary care. http://www nice org uk/Guidance/CG20. 2004.
5. Hammer GD, McPhee SJ, Education M-H. Pathophysiology of disease: an introduction to clinical medicine: McGraw-Hill Education Medical; 2014.
6. Hughes JR. Absence seizures: a review of recent reports with new concepts. Epilepsy & behavior. 2009;15(4):404-12. https://doi.org/10.1016/j.yebeh.2009.06.007
7. Reynolds EH. The ILAE/IBE/WHO epilepsy global campaign history. Epilepsia. 2002;43:9-11. https://doi.org/10.1046/j.1528-1157.43.s.6.5.x
8. Hesdorffer D, Logroscino G, Benn E, Katri N, Cascino G, Hauser W. Estimating risk for developing epilepsy: a population-based study in Rochester, Minnesota. Neurology. 2011;76(1):23-7. https://doi.org/10.1212/WNL.0b013e318204a36a
9. Ngugi AK, Bottomley C, Kleinschmidt I, Sander JW, Newton CR. Estimation of the burden of active and life‐time epilepsy: a meta‐analytic approach. Epilepsia. 2010;51(5):883-90. https://doi.org/10.1111/j.1528-1167.2009.02481.x
10. Stephen LJ, Brodie MJ. Epilepsy in elderly people. The Lancet. 2000;355(9213):1441-6. https://doi.org/10.1016/S0140-6736(00)02149-8
11. Pereira LS, Müller VT, da Mota Gomes M, Rotenberg A, Fregni F. Safety of repetitive transcranial magnetic stimulation in patients with epilepsy: a systematic review. Epilepsy & behavior. 2016;57:167-76. https://doi.org/10.1016/j.yebeh.2016.01.015
12. Noebels JL AM. Jasper's Basic Mechanisms of the Epilepsies. Oxford University Press; 2012. p. 466, 70. https://doi.org/10.1093/med/9780199746545.001.0001
13. Fisher RS, Boas WVE, Blume W, Elger C, Genton P, Lee P, et al. Epileptic seizures and epilepsy: definitions proposed by the International League Against Epilepsy (ILAE) and the International Bureau for Epilepsy (IBE). Epilepsia. 2005;46(4):470-2. https://doi.org/10.1111/j.0013-9580.2005.66104.x
14. Theodore WH. Transcranial magnetic stimulation in epilepsy. Epilepsy Currents. 2003;3(6):191-7. https://doi.org/10.1046/j.1535-7597.2003.03607.x
15. Kobayashi M, Pascual-Leone A. Transcranial magnetic stimulation in neurology. The Lancet Neurology. 2003;2(3):145-56. https://doi.org/10.1016/S1474-4422(03)00321-1
16. Barker AT, Jalinous R, Freeston IL. Non-invasive magnetic stimulation of human motor cortex. The Lancet. 1985;325(8437):1106-7. https://doi.org/10.1016/S0140-6736(85)92413-4
17. Carrette S, Boon P, Dekeyser C, Klooster DC, Carrette E, Meurs A, et al. Repetitive transcranial magnetic stimulation for the treatment of refractory epilepsy. Expert review of neurotherapeutics. 2016;16(9):1093-110. https://doi.org/10.1080/14737175.2016.1197119
18. Merton P, Morton H. Stimulation of the cerebral cortex in the intact human subject. Nature. 1980;285(5762):227-. https://doi.org/10.1038/285227a0
19. Cooper YA, Pianka ST, Alotaibi NM, Babayan D, Salavati B, Weil AG, et al. Repetitive transcranial magnetic stimulation for the treatment of drug‐resistant epilepsy: A systematic review and individual participant data meta‐analysis of real‐world evidence. Epilepsia Open. 2018;3(1):55-65. https://doi.org/10.1002/epi4.12092
20. Gersner R, Oberman L, Sanchez M, Chiriboga N, Kaye H, Pascual-Leone A, et al. H-coil repetitive transcranial magnetic stimulation for treatment of temporal lobe epilepsy: A case report. Epilepsy & behavior case reports. 2016;5:52-6. https://doi.org/10.1016/j.ebcr.2016.03.001
21. Maeda F, Keenan JP, Tormos JM, Topka H, Pascual-Leone A. Interindividual variability of the modulatory effects of repetitive transcranial magnetic stimulation on cortical excitability. Experimental brain research. 2000;133(4):425-30. https://doi.org/10.1007/s002210000432
22. Chen R, Classen J, Gerloff C, Celnik P, Wassermann E, Hallett M, et al. Depression of motor cortex excitability by low‐frequency transcranial magnetic stimulation. Neurology. 1997;48(5):1398-403. https://doi.org/10.1212/WNL.48.5.1398
23. Badawy R, Freestone D, Lai A, Cook M. Epilepsy: ever-changing states of cortical excitability. Neuroscience. 2012;222:89-99. https://doi.org/10.1016/j.neuroscience.2012.07.015
24. Kramer MA, Cash SS. Epilepsy as a disorder of cortical network organization. The Neuroscientist. 2012;18(4):360-72. https://doi.org/10.1177/1073858411422754
25. Machii K, Cohen D, Ramos-Estebanez C, Pascual-Leone A. Safety of rTMS to non-motor cortical areas in healthy participants and patients. Clinical Neurophysiology. 2006;117(2):455-71. https://doi.org/10.1016/j.clinph.2005.10.014
26. Fregni F, Thome-Souza S, Bermpohl F, Marcolin MA, Herzog A, Pascual-Leone A, et al. Antiepileptic effects of repetitive transcranial magnetic stimulation in patients with cortical malformations: an EEG and clinical study. Stereotactic and functional neurosurgery. 2005;83(2-3):57-62. https://doi.org/10.1159/000086674
27. Menkes DL, Gruenthal M. Slow‐frequency repetitive transcranial magnetic stimulation in a patient with focal cortical dysplasia. Epilepsia. 2000;41(2):240-2. https://doi.org/10.1111/j.1528-1157.2000.tb00146.x
28. Brighina F, Giglia G. Low-frequency transcranial magnetic stimulation in patients with cortical dysplasia-a preliminary study. J Neurol. 2003;250(761):e762. https://doi.org/10.1007/s00415-003-1080-6
29. Brasil-Neto JP, Araújo DPd, Teixeira WA, Araújo VP, Boechat-Barros R. Experimental therapy of epilepsy with transcranial magnetic stimulation: lack of additional benefit with prolonged treatment. Arquivos de neuro-psiquiatria. 2004;62:21-5. https://doi.org/10.1590/S0004-282X2004000100004
30. Misawa S, Kuwabara S, Shibuya K, Mamada K, Hattori T. Low-frequency transcranial magnetic stimulation for epilepsia partialis continua due to cortical dysplasia. Journal of the neurological sciences. 2005;234(1-2):37-9. https://doi.org/10.1016/j.jns.2005.03.035
31. Fregni F, Otachi PT, Do Valle A, Boggio PS, Thut G, Rigonatti SP, et al. A randomized clinical trial of repetitive transcranial magnetic stimulation in patients with refractory epilepsy. Annals of neurology. 2006;60(4):447-55. https://doi.org/10.1002/ana.20950
32. Sun W, Mao W, Meng X, Wang D, Qiao L, Tao W, et al. Low‐frequency repetitive transcranial magnetic stimulation for the treatment of refractory partial epilepsy: a controlled clinical study. Epilepsia. 2012;53(10):1782-9. https://doi.org/10.1111/j.1528-1167.2012.03626.x
33. Hsu W-Y, Cheng C-H, Lin M-W, Shih Y-H, Liao K-K, Lin Y-Y. Antiepileptic effects of low frequency repetitive transcranial magnetic stimulation: a meta-analysis. Epilepsy research. 2011;96(3):231-40. https://doi.org/10.1016/j.eplepsyres.2011.06.002
34. Kinoshita M, Ikeda A, Begum T, Yamamoto J, Hitomi T, Shibasaki H. Low-frequency repetitive transcranial magnetic stimulation for seizure suppression in patients with extratemporal lobe epilepsy-a pilot study. Seizure. 2005;14(6):387-92. https://doi.org/10.1016/j.seizure.2005.05.002
35. Cantello R, Rossi S, Varrasi C, Ulivelli M, Civardi C, Bartalini S, et al. Slow repetitive TMS for drug‐resistant epilepsy: clinical and EEG findings of a placebo‐controlled trial. Epilepsia. 2007;48(2):366-74. https://doi.org/10.1111/j.1528-1167.2006.00938.x
36. Seynaeve L, Devroye A, Dupont P, Van Paesschen W. Randomized crossover sham‐controlled clinical trial of targeted low‐frequency transcranial magnetic stimulation comparing a figure‐8 and a round coil to treat refractory neocortical epilepsy. Epilepsia. 2016;57(1):141-50. https://doi.org/10.1111/epi.13247
37. Theodore W, Hunter K, Chen R, Vega-Bermudez F, Boroojerdi B, Reeves-Tyer P, et al. Transcranial magnetic stimulation for the treatment of seizures: a controlled study. Neurology. 2002;59(4):560-2. https://doi.org/10.1212/WNL.59.4.560
38. Rossi S, Hallett M, Rossini PM, Pascual-Leone A, Group SoTC. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clinical neurophysiology. 2009;120(12):2008-39. https://doi.org/10.1016/j.clinph.2009.08.016
39. Hufnagel A, Elger C, Durwen H, Böker D, Entzian W. Activation of the epileptic focus by transcranial magnetic stimulation of the human brain. Annals of Neurology: Official Journal of the American Neurological Association and the Child Neurology Society. 1990;27(1):49-60. https://doi.org/10.1002/ana.410270109
40. Bae EH, Schrader LM, Machii K, Alonso-Alonso M, Riviello Jr JJ, Pascual-Leone A, et al. Safety and tolerability of repetitive transcranial magnetic stimulation in patients with epilepsy: a review of the literature. Epilepsy & behavior. 2007;10(4):521-8. https://doi.org/10.1016/j.yebeh.2007.03.004
41. Anderson B, Mishory A, Nahas Z, Borckardt JJ, Yamanaka K, Rastogi K, et al. Tolerability and safety of high daily doses of repetitive transcranial magnetic stimulation in healthy young men. The journal of ECT. 2006;22(1):49-53. https://doi.org/10.1097/00124509-200603000-00011
42. Koren D, Shefer O, Chistyakov A, Kaplan B, Feinsod M, Klein E. Neuropsychological effects of prefrontal slow rTMS in normal volunteers: a double-blind sham-controlled study. Journal of clinical and experimental neuropsychology. 2001;23(4):424-30. https://doi.org/10.1076/jcen.23.4.424.1225
43. Rossi S, Ulivelli M, Bartalini S, Galli R, Passero S, Battistini N, et al. Reduction of cortical myoclonus-related epileptic activity following slow-frequency rTMS. A case study. Neuroreport. 2004;15(2):293-6. https://doi.org/10.1097/00001756-200402090-00016
44. Fregni F, Boggio PS, Valle AC, Otachi P, Thut G, Rigonatti SP, et al. Homeostatic effects of plasma valproate levels on corticospinal excitability changes induced by 1 Hz rTMS in patients with juvenile myoclonic epilepsy. Clinical neurophysiology. 2006;117(6):1217-27. https://doi.org/10.1016/j.clinph.2006.02.015
45. Joo EY, Han SJ, Chung S-H, Cho J-W, Seo DW, Hong SB. Antiepileptic effects of low-frequency repetitive transcranial magnetic stimulation by different stimulation durations and locations. Clinical neurophysiology. 2007;118(3):702-8. https://doi.org/10.1016/j.clinph.2006.11.008
46. Santiago-Rodríguez E, Cárdenas-Morales L, Harmony T, Fernández-Bouzas A, Porras-Kattz E, Hernández A. Repetitive transcranial magnetic stimulation decreases the number of seizures in patients with focal neocortical epilepsy. Seizure. 2008;17(8):677-83. https://doi.org/10.1016/j.seizure.2008.04.005
47. Rotenberg A, Bae EH, Muller PA, Riviello Jr JJ, Bourgeois BF, Blum AS, et al. In-session seizures during low-frequency repetitive transcranial magnetic stimulation in patients with epilepsy. Epilepsy & Behavior. 2009;16(2):353-5. https://doi.org/10.1016/j.yebeh.2009.08.010
48. Sun W, Fu W, Mao W, Wang D, Wang Y. Low-frequency repetitive transcranial magnetic stimulation for the treatment of refractory partial epilepsy. Clinical EEG and neuroscience. 2011;42(1):40-4. https://doi.org/10.1177/155005941104200109
49. Muller PA, Pascual-Leone A, Rotenberg A. Safety and tolerability of repetitive transcranial magnetic stimulation in patients with pathologic positive sensory phenomena: a review of literature. Brain stimulation. 2012;5(3):320-9. e27. https://doi.org/10.1016/j.brs.2011.05.003
50. Fuggetta G, Noh NA. A neurophysiological insight into the potential link between transcranial magnetic stimulation, thalamocortical dysrhythmia and neuropsychiatric disorders. Experimental neurology. 2013;245:87-95. https://doi.org/10.1016/j.expneurol.2012.10.010
51. Lage C, Wiles K, Shergill SS, Tracy DK. A systematic review of the effects of low-frequency repetitive transcranial magnetic stimulation on cognition. Journal of Neural Transmission. 2016;123(12):1479-90. https://doi.org/10.1007/s00702-016-1592-8
52. Allen CH, Kluger BM, Buard I. Safety of transcranial magnetic stimulation in children: a systematic review of the literature. Pediatric neurology. 2017;68:3-17. https://doi.org/10.1016/j.pediatrneurol.2016.12.009
53. Boon P, De Cock E, Mertens A, Trinka E. Neurostimulation for drug-resistant epilepsy: a systematic review of clinical evidence for efficacy, safety, contraindications and predictors for response. Current opinion in neurology. 2018;31(2):198-210. https://doi.org/10.1097/WCO.0000000000000534
54. Bender Pape T, Kletzel SL, Aaronson AL, Guernon A, Carbone C, Chaudhry N, et al. Safety considerations for the use of transcranial magnetic stimulation as treatment for coma recovery in people with severe traumatic brain injury. Journal of Head Trauma Rehabilitation. 2020;35(6):430-8. https://doi.org/10.1097/HTR.0000000000000636
55. Baumer FM, Pfeifer K, Fogarty A, Pena-Solorzano D, Rolle CE, Wallace JL, et al. Cortical excitability, synaptic plasticity, and cognition in benign epilepsy with centrotemporal spikes: A pilot TMS-EMG-EEG study. Journal of Clinical Neurophysiology. 2020;37(2):170-80. https://doi.org/10.1097/WNP.0000000000000662
56. Kucuker MU, Almorsy AG, Sonmez AI, Ligezka AN, Doruk Camsari D, Lewis CP, et al. A systematic review of neuromodulation treatment effects on suicidality. Frontiers in human neuroscience. 2021. https://doi.org/10.3389/fnhum.2021.660926
57. Chen Y, Magnin C, Brunelin J, Leaune E, Fang Y, Poulet E. Can seizure therapies and noninvasive brain stimulations prevent suicidality? A systematic review. Brain and behavior. 2021;11(5):e02144. https://doi.org/10.1002/brb3.2144
58. Walton D, Spencer DC, Nevitt SJ, Michael BD. Transcranial magnetic stimulation for the treatment of epilepsy. Cochrane Database of Systematic Reviews. 2021(4). https://doi.org/10.1002/14651858.CD011025.pub3
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