DOI QR코드

DOI QR Code

Repetitive transcranial magnetic stimulation in central post-stroke pain: current status and future perspective

  • Riva Satya Radiansyah (Faculty of Medicine and Health, Institut Teknologi Sepuluh Nopember) ;
  • Deby Wahyuning Hadi (Department of Neurology, Faculty of Medicine, Universitas Airlangga – Dr. Soetomo General Academic Hospital)
  • Received : 2023.07.25
  • Accepted : 2023.09.14
  • Published : 2023.10.01

Abstract

Central post-stroke pain (CPSP) is an incapacitating disorder that impacts a substantial proportion of stroke survivors and can diminish their quality of life. Conventional therapies for CPSP, including tricyclic antidepressants, anticonvulsants, and opioids, are frequently ineffective, necessitating the investigation of alternative therapeutic strategies. Repetitive transcranial magnetic stimulation (rTMS) is now recognized as a promising noninvasive pain management method for CPSP. rTMS modulates neural activity through the administration of magnetic pulses to specific cortical regions. Trials analyzing the effects of rTMS on CPSP have generated various outcomes, but the evidence suggests possible analgesic benefits. In CPSP and other neuropathic pain conditions, high-frequency rTMS targeting the primary motor cortex (M1) with figure-eight coils has demonstrated significant pain alleviation. Due to its associaton with analgesic benefits, M1 is the most frequently targeted area. The duration and frequency of rTMS sessions, as well as the stimulation intensity, have been studied in an effort to optimize treatment outcomes. The short-term pain relief effects of rTMS have been observed, but the long-term effects (> 3 months) require further investigation. Aspects such as stimulation frequency, location, and treatment period can influence the efficacy of rTMS and ought to be considered while planning the procedure. Standardized guidelines for using rTMS in CPSP would optimize therapy protocols and improve patient outcomes. This review article provides an up-to-date overview of the incidence, clinical characteristics, outcome of rTMS in CPSP patients, and future perspective in the field.

Keywords

Acknowledgement

The authors gratefully acknowledge financial support from the Institut Teknologi Sepuluh Nopember for this work, under project scheme of the Publication Writing and IPR Incentive Program (PPHKI) 2023.

References

  1. Jonsson AC, Lindgren I, Hallstrom B, Norrving B, Lindgren A. Prevalence and intensity of pain after stroke: a population based study focusing on patients' perspectives. J Neurol Neurosurg Psychiatry 2006; 77: 590-5.  https://doi.org/10.1136/jnnp.2005.079145
  2. Kong KH, Woon VC, Yang SY. Prevalence of chronic pain and its impact on health-related quality of life in stroke survivors. Arch Phys Med Rehabil 2004; 85: 35-40.  https://doi.org/10.1016/S0003-9993(03)00369-1
  3. Naess H, Lunde L, Brogger J. The effects of fatigue, pain, and depression on quality of life in ischemic stroke patients: the Bergen Stroke Study. Vasc Health Risk Manag 2012; 8: 407-13.  https://doi.org/10.2147/VHRM.S32780
  4. Oh H, Seo W. A comprehensive review of central post-stroke pain. Pain Manag Nurs 2015; 16: 804-18.  https://doi.org/10.1016/j.pmn.2015.03.002
  5. MacGowan DJ, Janal MN, Clark WC, Wharton RN, Lazar RM, Sacco RL, et al. Central poststroke pain and Wallenberg's lateral medullary infarction: frequency, character, and determinants in 63 patients. Neurology 1997; 49: 120-5.  https://doi.org/10.1212/WNL.49.1.120
  6. Klit H, Finnerup NB, Jensen TS. Central post-stroke pain: clinical characteristics, pathophysiology, and management. Lancet Neurol 2009; 8: 857-68.  https://doi.org/10.1016/S1474-4422(09)70176-0
  7. Lampl C, Yazdi K, Roper C. Amitriptyline in the prophylaxis of central poststroke pain. Preliminary results of 39 patients in a placebo-controlled, long-term study. Stroke 2002; 33: 3030-2.  https://doi.org/10.1161/01.STR.0000037674.95228.86
  8. Head H, Holmes G. Sensory disturbances from cerebral lesions. Brain 1911; 34: 102-254.  https://doi.org/10.1093/brain/34.2-3.102
  9. Riddoch G. The clinical features of central pain. Lancet 1938; 231: 1205-9.  https://doi.org/10.1016/S0140-6736(00)89785-8
  10. Loeser JD, Treede RD. The Kyoto protocol of IASP Basic Pain Terminology. Pain 2008; 137: 473-77.  https://doi.org/10.1016/j.pain.2008.04.025
  11. Seifert CL, Mallar Chakravarty M, Sprenger T. The complexities of pain after stroke--a review with a focus on central post-stroke pain. Panminerva Med 2013; 55: 1-10. 
  12. Andersen G, Vestergaard K, Ingeman-Nielsen M, Jensen TS. Incidence of central post-stroke pain. Pain 1995; 61: 187-93.  https://doi.org/10.1016/0304-3959(94)00144-4
  13. Finnerup NB, Otto M, McQuay HJ, Jensen TS, Sindrup SH. Algorithm for neuropathic pain treatment: an evidence based proposal. Pain 2005; 118: 289-305.  https://doi.org/10.1016/j.pain.2005.08.013
  14. Westlund KN. Pain pathways: peripheral, spinal, ascending, and descending pathways. In: Practical management of pain. 5th ed. Edited by Benzon HT, Rathmell JP, Wu CL, Turk DC, Argoff CE, Hurley RW. Elsevier. 2014, pp 87-98.e5. 
  15. Sewards TV, Sewards MA. The medial pain system: neural representations of the motivational aspect of pain. Brain Res Bull 2002; 59: 163-80.  https://doi.org/10.1016/S0361-9230(02)00864-X
  16. Betancur DFA, Tarrago MDGL, Torres ILDS, Fregni F, Caumo W. Central post-stroke pain: an integrative review of somatotopic damage, clinical symptoms, and neurophysiological measures. Front Neurol 2021; 12: 678198. 
  17. Gerges ANH, Hordacre B, Pietro FD, Moseley GL, Berryman C. Do adults with stroke have altered interhemispheric inhibition? A systematic review with meta-analysis. J Stroke Cerebrovasc Dis 2022; 31: 106494. 
  18. Craig AD. A new version of the thalamic disinhibition hypothesis of central pain. Pain Forum 1998; 7: 1-14.  https://doi.org/10.1016/S1082-3174(98)70004-2
  19. Boivie J, Leijon G, Johansson I. Central post-stroke pain--a study of the mechanisms through analyses of the sensory abnormalities. Pain 1989; 37: 173-85.  https://doi.org/10.1016/0304-3959(89)90128-0
  20. Vartiainen N, Perchet C, Magnin M, Creac'h C, Convers P, Nighoghossian N, et al. Thalamic pain: anatomical and physiological indices of prediction. Brain 2016; 139: 708-22.  https://doi.org/10.1093/brain/awv389
  21. Baliki MN, Schnitzer TJ, Bauer WR, Apkarian AV. Brain morphological signatures for chronic pain. PLoS One 2011; 6: e26010. 
  22. Krause T, Asseyer S, Taskin B, Floel A, Witte AV, Mueller K, et al. The cortical signature of central poststroke pain: gray matter decreases in somatosensory, insular, and prefrontal cortices. Cereb Cortex 2016; 26: 80-8.  https://doi.org/10.1093/cercor/bhu177
  23. Li X, Feng Y, Gao F. Maladaptive reorganization in pain-related brain network contributing to the central post-stroke pain. Neuropsychiatry (London) 2019; 9: 2186-97. 
  24. Gritsch S, Bali KK, Kuner R, Vardeh D. Functional characterization of a mouse model for central poststroke pain. Mol Pain 2016; 12: 1744806916629049. 
  25. Kim JS. Pure sensory stroke. Clinical-radiological correlates of 21 cases. Stroke 1992; 23: 983-7.  https://doi.org/10.1161/01.STR.23.7.983
  26. Kim JH, Greenspan JD, Coghill RC, Ohara S, Lenz FA. Lesions limited to the human thalamic principal somatosensory nucleus (ventral caudal) are associated with loss of cold sensations and central pain. J Neurosci 2007; 27: 4995-5004.  https://doi.org/10.1523/JNEUROSCI.0716-07.2007
  27. Wang G, Thompson SM. Maladaptive homeostatic plasticity in a rodent model of central pain syndrome: thalamic hyperexcitability after spinothalamic tract lesions. J Neurosci 2008; 28: 11959-69.  https://doi.org/10.1523/JNEUROSCI.3296-08.2008
  28. Lenz FA, Weiss N, Ohara S, Lawson C, Greenspan JD. The role of the thalamus in pain. In: Supplements to clinical neurophysiology. Edited by Hallett M, Phillips LH, Schomer DL, Massey JM. Elsevier. 2004, pp 50-61. 
  29. Kadono Y, Koguchi K, Okada KI, Hosomi K, Hiraishi M, Ueguchi T, et al. Repetitive transcranial magnetic stimulation restores altered functional connectivity of central poststroke pain model monkeys. Sci Rep 2021; 11: 6126. 
  30. Kuan YH, Shih HC, Shyu BC. Involvement of P2X7 receptors and BDNF in the pathogenesis of central poststroke pain. Adv Exp Med Biol 2018; 1099: 211-27.  https://doi.org/10.1007/978-981-13-1756-9_18
  31. Schwartzman RJ, Grothusen J, Kiefer TR, Rohr P. Neuropathic central pain: epidemiology, etiology, and treatment options. Arch Neurol 2001; 58: 1547-50.  https://doi.org/10.1001/archneur.58.10.1547
  32. Latremoliere A, Woolf CJ. Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J Pain 2009; 10: 895-926.  https://doi.org/10.1016/j.jpain.2009.06.012
  33. Campbell JN, Meyer RA. Mechanisms of neuropathic pain. Neuron 2006; 52: 77-92.  https://doi.org/10.1016/j.neuron.2006.09.021
  34. Kohno T, Ji RR, Ito N, Allchorne AJ, Befort K, Karchewski LA, et al. Peripheral axonal injury results in reduced mu opioid receptor pre- and postsynaptic action in the spinal cord. Pain 2005; 117: 77-87.  https://doi.org/10.1016/j.pain.2005.05.035
  35. Li CY, Song YH, Higuera ES, Luo ZD. Spinal dorsal horn calcium channel alpha2delta-1 subunit upregulation contributes to peripheral nerve injury-induced tactile allodynia. J Neurosci 2004; 24: 8494-9.  https://doi.org/10.1523/JNEUROSCI.2982-04.2004
  36. Yoshimura M, Yonehara N. Alteration in sensitivity of ionotropic glutamate receptors and tachykinin receptors in spinal cord contribute to development and maintenance of nerve injury-evoked neuropathic pain. Neurosci Res 2006; 56: 21-8.  https://doi.org/10.1016/j.neures.2006.04.015
  37. Marchand F, Perretti M, McMahon SB. Role of the immune system in chronic pain. Nat Rev Neurosci 2005; 6: 521-32.  https://doi.org/10.1038/nrn1700
  38. Attal N, Fermanian C, Fermanian J, Lanteri-Minet M, Alchaar H, Bouhassira D. Neuropathic pain: are there distinct subtypes depending on the aetiology or anatomical lesion? Pain 2008; 138: 343-53.  https://doi.org/10.1016/j.pain.2008.01.006
  39. Hansen AP, Marcussen NS, Klit H, Andersen G, Finnerup NB, Jensen TS. Pain following stroke: a prospective study. Eur J Pain 2012; 16: 1128-36.  https://doi.org/10.1002/j.1532-2149.2012.00123.x
  40. Scholz J, Finnerup NB, Attal N, Aziz Q, Baron R, Bennett MI, et al.; Classification Committee of the Neuropathic Pain Special Interest Group (NeuPSIG). The IASP classification of chronic pain for ICD-11: chronic neuropathic pain. Pain 2019; 160: 53-9.  https://doi.org/10.1097/j.pain.0000000000001365
  41. Kim MS, Kim BY, Saghetlians A, Zhang X, Okida T, Kim SY. Anti-nociceptive effects of dual neuropeptide antagonist therapy in mouse model of neuropathic and inflammatory pain. Korean J Pain 2022; 35: 173-82.  https://doi.org/10.3344/kjp.2022.35.2.173
  42. Obata H. Analgesic mechanisms of antidepressants for neuropathic pain. Int J Mol Sci 2017; 18: 2483. 
  43. Dworkin RH, O'Connor AB, Backonja M, Farrar JT, Finnerup NB, Jensen TS, et al. Pharmacologic management of neuropathic pain: evidence-based recommendations. Pain 2007; 132: 237-51.  https://doi.org/10.1016/j.pain.2007.08.033
  44. Offord J, Isom LL. Drugging the undruggable: gabapentin, pregabalin and the calcium channel α2δ subunit. Crit Rev Biochem Mol Biol 2015; 51: 246-56.  https://doi.org/10.3109/10409238.2016.1173010
  45. Vranken JH, Dijkgraaf MG, Kruis MR, van der Vegt MH, Hollmann MW, Heesen M. Pregabalin in patients with central neuropathic pain: a randomized, double-blind, placebo-controlled trial of a flexible-dose regimen. Pain 2008; 136: 150-7.  https://doi.org/10.1016/j.pain.2007.06.033
  46. Stefani A, Spadoni F, Siniscalchi A, Bernardi G. Lamotrigine inhibits Ca2+ currents in cortical neurons: functional implications. Eur J Pharmacol 1996; 307: 113-6.  https://doi.org/10.1016/0014-2999(96)00265-8
  47. Sansone RA, Sansone LA. Serotonin norepinephrine reuptake inhibitors: a pharmacological comparison. Innov Clin Neurosci 2014; 11: 37-42. 
  48. Jo S, Bean BP. Sidedness of carbamazepine accessibility to voltage-gated sodium channels. Mol Pharmacol 2014; 85: 381-7.  https://doi.org/10.1124/mol.113.090472
  49. Edinoff AN, Kaplan LA, Khan S, Petersen M, Sauce E, Causey CD, et al. Full opioid agonists and tramadol: pharmacological and clinical considerations. Anesth Pain Med 2021; 11: e119156. 
  50. Holbech JV, Jung A, Jonsson T, Wanning M, Bredahl C, Bach FW. Combination treatment of neuropathic pain: Danish expert recommendations based on a Delphi process. J Pain Res 2017; 10: 1467-75.  https://doi.org/10.2147/JPR.S138099
  51. Kim JS. Pharmacological management of central post-stroke pain: a practical guide. CNS Drugs 2014; 28: 787-97.  https://doi.org/10.1007/s40263-014-0194-y
  52. Banerjee M, Pal S, Bhattacharya B, Ghosh B, Mondal S, Basu J. A comparative study of efficacy and safety of gabapentin versus amitriptyline as coanalgesics in patients receiving opioid analgesics for neuropathic pain in malignancy. Indian J Pharmacol 2013; 45: 334-8.  https://doi.org/10.4103/0253-7613.115000
  53. Winstein CJ, Stein J, Arena R, Bates B, Cherney LR, Cramer SC, et al.; American Heart Association Stroke Council, Council on Cardiovascular and Stroke Nursing, Council on Clinical Cardiology, and Council on Quality of Care and Outcomes Research. Guidelines for adult stroke rehabilitation and recovery: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2016; 47: e98-169. Erratum in: Stroke 2017; 48: e78. Erratum in: Stroke 2017; 48: e369. 
  54. Intercollegiate Stroke Working Party. National clinical guideline for stroke. 5th ed. Royal College of Physicians. 2016, pp 1-178. 
  55. Teasell R, Salbach NM, Foley N, Mountain A, Cameron JI, Jong A, et al. Canadian stroke best practice recommendations: rehabilitation, recovery, and community participation following stroke. Part one: rehabilitation and recovery following stroke; 6th edition update 2019. Int J Stroke 2020; 15: 763-88.  https://doi.org/10.1177/1747493019897843
  56. Iglesias AH. Transcranial magnetic stimulation as treatment in multiple neurologic conditions. Curr Neurol Neurosci Rep 2020; 20: 1. 
  57. Vidal-Dourado M, Conforto AB, Caboclo LO, Scaff M, Guilhoto LM, Yacubian EM. Magnetic fields in noninvasive brain stimulation. Neuroscientist 2014; 20: 112-21.  https://doi.org/10.1177/1073858413491145
  58. Diana M, Raij T, Melis M, Nummenmaa A, Leggio L, Bonci A. Rehabilitating the addicted brain with transcranial magnetic stimulation. Nat Rev Neurosci 2017; 18: 685-93.  https://doi.org/10.1038/nrn.2017.113
  59. Barker AT, Jalinous R, Freeston IL. Non-invasive magnetic stimulation of human motor cortex. Lancet 1985; 1: 1106-7.  https://doi.org/10.1016/S0140-6736(85)92413-4
  60. Marcos Z. Alvaro Pascual-Leone: a pioneer of noninvasive brain stimulation. Lancet Neurol 2013; 12: 853. 
  61. Burke MJ, Fried PJ, Pascual-Leone A. Transcranial magnetic stimulation: Neurophysiological and clinical applications. Handb Clin Neurol 2019; 163: 73-92.  https://doi.org/10.1016/B978-0-12-804281-6.00005-7
  62. Hallett M. Transcranial magnetic stimulation and the human brain. Nature 2000; 406: 147-50.  https://doi.org/10.1038/35018000
  63. Di Lazzaro V, Profice P, Ranieri F, Capone F, Dileone M, Oliviero A, et al. I-wave origin and modulation. Brain Stimul 2012; 5: 512-25.  https://doi.org/10.1016/j.brs.2011.07.008
  64. Leung A, Donohue M, Xu R, Lee R, Lefaucheur JP, Khedr EM, et al. rTMS for suppressing neuropathic pain: a meta-analysis. J Pain 2009; 10: 1205-16.  https://doi.org/10.1016/j.jpain.2009.03.010
  65. Jin Y, Xing G, Li G, Wang A, Feng S, Tang Q, et al. High frequency repetitive transcranial magnetic stimulation therapy for chronic neuropathic pain: a meta-analysis. Pain Physician 2015; 18: E1029-46.  https://doi.org/10.36076/ppj.2015/18/E1029
  66. Pecuch PW, Evers S, Folkerts HW, Michael N, Arolt V. The cerebral hemodynamics of repetitive transcranial magnetic stimulation. Eur Arch Psychiatry Clin Neurosci 2000; 250: 320-4.  https://doi.org/10.1007/s004060070007
  67. Vernieri F, Maggio P, Tibuzzi F, Filippi MM, Pasqualetti P, Melgari JM, et al. High frequency repetitive transcranial magnetic stimulation decreases cerebral vasomotor reactivity. Clin Neurophysiol 2009; 120: 1188-94.  https://doi.org/10.1016/j.clinph.2009.03.021
  68. Ohn SH, Chang WH, Park CH, Kim ST, Lee JI, Pascual-Leone A, et al. Neural correlates of the antinociceptive effects of repetitive transcranial magnetic stimulation on central pain after stroke. Neurorehabil Neural Repair 2012; 26: 344-52.  https://doi.org/10.1177/1545968311423110
  69. Goto T, Saitoh Y, Hashimoto N, Hirata M, Kishima H, Oshino S, et al. Diffusion tensor fiber tracking in patients with central post-stroke pain; correlation with efficacy of repetitive transcranial magnetic stimulation. Pain 2008; 140: 509-18.  https://doi.org/10.1016/j.pain.2008.10.009
  70. Ahmed MA, Mohamed SA, Sayed D. Long-term antalgic effects of repetitive transcranial magnetic stimulation of motor cortex and serum beta-endorphin in patients with phantom pain. Neurol Res 2011; 33: 953-8.  https://doi.org/10.1179/1743132811Y.0000000045
  71. Pan LJ, Zhu HQ, Zhang XA, Wang XQ. The mechanism and effect of repetitive transcranial magnetic stimulation for post-stroke pain. Front Mol Neurosci 2023; 15: 1091402. 
  72. Lin RL, Douaud G, Filippini N, Okell TW, Stagg CJ, Tracey I. Structural connectivity variances underlie functional and behavioral changes during pain relief induced by neuromodulation. Sci Rep 2017; 7: 41603. 
  73. Mitchell AS, Chakraborty S. What does the mediodorsal thalamus do? Front Syst Neurosci 2013; 7: 37. 
  74. Zhao CG, Sun W, Ju F, Jiang S, Wang H, Sun XL, et al. Analgesic effects of navigated repetitive transcranial magnetic stimulation in patients with acute central poststroke pain. Pain Ther 2021; 10: 1085-100. Erratum in: Pain Ther 2021; 10: 1101-3.  https://doi.org/10.1007/s40122-021-00270-z
  75. Garcia-Larrea L, Peyron R. Motor cortex stimulation for neuropathic pain: from phenomenology to mechanisms. Neuroimage 2007; 37 Suppl 1: S71-9.  https://doi.org/10.1016/j.neuroimage.2007.05.062
  76. Attal N, Ayache SS, Ciampi De Andrade D, Mhalla A, Baudic S, Jazat F, et al. Repetitive transcranial magnetic stimulation and transcranial direct-current stimulation in neuropathic pain due to radiculopathy: a randomized sham-controlled comparative study. Pain 2016; 157: 1224-31.  https://doi.org/10.1097/j.pain.0000000000000510
  77. Lindholm P, Lamusuo S, Taiminen T, Pesonen U, Lahti A, Virtanen A, et al. Right secondary somatosensory cortex-a promising novel target for the treatment of drug-resistant neuropathic orofacial pain with repetitive transcranial magnetic stimulation. Pain 2015; 156: 1276-83.  https://doi.org/10.1097/j.pain.0000000000000175
  78. Lefaucheur JP. The use of repetitive transcranial magnetic stimulation (rTMS) in chronic neuropathic pain. Neurophysiol Clin 2006; 36: 117-24.  https://doi.org/10.1016/j.neucli.2006.08.002
  79. Kisler LB, Weissman-Fogel I, Sinai A, Sprecher E, Chistyakov AV, Shamay-Tsoory S, et al. Bi-phasic activation of the primary motor cortex by pain and its relation to pain-evoked potentials - an exploratory study. Behav Brain Res 2017; 328: 209-17.  https://doi.org/10.1016/j.bbr.2017.04.006
  80. Cha M, Ji Y, Masri R. Motor cortex stimulation activates the incertothalamic pathway in an animal model of spinal cord injury. J Pain 2013; 14: 260-9.  https://doi.org/10.1016/j.jpain.2012.11.007
  81. Yang L, Liu X, Yao K, Sun Y, Jiang F, Yan H, et al. HCN channel antagonist ZD7288 ameliorates neuropathic pain and associated depression. Brain Res 2019; 1717: 204-13.  https://doi.org/10.1016/j.brainres.2019.03.036
  82. Lanza G, Arico D, Lanuzza B, Cosentino FII, Tripodi M, Giardina F, et al. Facilitatory/inhibitory intracortical imbalance in REM sleep behavior disorder: early electrophysiological marker of neurodegeneration? Sleep 2020; 43: zsz242. 
  83. Hosomi K, Kishima H, Oshino S, Hirata M, Tani N, Maruo T, et al. Cortical excitability changes after high-frequency repetitive transcranial magnetic stimulation for central poststroke pain. Pain 2013; 154: 1352-7.  https://doi.org/10.1016/j.pain.2013.04.017
  84. Hoogendam JM, Ramakers GM, Di Lazzaro V. Physiology of repetitive transcranial magnetic stimulation of the human brain. Brain Stimul 2010; 3: 95-118.  https://doi.org/10.1016/j.brs.2009.10.005
  85. Cooke SF, Bliss TV. Plasticity in the human central nervous system. Brain 2006; 129: 1659-73.  https://doi.org/10.1093/brain/awl082
  86. Obata K, Yamanaka H, Dai Y, Tachibana T, Fukuoka T, Tokunaga A, et al. Differential activation of extracellular signal-regulated protein kinase in primary afferent neurons regulates brain-derived neurotrophic factor expression after peripheral inflammation and nerve injury. J Neurosci 2003; 23: 4117-26.  https://doi.org/10.1523/JNEUROSCI.23-10-04117.2003
  87. Ikeda K, Hazama K, Itano Y, Ouchida M, Nakatsuka H. Development of a novel analgesic for neuropathic pain targeting brain-derived neurotrophic factor. Biochem Biophys Res Commun 2020; 531: 390-5.  https://doi.org/10.1016/j.bbrc.2020.07.109
  88. Siuciak JA, Altar CA, Wiegand SJ, Lindsay RM. Antinociceptive effect of brain-derived neurotrophic factor and neurotrophin-3. Brain Res 1994; 633: 326-30.  https://doi.org/10.1016/0006-8993(94)91556-3
  89. Chail A, Saini RK, Bhat PS, Srivastava K, Chauhan V. Transcranial magnetic stimulation: a review of its evolution and current applications. Ind Psychiatry J 2018; 27: 172-80.  https://doi.org/10.4103/ipj.ipj_88_18
  90. Treister R, Lang M, Klein MM, Oaklander AL. Noninvasive transcranial magnetic stimulation (TMS) of the motor cortex for neuropathic pain-at the tipping point? Rambam Maimonides Med J 2013; 4: e0023. 
  91. Lin H, Li W, Ni J, Wang Y. Clinical study of repetitive transcranial magnetic stimulation of the motor cortex for thalamic pain. Medicine (Baltimore) 2018; 97: e11235. 
  92. Najib U, Bashir S, Edwards D, Rotenberg A, Pascual-Leone A. Transcranial brain stimulation: clinical applications and future directions. Neurosurg Clin N Am 2011; 22: 233-51, ix.  https://doi.org/10.1016/j.nec.2011.01.002
  93. Machado S, Arias-Carrion O, Paes F, Vieira RT, Caixeta L, Novaes F, et al. Repetitive transcranial magnetic stimulation for clinical applications in neurological and psychiatric disorders: an overview. Eurasian J Med 2013; 45: 191-206.  https://doi.org/10.5152/eajm.2013.39
  94. Kobayashi M, Fujimaki T, Mihara B, Ohira T. Repetitive transcranial magnetic stimulation once a week induces sustainable long-term relief of central poststroke pain. Neuromodulation 2015; 18: 249-54.  https://doi.org/10.1111/ner.12301
  95. Khedr EM, Kotb H, Kamel NF, Ahmed MA, Sadek R, Rothwell JC. Longlasting antalgic effects of daily sessions of repetitive transcranial magnetic stimulation in central and peripheral neuropathic pain. J Neurol Neurosurg Psychiatry 2005; 76: 833-8.  https://doi.org/10.1136/jnnp.2004.055806
  96. Alhassani G, Liston MB, Schabrun SM. Interhemispheric inhibition is reduced in response to acute muscle pain: a cross-sectional study using transcranial magnetic stimulation. J Pain 2019; 20: 1091-9.  https://doi.org/10.1016/j.jpain.2019.03.007
  97. Migita K, Uozumi T, Arita K, Monden S. Transcranial magnetic coil stimulation of motor cortex in patients with central pain. Neurosurgery 1995; 36: 1037-9.  https://doi.org/10.1227/00006123-199505000-00025
  98. Saitoh Y, Hirayama A, Kishima H, Shimokawa T, Oshino S, Hirata M, et al. Reduction of intractable deafferentation pain due to spinal cord or peripheral lesion by high-frequency repetitive transcranial magnetic stimulation of the primary motor cortex. J Neurosurg 2007; 107: 555-9.  https://doi.org/10.3171/JNS-07/09/0555
  99. Matsumura Y, Hirayama T, Yamamoto T. Comparison between pharmacologic evaluation and repetitive transcranial magnetic stimulation-induced analgesia in poststroke pain patients. Neuromodulation 2013; 16: 349-54.  https://doi.org/10.1111/ner.12019
  100. Ojala J, Vanhanen J, Harno H, Lioumis P, Vaalto S, Kaunisto MA, et al. A randomized, sham-controlled trial of repetitive transcranial magnetic stimulation targeting M1 and S2 in central poststroke pain: a pilot trial. Neuromodulation 2022; 25: 538-48.  https://doi.org/10.1111/ner.13496
  101. Hasan M, Whiteley J, Bresnahan R, MacIver K, Sacco P, Das K, et al. Somatosensory change and pain relief induced by repetitive transcranial magnetic stimulation in patients with central poststroke pain. Neuromodulation 2014; 17: 731-6.  https://doi.org/10.1111/ner.12198
  102. de Oliveira RA, de Andrade DC, Mendonca M, Barros R, Luvisoto T, Myczkowski ML, et al. Repetitive transcranial magnetic stimulation of the left premotor/dorsolateral prefrontal cortex does not have analgesic effect on central poststroke pain. J Pain 2014; 15: 1271-81.  https://doi.org/10.1016/j.jpain.2014.09.009
  103. Malfitano C, Rossetti A, Scarano S, Malloggi C, Tesio L. Efficacy of repetitive transcranial magnetic stimulation for acute central post-stroke pain: a case study. Front Neurol 2021; 12: 742567. 
  104. Yang S, Chang MC. Effect of repetitive transcranial magnetic stimulation on pain management: a systematic narrative review. Front Neurol 2020; 11: 114. 
  105. Lefaucheur JP, Drouot X, Nguyen JP. Interventional neurophysiology for pain control: duration of pain relief following repetitive transcranial magnetic stimulation of the motor cortex. Neurophysiol Clin 2001; 31: 247-52.  https://doi.org/10.1016/S0987-7053(01)00260-X
  106. Cruccu G, Aziz TZ, Garcia-Larrea L, Hansson P, Jensen TS, Lefaucheur JP, et al. EFNS guidelines on neurostimulation therapy for neuropathic pain. Eur J Neurol 2007; 14: 952-70.  https://doi.org/10.1111/j.1468-1331.2007.01916.x
  107. Machii K, Cohen D, Ramos-Estebanez C, Pascual-Leone A. Safety of rTMS to non-motor cortical areas in healthy participants and patients. Clin Neurophysiol 2006; 117: 455-71.  https://doi.org/10.1016/j.clinph.2005.10.014
  108. Klomjai W, Katz R, Lackmy-Vallee A. Basic principles of transcranial magnetic stimulation (TMS) and repetitive TMS (rTMS). Ann Phys Rehabil Med 2015; 58: 208-13.  https://doi.org/10.1016/j.rehab.2015.05.005
  109. Rossini PM, Burke D, Chen R, Cohen LG, Daskalakis Z, Di Iorio R, et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee. Clin Neurophysiol 2015; 126: 1071-107.  https://doi.org/10.1016/j.clinph.2015.02.001
  110. Wassermann EM. 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 1998; 108: 1-16.  https://doi.org/10.1016/S0168-5597(97)00096-8
  111. Bae EH, Schrader LM, Machii K, Alonso-Alonso M, Riviello JJ Jr, Pascual-Leone A, et al. Safety and tolerability of repetitive transcranial magnetic stimulation in patients with epilepsy: a review of the literature. Epilepsy Behav 2007; 10: 521-8. https://doi.org/10.1016/j.yebeh.2007.03.004