M1区联合背外侧前额叶高频重复经颅磁刺激对脊髓损伤后神经病理性疼痛患者脑电图θ振幅的效果

doi:10.3969/j.issn.1006-9771.2024.01.012

Abstract

Abstract:

Objective To explore the efficacy of high-frequency repetitive transcranial magnetic stimulation (rTMS) in M1 region combined with dorsolateral prefrontal cortex (DLPFC) on electroencephalogram (EEG) θ frequency band amplitude of patients with neuropathic pain (NP) after spinal cord injury.

Methods From June, 2022 to June, 2023, 50 NP patients after SCI in Qingdao University Affiliated Hospital were included and divided into M1 region stimulation group (n = 25) and M1 region combined with DLPFC stimulation group (the combined stimulation group, n = 25). M1 region stimulation group received 10 Hz rTMS in the left M1 region, while the combined stimulation group received same stimulation in left M1 region combined with DLPFC, for three weeks. Before and after intervention, the pain was assessed with Short Form of McGill Pain Questionnaire (SF-MPQ), the depression and anxiety status were evaluated using Hamilton Depression Scale (HAMD) and Hamilton Anxiety Scale (HAMA), and the EEG θ frequency band amplitude was recorded to detect the changes of brain electrophysiological activity.

Results Four cases in M1 region stimulation group, and two cases in the combined stimulation group were dropped. After intervention, the total score of SF-MPQ and the scores of the subscales, the scores of HMMD and HAMA decreased in both groups (|t| > 2.523, P < 0.05). The EEG θ frequency band amplitude significantly reduced in the prefrontal and frontal regions in M1 region stimulation group (|t| > 5.243, P < 0.001), and it also significantly reduced in the prefrontal, frontal regions, central and parietal regions in the combined stimulation group (|t| > 4.630, P < 0.001). All the scores were lower (|t| > 2.270, Z = -1.973, P < 0.05), and the EEG θ frequency band amplitude in the prefrontal, frontal regions, central and parietal regions were lower (P < 0.05) in the combined stimulation group than in M1 region stimulation group.

Conclusion High frequency rTMS is an effective analgesic method on NP after SCI, which can improve their depression and anxiety symptoms and reduce the EEG θ frequency band amplitude. Compared with M1 region rTMS stimulation, the combination of M1 region and DLPFC rTMS is more effective.

Key words: spinal cord injury, neuropathic pain, repetitive transcranial magnetic stimulation, electroencephalogram, θ frequency band amplitude

CLC Number:

R651.2

LIU Dong, XU Zihan, LI Jiang, JU Ping. Effect of high-frequency repetitive transcranial magnetic stimulation in M1 region combined with dorsolateral prefrontal cortex on electroencephalogram θ frequency band amplitude of patients with neuropathic pain after spinal cord injury[J]. 《Chinese Journal of Rehabilitation Theory and Practice》, 2024, 30(1): 87-94.

Figures/Tables 10

Table 1

Table 2

Table 3

Table 4

Table 5

Table 6

Table 7

Table 8

Figure 1

Figure 2

References 36

[1]	NIELSEN S D, FAABORG P M, CHRISTENSEN P, et al. Chronic abdominal pain in long-term spinal cord injury: a follow-up study[J]. Spinal Cord, 2017, 55(3): 290-293. doi: 10.1038/sc.2016.124 pmid: 27502843
[2]	ALMEIDA C, MONTEIRO-SOARES M, FERNANDES Â. Should non-pharmacological and non-surgical interventions be used to manage neuropathic pain in adults with spinal cord injury? A systematic review[J]. Pain, 2022, 23(9): 1510-1529.
[3]	DAVARI M, AMANI B, AMANI B, et al. Pregabalin and gabapentin in neuropathic pain management after spinal cord injury: a systematic review and meta-analysis[J]. Korean J Pain, 2020, 33(1): 3-12. doi: 10.3344/kjp.2020.33.1.3 pmid: 31888312
[4]	ZHAO C G, SUN W, JU F, et al. Analgesic effects of directed repetitive transcranial magnetic stimulation in acute neuropathic pain after spinal cord injury[J]. Pain Med, 2020, 21(6): 1216-1223. doi: 10.1093/pm/pnz290
[5]	ALAMRI A, PEREIRA E A C. Deep brain stimulation for chronic pain[J]. Neurosurg Clin N Am, 2022, 33(3): 311-321. doi: 10.1016/j.nec.2022.02.013 pmid: 35718401
[6]	KLOMJAI W, KATZ R, LACKMY-VALLÉE A. Basic principles of transcranial magnetic stimulation (TMS) and repetitive TMS (rTMS)[J]. Ann Phys Rehabil Med, 2015, 58(4): 208-213. doi: S1877-0657(15)00079-2 pmid: 26319963
[7]	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)[J]. Clin Neurophysiol, 2020, 131(2): 474-528. doi: 10.1016/j.clinph.2019.11.002
[8]	SEMINOWICZ D A, MOAYEDI M. The dorsolateral prefrontal cortex in acute and chronic pain[J]. Pain, 2017, 18(9): 1027-1035.
[9]	VELDEMA J, GHARABAGHI A. Non-invasive brain stimulation for improving gait, balance, and lower limbs motor function in stroke[J]. J Neuroeng Rehabil, 2022, 19(1): 84. doi: 10.1186/s12984-022-01062-y pmid: 35922846
[10]	ZHU Y, LI D, ZHOU Y, et al. Systematic review and meta-analysis of high-frequency rtms over the dorsolateral prefrontal cortex on chronic pain and chronic-pain-accompanied depression[J]. ACS Chem Neurosci, 2022, 13(17): 2547-2556. doi: 10.1021/acschemneuro.2c00395 pmid: 35969469
[11]	CHE X, CASH R F H, LUO X, et al. High-frequency rTMS over the dorsolateral prefrontal cortex on chronic and provoked pain: a systematic review and meta-analysis[J]. Brain Stimul, 2021, 14(5): 1135-1146. doi: 10.1016/j.brs.2021.07.004 pmid: 34280583
[12]	OMEJC N, ROJC B, BATTAGLINI P P, et al. Review of the therapeutic neurofeedback method using electroencephalography: EEG Neurofeedback[J]. Bosn J Basic Med Sci, 2019, 19(3): 213-220.
[13]	MOHAMAD SAFIAI N I, MOHAMAD N A, BASRI H, et al. High-frequency repetitive transcranial magnetic stimulation at dorsolateral prefrontal cortex for migraine prevention: a systematic review and meta-analysis[J]. Cephalalgia, 2022, 42(10): 1071-1085. doi: 10.1177/03331024221092423
[14]	FENG Y, ZHANG B, ZHANG J, et al. Effects of non-invasive brain stimulation on headache intensity and frequency of headache attacks in patients with migraine: a systematic review and meta-analysis[J]. Headache, 2019, 59(9): 1436-1447. doi: 10.1111/head.13645 pmid: 31535368
[15]	PENG W, TANG D. Pain related cortical oscillations: methodological advances and potential applications[J]. Front Comput Neurosci, 2016, 4(10): 9.
[16]	李艳敏. 左侧背外侧前额叶高频重复经颅磁刺激对健康青年人认知功能的影响及其神经电生理、脑代谢机制[D]. 石家庄: 河北医科大学, 2017.
	LI Y M. The effect of high-frequency repetitive transcranial magnetic stimulation of the left dorsolateral prefrontal lobe on cognitive function and its neuroelectrophysiological and brain metabolic mechanisms in healthy young people[D]. Shijiazhuang: Hebei Medical University, 2017.
[17]	刘思诗. 经颅磁刺激抑制左侧背外侧前额叶对执行功能的影响及其神经机制:一项ERP研究[D]. 广州: 南方医科大学, 2021.
	LIU S S. The effect of transcranial magnetic stimulation on the left dorsolateral prefrontal lobe and its neural mechanism on executive function: an ERP study[D]. Guangzhou: Southern Medical University, 2021
[18]	OCAY D D, TEEL E F, LUO O D, et al. Electroencephalographic characteristics of children and adolescents with chronic musculoskeletal pain[J]. Pain Rep, 2022, 7(6): e1054. doi: 10.1097/PR9.0000000000001054 pmid: 36601627
[19]	顾晗滢. 帕金森病合并慢性骨骼肌疼痛患者的定量脑电图分析[D]. 苏州: 苏州大学, 2020.
	GU H Y. Quantitative electroencephalographic analysis of Parkinson's disease patients with chronic skeletal muscle pain[D]. Suzhou: Soochow University, 2020
[20]	DUAN R, QU M, YUAN Y, et al. Clinical benefit of rehabilitation training in spinal cord injury: a systematic review and meta-analysis[J]. Spine (Phila Pa 1976), 2021, 46(6): E398-E410. doi: 10.1097/BRS.0000000000003789
[21]	MARTÍ-SALVADOR M, HIDALGO-MORENO L, DOMÉNECH-FERNÁNDEZ J, et al. Osteopathic manipulative treatment including specific diaphragm techniques improves pain and disability in chronic nonspecific low back pain: a randomized trial[J]. Arch Phys Med Rehabil, 2018, 99(9): 1720-1729. doi: 10.1016/j.apmr.2018.04.022
[22]	WIDERSTRÖM-NOGA E. Neuropathic pain and spinal cord injury: management, phenotypes, and biomarkers[J]. Drugs, 2023, 83(11): 1001-1025. doi: 10.1007/s40265-023-01903-7
[23]	GURBA K N, CHAUDHRY R, HAROUTOUNIAN S. Central neuropathic pain syndromes: current and emerging pharmacological strategies[J]. CNS Drugs, 2022, 36(5): 483-516. doi: 10.1007/s40263-022-00914-4 pmid: 35513603
[24]	CHEN J, LI L, CHEN S R, et al. The α2δ-1-NMDA receptor complex is critically involved in neuropathic pain development and gabapentin therapeutic actions[J]. Cell Rep, 2018, 22(9): 2307-2321. doi: S2211-1247(18)30189-X pmid: 29490268
[25]	O'CONNELL N E, MARSTON L, SPENCER S, et al. Non-invasive brain stimulation techniques for chronic pain[J]. Cochrane Database Syst Rev, 2018, 4(4): CD008208.
[26]	LI J, WEI Y, ZHOU J, et al. Activation of locus coeruleus-spinal cord noradrenergic neurons alleviates neuropathic pain in mice via reducing neuroinflammation from astrocytes and microglia in spinal dorsal horn[J]. Neuroinflammation, 2022, 19(1): 123. doi: 10.1186/s12974-022-02489-9
[27]	HASAN M, WHITELEY J, BRESNAHAN R, et al. Somatosensory change and pain relief induced by repetitive transcranial magnetic stimulation in patients with central poststroke pain[J]. Neuromodulation, 2014, 17(8): 731-736. doi: 10.1111/ner.12198 pmid: 24934719
[28]	MOISSET X, DE ANDRADE D C, BOUHASSIRA D. From pulses to pain relief: an update on the mechanisms of rTMS-induced analgesic effects[J]. Eur J Pain, 2016, 20(5): 689-700. doi: 10.1002/ejp.811 pmid: 26471248
[29]	GAN Z, GANGADHARAN V, LIU S, et al. Layer-specific pain relief pathways originating from primary motor cortex[J]. Science, 2022, 378(6626): 1336-1343. doi: 10.1126/science.add4391 pmid: 36548429
[30]	KINNEY K R, HANLON C A. Changing cerebral blood flow, glucose metabolism, and dopamine binding through transcranial magnetic stimulation: a systematic review of transcranial magnetic stimulation-positron emission tomography literature[J]. Pharmacol Rev, 2022, 74(4): 918-932. doi: 10.1124/pharmrev.122.000579 pmid: 36779330
[31]	NATALE G, PIGNATARO A, MARINO G, et al. Transcranial magnetic stimulation exerts "rejuvenation" effects on corticostriatal synapses after partial dopamine depletion[J]. Mov Disord, 2021, 36(10): 2254-2263. doi: 10.1002/mds.v36.10
[32]	NARDONE R, HÖLLER Y, LANGTHALER P B, et al. rTMS of the prefrontal cortex has analgesic effects on neuropathic pain in subjects with spinal cord injury[J]. Spinal Cord, 2017, 55(1): 20-25. doi: 10.1038/sc.2016.87 pmid: 27241450
[33]	KOUTSOMITROS T, EVAGOROU O, SCHUHMANN T, et al. Advances in transcranial magnetic stimulation (TMS) and its applications in resistant depression[J]. Psychiatriki, 2021, 32(Supplement I): 90-98. doi: 10.22365/jpsych.2021.054 pmid: 34990384
[34]	CARDENAS V A, BHAT J V, HORWEGE A M, et al. Anatomical and fMRI-network comparison of multiple DLPFC targeting strategies for repetitive transcranial magnetic stimulation treatment of depression[J]. Brain Stimul, 2022, 15(1): 63-72. doi: 10.1016/j.brs.2021.11.008
[35]	VEMPATI R, SHARMA L D. EEG rhythm based emotion recognition using multivariate decomposition and ensemble machine learning classifier[J]. Neurosci Methods, 2023, 393: 109879. doi: 10.1016/j.jneumeth.2023.109879
[36]	FARABBI A, POLO E M, BARBIERI R, et al. Comparison of different emotion stimulation modalities: an EEG signal analysis[J]. Annu Int Conf IEEE Eng Med Biol Soc, 2022, 2022: 3710-3713. doi: 10.1109/EMBC48229.2022.9871725 pmid: 36086568

组别	n	性别(男/女)/n	年龄/岁	病程/d
M1区刺激组	25	12/13	32.68±6.66	55.88±19.55
联合刺激组	25	15/10	31.32±7.84	59.28±21.13
χ²/t值		0.325	-0.661	0.591
P值		0.569	0.512	0.558

组别	n	治疗前	治疗后	t值	P值
M1区刺激组	21	17.33±2.97	8.90±2.64	-10.988	< 0.001
联合刺激组	23	17.78±2.78	5.96±3.31	-18.214	< 0.001
t值		0.518	-3.244
P值		0.607	0.002

组别	n	治疗前	治疗后	t值	P值
M1区刺激组	21	7.29±1.38	3.48±1.50	-8.085	< 0.001
联合刺激组	23	7.43±1.65	2.30±1.33	-11.506	< 0.001
t值		0.323	-2.744
P值		0.748	0.009

组别	n	治疗前	治疗后	Z值	P值
M1区刺激组	21	7(6, 8)	3(2, 4)	-4.040	< 0.001
联合刺激组	23	8(6, 9)	3(1, 3)	-4.220	< 0.001
Z值		-0.938	-1.973
P值		0.348	0.048

组别	n	治疗前	治疗后	t值	P值
M1区刺激组	21	2.81±1.12	2.04±1.16	-2.769	0.012
联合刺激组	23	2.74±1.25	1.26±1.14	-7.895	< 0.001
t值		-0.196	-2.270
P值		0.846	0.028

Effect of high-frequency repetitive transcranial magnetic stimulation in M1 region combined with dorsolateral prefrontal cortex on electroencephalogram θ frequency band amplitude of patients with neuropathic pain after spinal cord injury

RichHTML

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

Figures/Tables 10

References 36

Related Articles 15

Metrics

Comments

Recommended 0

组别	n	治疗前	治疗后	t值	P值
M1区刺激组	21	9.43±2.20	6.57±3.08	-4.710	< 0.001
联合刺激组	23	8.96±3.39	4.61±2.61	-5.491	< 0.001
t值		-0.542	-2.290
P值		0.591	0.027

组别	n	治疗前	治疗后	t值	P值
M1区刺激组	21	8.38±2.75	6.38±2.38	-2.523	0.020
联合刺激组	23	8.30±2.91	4.48±2.97	-4.816	< 0.001
t值		-0.089	-2.333
P值		0.929	0.025

区域	组别	n	治疗前	治疗后	t值	P值
前额区	M1区刺激组	21	1.44±0.17	1.20±0.10	-5.243	< 0.001
前额区	联合刺激组	23	1.45±0.13	1.09±0.15^a	-9.152	< 0.001
额区	M1区刺激组	21	1.52±0.2	1.23±0.13	-5.721	< 0.001
额区	联合刺激组	23	1.51±0.16	1.20±0.11^b	-6.515	< 0.001
侧额区	M1区刺激组	21	1.09±0.18	1.03±0.12	-1.483	0.154
侧额区	联合刺激组	23	1.07±0.17	0.99±0.13	-1.915	0.068
中央区	M1区刺激组	21	1.30±0.18	1.24±0.13	-1.212	0.238
中央区	联合刺激组	23	1.26±0.17	1.07±0.11^c	-4.630	< 0.001
颞区	M1区刺激组	21	0.95±0.06	0.96±0.05	0.984	0.337
颞区	联合刺激组	23	0.95±0.05	0.93±0.09	-0.772	0.448
顶区	M1区刺激组	21	1.31±0.16	1.33±0.11	0.472	0.645
顶区	联合刺激组	23	1.42±0.18	1.08±0.12^d	-8.675	< 0.001
后颞区	M1区刺激组	21	0.98±0.05	0.95±0.05	-1.534	0.142
后颞区	联合刺激组	23	0.97±0.1	0.95±0.06	-0.494	0.627
枕区	M1区刺激组	21	0.96±0.06	0.93±0.07	-1.393	0.179
枕区	联合刺激组	23	0.94±0.06	0.97±0.05	1.710	0.103

[1]	WANG Haiyun, WANG Yin, ZHOU Xinjie, HE Aiqun. Effect of transcranial direct current stimulation combined with acupuncture on central and upper limb function in stroke patients based on central-peripheral-central theory [J]. 《Chinese Journal of Rehabilitation Theory and Practice》, 2023, 29(8): 919-925.
[2]	CHEN Yiting, WANG Qian, CUI Shenhong, LI Yingcai, ZHANG Siyu, WEI Yanxu, REN Hui, LENG Jun, CHEN Bin. Effect of bilateral sequential repetitive transcranial magnetic stimulation on motor function of upper limbs in stroke patients [J]. 《Chinese Journal of Rehabilitation Theory and Practice》, 2023, 29(8): 926-932.
[3]	MENG Xiangqiang, XIONG Qi, CHEN Gengfa, BAI Yang, ZOU Tianzi, FENG Zhen. Effect of repetitive transcranial magnetic stimulation combined with median nerve electrical stimulation on patients with prolonged disorders of consciousness in different age [J]. 《Chinese Journal of Rehabilitation Theory and Practice》, 2023, 29(8): 940-947.
[4]	LI Fang, HUO Su, DU Jubao, LIU Xiuzhen, LI Xiaoshuang, SONG Weiqun. Effect of transcranial direct current stimulation combined with task-oriented rehabilitation training on forelimb motor dysfunction in rats with spinal cord injury [J]. 《Chinese Journal of Rehabilitation Theory and Practice》, 2023, 29(7): 777-781.
[5]	LIU Ning, LIU Yuquan, ZHU Bin, YU Lingjia, TAN Haining, YANG Yong, LI Xiang. Application of International Standards for Neurological Classification of Spinal Cord Injury in China: a bibliometrics re-analysis [J]. 《Chinese Journal of Rehabilitation Theory and Practice》, 2023, 29(7): 808-815.
[6]	WANG Yiji, ZHOU Hongjun, HE Zejia, LIU Genlin, ZHENG Ying, HAO Chunxia, WEI Bo, KANG Haiqiong, ZHANG Ying, LU Xiaolei, YUAN Yuan, MENG Qianru. Relationship between symmetry of lower limb function and gait symmetry in patients with incomplete spinal cord injury [J]. 《Chinese Journal of Rehabilitation Theory and Practice》, 2023, 29(6): 639-645.
[7]	YUAN Yuan, ZHOU Hongjun, CONG Xinying, LIU Genlin, WEI Bo, ZHENG Ying, HAO Chunxia, ZHANG Ying, WANG Yiji, KANG Haiqiong, LU Xiaolei, MENG Qianru. Relationship between impairment and magnetic resonance imaging finding in patients with traumatic cervical spinal cord injury after surgery [J]. 《Chinese Journal of Rehabilitation Theory and Practice》, 2023, 29(6): 725-730.
[8]	JIANG Le, DU Liangjie, HUANG Fubiao. Mood states and cognitive performance in patients with complete spinal cord injury [J]. 《Chinese Journal of Rehabilitation Theory and Practice》, 2023, 29(5): 576-581.
[9]	GUO Shuang, XIE Yongqi, ZHANG Liang, ZHANG Chunjia, PENG Run, YANG Degang, YANG Mingliang. Related factors and prediction model for neurological outcome of dance-associated pediatric spinal cord injury without radiographic abnormality [J]. 《Chinese Journal of Rehabilitation Theory and Practice》, 2023, 29(5): 582-589.
[10]	WANG Yan, JIN Longtao. Effect of acupuncture on children with attention deficit hyperactivity disorder [J]. 《Chinese Journal of Rehabilitation Theory and Practice》, 2023, 29(5): 615-620.
[11]	HU Xueyan, JIANG Xiaofeng, SHAN Lei, YANG Lingyu, CHEN Yudong, MA Lin, LIU Lixu, ZHANG Tong. Effect of low frequency or high frequency repetitive transcranial magnetic stimulation on stroke patients with nonfluent aphasia [J]. 《Chinese Journal of Rehabilitation Theory and Practice》, 2023, 29(3): 249-255.
[12]	SUN Fengbao, ZENG Yaqin, OUYANG Yao, JIN Zhenhua, ZHANG Xiaofeng. Effect of low frequency repetitive transcranial magnetic stimulation combined with bilateral isokinematic training on upper limb motor function of stroke patients [J]. 《Chinese Journal of Rehabilitation Theory and Practice》, 2023, 29(3): 256-261.
[13]	LIANG Tianjia, LONG Yaobin, LU Liyan, ZHOU Jinying, HUANG Fucai, WU Yingchao, LONG Yaoxiang, WEI Xiaocui. Effect of proprioceptive neuromuscular facilitation rope training and repetitive transcranial magnetic stimulation on upper limb motor function of stroke patients with hemiplegia [J]. 《Chinese Journal of Rehabilitation Theory and Practice》, 2023, 29(3): 262-268.
[14]	HUANG Kaiqi, XIN Rong, LING Gengqiang, WANG Pu. Repetitive transcranial magnetic stimulation for lower limb dysfunction post stroke: a scoping review [J]. 《Chinese Journal of Rehabilitation Theory and Practice》, 2023, 29(3): 286-293.
[15]	MA Qishou, LI Zhongyuan, FU Weiwei, LIN Qian. Effect of repetitive transcranial magnetic stimulation on walking of stroke patients at recovery stage [J]. 《Chinese Journal of Rehabilitation Theory and Practice》, 2023, 29(2): 167-173.