Ann Rehabil Med.  2016 Oct;40(5):806-815. 10.5535/arm.2016.40.5.806.

Prediction of Motor Recovery Using Quantitative Parameters of Motor Evoked Potential in Patients With Stroke

• Jo JY
• Lee A
• Kim MS
• Park E
• Chang WH
• Shin YI
• Kim YH

• KMID: 2382912
• DOI: http://doi.org/10.5535/arm.2016.40.5.806

Abstract

OBJECTIVE
To investigate the clinical significance of quantitative parameters in transcranial magnetic stimulation (TMS)-induced motor evoked potentials (MEP) which can be adopted to predict functional recovery of the upper limb in stroke patients in the early subacute phase.
METHODS
One hundred thirteen patients (61 men, 52 women; mean age 57.8±12.2 years) who suffered faiarst-ever stroke were included in this study. All participants underwent TMS-induced MEP session to assess the corticospinal excitability of both hand motor cortices within 3 weeks after stroke onset. After the resting motor threshold (rMT) was assessed, five sweeps of MEP were performed, and the mean amplitude of the MEP was measured. Latency of MEP, volume of the MEP output curve, recruitment ratios, and intracortical inhibition and facilitation were also measured. Motor function was assessed using the Fugl-Meyer Assessment scale (FMA) within 3 weeks and at 3 months after stroke onset. Correlation analysis was performed between TMS-induced MEP derived measures and FMA scores.
RESULTS
In the MEP response group, rMT and rMT ratio measures within 3 weeks after stroke onset showed a significant negative correlation with the total and upper limb FMA scores at 3 months after stroke (p<0.001). Multiple regression analysis revealed that FMA score and rMT ratio, but not rMT within 3 weeks were independent prognostic factors for FMA scores at 3 months after stroke.
CONCLUSION
These results indicated that the quantitative parameter of TMS-induced MEP, especially rMT ratio in the early subacute phase, could be used as a parameter to predict motor function in patients with stroke.

Keyword

Motor recovery; Motor evoked potentials (MEP); Transcranial magnetic stimulation; Stroke; Prognosis

MeSH Terms

Evoked Potentials, Motor*
Female
Hand
Humans
Male
Prognosis
Stroke*
Transcranial Magnetic Stimulation
Upper Extremity

Reference

1. Minino AM, Murphy SL, Xu J, Kochanek KD. Deaths: final data for 2008. Natl Vital Stat Rep. 2011; 59:1–126.

2. Duncan PW, Goldstein LB, Matchar D, Divine GW, Feussner J. Measurement of motor recovery after stroke. Outcome assessment and sample size requirements. Stroke. 1992; 23:1084–1089. PMID: 1636182.

3. Groisser BN, Copen WA, Singhal AB, Hirai KK, Schaechter JD. Corticospinal tract diffusion abnormalities early after stroke predict motor outcome. Neurorehabil Neural Repair. 2014; 28:751–760. PMID: 24519021.

4. Shelton FN, Reding MJ. Effect of lesion location on upper limb motor recovery after stroke. Stroke. 2001; 32:107–112. PMID: 11136923.

5. Nelles G, Spiekramann G, Jueptner M, Leonhardt G, Muller S, Gerhard H, et al. Evolution of functional reorganization in hemiplegic stroke: a serial positron emission tomographic activation study. Ann Neurol. 1999; 46:901–909. PMID: 10589543.

6. Kwon YH, Son SM, Lee J, Bai DS, Jang SH. Combined study of transcranial magnetic stimulation and diffusion tensor tractography for prediction of motor outcome in patients with corona radiata infarct. J Rehabil Med. 2011; 43:430–434. PMID: 21403983.

7. Rapisarda G, Bastings E, de Noordhout AM, Pennisi G, Delwaide PJ. Can motor recovery in stroke patients be predicted by early transcranial magnetic stimulation? Stroke. 1996; 27:2191–2196. PMID: 8969779.

8. Nascimbeni A, Gaffuri A, Imazio P. Motor evoked potentials: prognostic value in motor recovery after stroke. Funct Neurol. 2006; 21:199–203. PMID: 17367579.

9. Choi TW, Jang SG, Yang SN, Pyun SB. Factors affecting the motor evoked potential responsiveness and parameters in patients with supratentorial stroke. Ann Rehabil Med. 2014; 38:19–28. PMID: 24639922.

10. Kim GW, Won YH, Park SH, Seo JH, Ko MH. Can motor evoked potentials be an objective parameter to assess extremity function at the acute or subacute stroke stage? Ann Rehabil Med. 2015; 39:253–261. PMID: 25932422.

11. Lee SY, Lim JY, Kang EK, Han MK, Bae HJ, Paik NJ. Prediction of good functional recovery after stroke based on combined motor and somatosensory evoked potential findings. J Rehabil Med. 2010; 42:16–20. PMID: 20111839.

12. Song Z, Dang L, Zhou Y, Dong Y, Liang H, Zhu Z, et al. Why do stroke patients with negative motor evoked potential show poor limb motor function recovery? Neural Regen Res. 2013; 8:2713–2724. PMID: 25206582.

13. Hendricks HT, Pasman JW, van Limbeek J, Zwarts MJ. Motor evoked potentials in predicting recovery from upper extremity paralysis after acute stroke. Cerebrovasc Dis. 2003; 16:265–271. PMID: 12865615.

14. Pennisi G, Rapisarda G, Bella R, Calabrese V, Maertens De Noordhout A, et al. Absence of response to early transcranial magnetic stimulation in ischemic stroke patients: prognostic value for hand motor recovery. Stroke. 1999; 30:2666–2670. PMID: 10582994.

15. Nardone R, Tezzon F. Inhibitory and excitatory circuits of cerebral cortex after ischaemic stroke: prognostic value of the transcranial magnetic stimulation. Electromyogr Clin Neurophysiol. 2002; 42:131–136. PMID: 11977426.

16. 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; 126:1071–1107. PMID: 25797650.

17. Hallett M, Chen R, Ziemann U, Cohen LG. Reorganization in motor cortex in amputees and in normal volunteers after ischemic limb deafferentation. Electroencephalogr Clin Neurophysiol Suppl. 1999; 51:183–187. PMID: 10590950.

18. Nitsche MA, Paulus W. Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology. 2001; 57:1899–1901. PMID: 11723286.

19. Nitsche MA, Roth A, Kuo MF, Fischer AK, Liebetanz D, Lang N, et al. Timing-dependent modulation of associative plasticity by general network excitability in the human motor cortex. J Neurosci. 2007; 27:3807–3812. PMID: 17409245.

20. Ziemann U, Lönnecker S, Steinhoff BJ, Paulus W. Effects of antiepileptic drugs on motor cortex excitability in humans: a transcranial magnetic stimulation study. Ann Neurol. 1996; 40:367–378. PMID: 8797526.

21. Uhm KE, Kim YH, Yoon KJ, Hwang JM, Chang WH. BDNF genotype influence the efficacy of rTMS in stroke patients. Neurosci Lett. 2015; 594:117–121. PMID: 25817361.

22. Zhang X, Woolley DG, Swinnen SP, Feys H, Meesen R, Wenderoth N. Changes in corticomotor excitability and intracortical inhibition of the primary motor cortex forearm area induced by anodal tDCS. PLoS One. 2014; 9:e101496. PMID: 24999827.

23. Groppa S, Oliviero A, Eisen A, Quartarone A, Cohen LG, Mall V, et al. A practical guide to diagnostic transcranial magnetic stimulation: report of an IFCN committee. Clin Neurophysiol. 2012; 123:858–882. PMID: 22349304.

24. McConnell KA, Nahas Z, Shastri A, Lorberbaum JP, Kozel FA, Bohning DE, et al. The transcranial magnetic stimulation motor threshold depends on the distance from coil to underlying cortex: a replication in healthy adults comparing two methods of assessing the distance to cortex. Biol Psychiatry. 2001; 49:454–459. PMID: 11274657.

25. Takechi U, Matsunaga K, Nakanishi R, Yamanaga H, Murayama N, Mafune K, et al. Longitudinal changes of motor cortical excitability and transcallosal inhibition after subcortical stroke. Clin Neurophysiol. 2014; 125:2055–2069. PMID: 24636830.

26. Prashantha DK, Sriranjini SJ, Sathyaprabha TN, Nagaraja D, Pal PK. Evaluation of the motor cortical excitability changes after ischemic stroke. Ann Indian Acad Neurol. 2013; 16:394–397. PMID: 24101824.

27. Cicinelli P, Pasqualetti P, Zaccagnini M, Traversa R, Oliveri M, Rossini PM. Interhemispheric asymmetries of motor cortex excitability in the postacute stroke stage: a paired-pulse transcranial magnetic stimulation study. Stroke. 2003; 34:2653–2658. PMID: 14551397.

28. Takeuchi N, Oouchida Y, Izumi S. Motor control and neural plasticity through interhemispheric interactions. Neural Plast. 2012; 2012:823285. PMID: 23326685.

29. Shimizu T, Hosaki A, Hino T, Sato M, Komori T, Hirai S, et al. Motor cortical disinhibition in the unaffected hemisphere after unilateral cortical stroke. Brain. 2002; 125(Pt 8):1896–1907. PMID: 12135979.

30. Matamala JM, Nunez C, Lera L, Verdugo RJ, Sanchez H, Albala C, et al. Motor evoked potentials by transcranial magnetic stimulation in healthy elderly people. Somatosens Mot Res. 2013; 30:201–205. PMID: 23767989.

31. Liepert J, Hamzei F, Weiller C. Motor cortex disinhibition of the unaffected hemisphere after acute stroke. Muscle Nerve. 2000; 23:1761–1763. PMID: 11054757.

32. Manganotti P, Patuzzo S, Cortese F, Palermo A, Smania N, Fiaschi A. Motor disinhibition in affected and unaffected hemisphere in the early period of recovery after stroke. Clin Neurophysiol. 2002; 113:936–943. PMID: 12048054.

33. Morishita T, Ninomiya M, Uehara K, Funase K. Increased excitability and reduced intracortical inhibition in the ipsilateral primary motor cortex during a fine-motor manipulation task. Brain Res. 2011; 1371:65–73. PMID: 21093420.

34. Blicher JU, Jakobsen J, Andersen G, Nielsen JF. Cortical excitability in chronic stroke and modulation by training: a TMS study. Neurorehabil Neural Repair. 2009; 23:486–493. PMID: 19221005.

35. Garry MI, Kamen G, Nordstrom MA. Hemispheric differences in the relationship between corticomotor excitability changes following a fine-motor task and motor learning. J Neurophysiol. 2004; 91:1570–1578. PMID: 14627660.

36. Blicher JU, Nielsen JF. Cortical and spinal excitability changes after robotic gait training in healthy participants. Neurorehabil Neural Repair. 2009; 23:143–149. PMID: 19047360.

37. Lotze M, Braun C, Birbaumer N, Anders S, Cohen LG. Motor learning elicited by voluntary drive. Brain. 2003; 126(Pt 4):866–872. PMID: 12615644.

38. Takeuchi N, Tada T, Toshima M, Ikoma K. Correlation of motor function with transcallosal and intracortical inhibition after stroke. J Rehabil Med. 2010; 42:962–966. PMID: 21031294.

39. Paulus W, Classen J, Cohen LG, Large CH, Di Lazzaro V, Nitsche M, et al. State of the art: Pharmacologic effects on cortical excitability measures tested by transcranial magnetic stimulation. Brain Stimul. 2008; 1:151–163. PMID: 20633382.

40. Kothari M, Svensson P, Nielsen JF, Baad-Hansen L. Influence of position and stimulation parameters on intracortical inhibition and facilitation in human tongue motor cortex. Brain Res. 2014; 1557:83–89. PMID: 24534367.