Content » Vol 45, Issue 9

Original report

Effects of repetitive trascranial magnetic stimulation on repetitive facilitation exercises of the hemiplegic hand in chronic stroke patients

Table III. Pre- and post-treatment Modified Ashworth Scale (MAS) score

Pre-treatment

Median (range)

Post-treatment

Median (range)

MAS (elbow)

Motor rTMS

Sham rTMS

4 weeks

1 (0–1.5)

1 (0–1.5)

1 (0–1.5)

1 (0–2)

1 (0–1.5)

1 (0–2)

MAS (wrist)

Motor rTMS

Sham rTMS

4 weeks

1 (0–2)

1 (0–1.5)

1 (0–1.5)

1 (0–2)

1 (0–2)

1 (0–2)

MAS (fingers)

Motor rTMS

Sham rTMS

4 weeks

1 (0–2)

1 (0–1.5)

1 (0–1.5)

0 (0–2)

0 (0–2)

0 (0–2)*

*p<0.05 Comparison between pre- and post-treatment values in each group according to the Wilcoxon t-test.

A MAS score of 1+ was treated as 1.5.

DISCUSSION

Multiple sessions of 1-Hz rTMS facilitated the effects of RFEs in improving the motor function of the affected upper limb, but did not change spasticity in chronic stroke patients. Significantly larger improvements were observed in the ARAT score compared with sham rTMS. The FMA, ARAT and STEF scores improved significantly during the motor rTMS sessions, but the trend did not reach statistical significance during sham rTMS sessions. The MAS score and F/M ratio of the affected side did not change significantly. These results demonstrated that priming by rTMS enhanced the improvement in the affected hand function through a motor-training effect in chronic patients after stroke. Combining 1-Hz rTMS to the unaffected motor cortex with RFEs produced significantly greater improvement than sham rTMS.

The present study extends the findings of previous studies. This study was based on the hypothesis that the application of 1-Hz rTMS to the unaffected motor cortex decreased the transcallosal inhibition (2) and increased the local excitability of the affected motor cortex, which could represent an increase in synaptic efficacy. Previous studies reported that 1-Hz rTMS to the unaffected motor cortex improved the function of affected upper limbs in chronic stroke patients. Single sessions of 1-Hz rTMS for 25 min (1,500 pulses) improved the pinch acceleration (2). Stimulation at 1 Hz (600 pulses) decreased single and choice reaction time (4). Single sessions of 1-Hz rTMS for 25 min (1,500 pulses) enhanced the effect of motor training on pinch force in stroke patients (3). Multiple sessions of 1-Hz rTMS for 25 min (1,500 pulses) for 10 days boosted the effect of physiotherapy in chronic stroke patients (10). In the present study, 1-Hz rTMS for 4 min (240 pulses) facilitated the effect of RFEs, supporting and extending the findings of previous studies.

Although high correlations have previously been documented for the FMA and ARAT (18), there was a difference in gain between sessions for FMA and ARAT in this study. STEF was designed to evaluate the speed of carrying objects, which might be difficult to differentiate among subjects with moderate impairment. The small size of the study group might prevent us from detecting a clear difference in gain between sessions for FMA, STEF and ARAT.

Short duration (4 min, 240 pulses) 1-Hz rTMS facilitated the effect of RFEs on hemiplegic upper-limb function in our study. The effects would have been greater if the period of rTMS was longer. But there were two reasons why we used 4 min 1-Hz rTMS, even though many previous studies have used 25 min. First, previous studies reported the effect of short duration of 1-Hz rTMS. MEPs were significantly reduced after 1-Hz rTMS for 4 min (240 pulses) (19). Significant inhibition continued for 5 min after 150 pulses of 1-Hz rTMS (20). Short duration 1-Hz rTMS could affect the excitability of the motor cortex. Stimulation at 1 Hz, 10 min (600 pulses) decreased single and choice reaction time in stroke patients (4). Thus, it might be possible to induce a temporary state in which motor learning was optimized even after short duration 1-Hz rTMS. Secondly, short-lasting effects of 1-Hz rTMS were considered sufficient for enhancing the effect of RFEs, because the RFEs were able to facilitate and directly repeat isolated movements in the hemiplegic upper limb over a relatively short time-period. If the minimum period of effective rTMS was known, it might be of great benefit to stroke patients. Koganemaru et al. (21) reported that combining motor training with 5-Hz rTMS could facilitate use-dependent plasticity and achieve functional recovery of motor impairments. RFEs can repeat and improve target movements, such as finger extension, thumb abduction and elbow extension. Combining rTMS and RFEs might facilitate use-dependent plasticity. Short-duration of 1-Hz rTMS to the unaffected motor cortex and RFEs could therefore be an effective rehabilitative approach for patients with hemiplegic stroke.

F-waves can be used to study long-pathway nerve conduction and motor neurone excitability. We used MAS scores and F-waves to measure spasticity. Although we expected 1-Hz rTMS to reduce spasticity and F-wave amplitudes, the MAS score and F/M ratio of the affected upper limb did not change during our study. We put forward 3 reasons why the MAS and F/M ratio of the affected upper limb did not change. First, the adequacy of MAS is not conclusive, although the MAS is often used to assess spasticity (22). Secondly, the range of MAS scores before the first session were 0–2, thus we only measured mild-to-moderate spasticity. MAS scores might change after rTMS sessions in patients with severe spasticity. Thirdly, the rTMS conditions are different from other reports. Valle et al. (23) showed that there was a significant reduction in spasticity after multiple sessions of 5-Hz rTMS, but not 1-Hz. Mally & Dinya (24) showed that multiple sessions of 1-Hz rTMS using a circular coil significantly reduced the spasticity of affected limbs in chronic stroke patients. Kondo et al. (25) reported that a single session of 1-Hz rTMS significantly decreased the F/M ratio in affected upper limbs. Reducing spasticity after rTMS in stroke patients might thus depend on the stimulated area or the duration and frequency of rTMS.

Some limitations of the current study should be noted. First, we did not measure neurophysiological data except for upper-limb F-waves. We were unable to investigate whether 1-Hz rTMS decreased excitability in the intact hemisphere and increased excitability in the affected hemisphere. Secondly, our sham rTMS may affect the sensory cortex, because the position 5 cm posterior of the motor cortex is close to the sensory cortex. Thus, the motor cortex may be influenced indirectly through the sensory cortex. Thirdly, the small size of the study group prevented us from examining the effects of differences in the severity of hemiplegia using subgroup analysis. Further research is needed to confirm the effectiveness of combining 1-Hz rTMS and RFEs.

In conclusion, this study shows that multiple sessions of 1-Hz rTMS of the unaffected motor cortex facilitates the effects of RFEs on hemiplegic upper-limb function in chronic stroke patients.

REFERENCES

1. Murase N, Duque J, Mazzocchio R, Cohen LG. Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol 2004; 55: 400–409.

2. Takeuchi N, Chuma T, Matsuo Y, Watanabe I, Ikoma K. Repetitive transcranial magnetic stimulation of contralesional primary motor cortex improves hand function after stroke. Stroke 2005; 36: 2681–2686.

3. Takeuchi N, Tada T, Toshima M, Chuma T, Matsuo Y, Ikoma K. Inhibition of the unaffected motor cortex by 1 Hz repetitive transcranial magnetic stimulation enhances motor performance and training effect of the paretic hand in patients with chronic stroke. J Rehabil Med 2008; 40: 298–303.

4. Mansur CG, Fregni F, Boggio PS, Riberto M, Galluci-Neto J, Santos CM, et al. A sham stimulation-controlled trial of rTMS of the unaffected hemisphere in stroke patients. Neurology 2005; 64: 1802–1804.

5. Nowak DA, Grefkes C, Dafotakis M, Eickhoff S, Kust J, Karbe H, et al. Effects of low-frequency repetitive transcranial magnetic stimulation of the contralesional primary motor cortex on movement kinematics and neural activity in subcortical stroke. Arch Neurol 2008; 65: 741–747.

6. Dafotakis M, Grefkes C, Eickhoff SB, Karbe H, Fink GR, Nowak DA. Effects of rTMS on grip force control following subcortical stroke. Exp Neurol 2008; 211: 407–412.

7. Fregni F, Boggio PS, Valle AC, Rocha RR, Duarte J, Ferreira MJL, et al. A sham-controlled trial of a 5-day course of repetitive transcranial magnetic stimulation of the unaffected hemisphere in stroke patients. Stroke 2006; 37: 2115–2122.

8. Emara TH, Moustafa RR, ElNahas NM, ElGanzoury AM, Abdo TA, Mohamed SA, et al. Repetitive transcranial magnetic stimulation at 1Hz and 5Hz produces sustained improvement in motor function and disability after ischaemic stroke. Eur J Neurol 2010; 17: 1203–1209.

9. Hsu WY, Cheng CH, Liao KK. Lee IH, Lin YY. Effects of repetitive magnetic stimulation on motor function in patients with stroke. A meta-analysis. Stroke 2012; 43: 1849–1857.

10. Avenanti A, Coccia M, Ladavas E, Provinciali L, Ceravolo MG. Low-frequency rTMS promotes use-dependent motor plasticity in chronic stroke, a randomized trial. Neurology 2012; 78: 256–264.

11. Seniów J, Bilik M, Lesniak M, Waldowski K, Iwanski S, Czlonkowska A. Transcranial magnetic stimulation combined with physiotherapy in rehabilitation of poststroke hemiparesis: a randomized, double-blind, placebo-controlled study. Neurorehabil Neural Repair 2012; 26: 1072–1079.

12. Kawahira K, Shimodozono M, Etoh S, Kamada K, Noma T, Tanaka N. Effects of intensive repetition of a new facilitation technique on motor functional recovery of the hemiplegic upper limb and hand. Brain Inj 2010; 24: 1202–1213.

13. Shimodozono M, Noma T, Nomoto Y, Hisamatsu N, Kamada K, Miyata R, et al. Benefits of a repetitive facilitative exercise program for the upper paretic extremity after subacute stroke: a randomized controlled trial. Neurorehabil Neural Repair 2013; 27: 296–305.

14. Fugl-Meyer AR, Jaasko L, Leyman I, Olsson S, Steglind S. The post-stroke hemiplegic patient. 1. A method for evaluation of physical performance. Scand J Rehab Med 1975; 7: 13–31.

15. Yozbatiran N, Der-Yeghiaian L, Cramer SC. A standardized approach to performing the action research arm test. Neurorehabil Neural Repair 2008, 22: 78–90.

16. Bohannon RW, Smith MB. Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther 1987; 67: 206–207.

17. Rossi S, Hallett M, Rossini PM, Pascual-Leone A, The Safety of TMS Consensus Group. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 2009; 120: 2008–2039.

18. Platz T, Pinkowski C, van Wijck F, Kim I-H, di Bella P, Johnson G. Reliability and validity of arm function assessment with standardized guidelines for the FugI-Meyer Test, Action Research Arm Test and Box and Block Test: a multicentre study. Clin Rehabil 2005; 19: 404–411.

19. Maeda F, Keenan JP, Tormos JM, Topka H, Pascual-Leone A. Modulation of corticospinal excitability by repetitive transcranial magnetic stimulation. Clin Neurophysiol 2000; 111: 800–805.

20. Touge T, Gerschlager W, Brown P, Rothwell JC. Are the after-effects of low-frequency rTMS on motor cortex excitability due to changes in the efficacy of cortical synapses? Clin Neurophysiol 2001; 112: 2138–2145.

21. Koganemaru S, Mima T, Thabit MN, Ikkaku T, Shimada K, Kanematsu M, et al. Recovery of upper-limb function due to enhanced use-dependent plasticity in chronic stroke patients. Brain 2010; 133; 3373–3384.

22. Alibiglou L, Rymer WZ, Harvey RL, Mirbagheri MM. The relation between Ashworth scores and neuromechanical measurements of spasticity following stroke. J Neuroengineering Rehabil 2008, 15: 5–18.

23. Valle AC, Dionisio K, Pitskel NB, Pascual-Leone A, Orsati F, Ferreira MJ, et al. Low and high-frequency repetitive transcranial magnetic stimulation for the treatment of spasticity. Dev Med Child Neurol 2007; 49: 534–538.

24. Mally J, Dinya E. Recovery of motor disability and spasticity in post-stroke after repetitive transcranial magnetic stimulation (rTMS). Brain Res Bull 2008; 76: 388–395.

25. Kondo T, Kakuda W, Yamada N, Shimizu M, Hagino H, Abo M. Effect of low-frequency rTMS on motor neuron excitability after stroke. Acta Neurol Scand 2013; 127: 26–30.

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