Mixed effectiveness of rTMS and retraining in the treatment of focal hand dystonia

Teresa J Kimberley, Rebekah L S Schmidt, Mo Chen, Dennis D Dykstra, Cathrin M Buetefisch, Teresa J Kimberley, Rebekah L S Schmidt, Mo Chen, Dennis D Dykstra, Cathrin M Buetefisch

Abstract

Though the pathophysiology of dystonia remains uncertain, two primary factors implicated in the development of dystonic symptoms are excessive cortical excitability and impaired sensorimotor processing. The aim of this study was to determine the functional efficacy of an intervention combining repetitive transcranial magnetic stimulation (rTMS) and sensorimotor retraining. A randomized, single-subject, multiple baseline design with crossover was used to examine participants with focal hand dystonia (FHD) (n = 9).

Intervention: 5 days rTMS + sensorimotor retraining (SMR) vs. Five days rTMS + control therapy (CTL) (which included stretching and massage). The rTMS was applied to the premotor cortex at 1 Hz at 80% resting motor threshold for 1200 pulses. For sensorimotor retraining, a subset of the Learning-based Sensorimotor Training program was followed. Each session in both groups consisted of rTMS followed immediately by 30 min of the therapy intervention (SMR or CTL). Contrary to our hypothesis, group analyses revealed no additional benefit from the SMR training vs. CTL. When analyzed across group however, there was significant improvement from the first baseline assessment in several measures, including tests of sensory ability and self-rated changes. The patient rated improvements were accompanied by a moderate effect size suggesting clinical meaningfulness. These results provide encouragement for further investigation of rTMS in FHD with a need to optimize a secondary intervention and determine likely responders vs. non-responders.

Keywords: human; neuromodulation; rehabilitation; sensory; transcranial magnetic stimulation; writer's cramp.

Figures

Figure 1
Figure 1
Consort diagram of screened and enrolled participants. Participants were randomly assigned to either the rTMS + SMR or rTMS + CTL intervention first and then crossed over to receive the other intervention after 1-month washout. (SMR, sensorimotor retraining intervention; CTL, control intervention; rTMS, repetitive transcranial magnetic stimulation).
Figure 2
Figure 2
Global rating of change (GROC) scores from first baseline to all subsequent assessments. This graph demonstrates mean change (±SE) over time, excluding one participant (#7) who appeared to misunderstand the rating (see text). Note, all individuals received both interventions. CTL-SMR (light gray) received the rTMS + CTL first and then the rTMS + SMR in Phase 2. The SMR-CTL (dark gray) group received rTMS + SMR first and then rTMS + CTL in Phase 2. GROC was assessed at one baseline, post-test and follow up for each phase. (SMR, sensorimotor retraining; rTMS, repetitive transcranial magnetic stimulation; CTL, control).
Figure 3
Figure 3
Arm Dystonia Disability Scale (ADDS) in first phase of treatment (CTLn= 4 in dark gray, SMRn= 5 in light gray). Regardless of intervention, all subjects reported improvement in self-perceived function. Mean (±SE). ADDS was tested at one baseline, post-test and follow up for each phase. (SMR, sensorimotor retraining, rTMS, repetitive transcranial magnetic stimulation, CTL, control).
Figure 4
Figure 4
Single subject analysis. Raw data presented across both phases. Lines represent mean (solid) and two SD (dashed) of baseline; dark gray, SMR; light gray, CTL. Cortical silent period (CSP) duration, average handwriting pressure while drawing loops, Global rating of change (GROC) scores (0, change; 1, almost the same). Improved handwriting quality after both interventions was observed while pressure remained stable. CSP suggests a decrease in excitability at both post-tests and at SMR follow-up.

References

    1. Abbruzzese G., Berardelli A. (2003). Sensorimotor integration in movement disorders. Mov. Disord. 18, 231–240. 10.1002/mds.10327
    1. Altenmuller E., Jabusch H. C. (2010). Focal dystonia in musicians: phenomenology, pathophysiology, triggering factors, and treatment. Med. Probl. Perform. Art. 25, 3–9. 10.1111/j.1468-1331.2010.03048.x
    1. Backman C. L., Harris S. R., Chisholm J. A., Monette A. D. (1997). Single-subject research in rehabilitation: a review of studies using AB, withdrawal, multiple baseline, and alternating treatments designs. Arch. Phys. Med. Rehabil. 78, 1145–1153. 10.1016/S0003-9993(97)90142-8
    1. Belvisi D., Suppa A., Marsili L., Di Stasio F., Parvez A. K., Agostino R., et al. . (2013). Abnormal experimentally-and behaviorally-induced LTP-like plasticity in focal hand dystonia. Exp. Neurol. 240, 64–74. 10.1016/j.expneurol.2012.11.003
    1. Borich M., Arora S., Kimberley T. J. (2009). Lasting effects of repeated rTMS application in focal hand dystonia. Restor. Neurol. Neurosci. 27, 55–65. 10.3233/RNN-2009-0461
    1. Butefisch C. M., Boroojerdi B., Chen R., Battaglia F., Hallett M., Butefisch C. M., et al. . (2005). Task-dependent intracortical inhibition is impaired in focal hand dystonia. Mov. Disord. 20, 545–551. 10.1002/mds.20367
    1. Butefisch C. M., Khurana V., Kopylev L., Cohen L. G., Butefisch C. M., Khurana V., et al. . (2004). Enhancing encoding of a motor memory in the primary motor cortex by cortical stimulation. J. Neurophysiol. 91, 2110–2116. 10.1152/jn.01038.2003
    1. Byl N., Leano J., Cheney L. K., Byl N., Leano J., Cheney L. K. (2002). The Byl–Cheney–Boczai Sensory Discriminator: reliability, validity, and responsiveness for testing stereognosis. J. Hand Ther. 15, 315–330. 10.1016/S0894-1130(02)80003-5
    1. Byl N. N., Archer E. S., McKenzie A., Byl N. N., Archer E. S., McKenzie A. (2009). Focal hand dystonia: effectiveness of a home program of fitness and learning-based sensorimotor and memory training. J. Hand Ther. 22, 183–197. Quiz 198. 10.1016/j.jht.2008.12.003
    1. Byl N. N., McKenzie A. (2000). Treatment effectiveness for patients with a history of repetitive hand use and focal hand dystonia: a planned, prospective follow-up study. J. Hand Ther. 13, 289–301. 10.1016/S0894-1130(00)80021-6
    1. Byl N. N., Nagajaran S., McKenzie A. L. (2003). Effect of sensory discrimination training on structure and function in patients with focal hand dystonia: a case series. Arch. Phys. Med. Rehabil. 84, 1505–1514. 10.1016/S0003-9993(03)00276-4
    1. Caligiuri M. P., Teulings H.-L., Dean C. E., Niculescu A. B., Lohr J. (2009). Handwriting movement analyses for monitoring drug-induced motor side effects in schizophrenia patients treated with risperidone. Hum. Mov. Sci. 28, 633–642. 10.1016/j.humov.2009.07.007
    1. Caligiuri M. P., Teulings H.-L., Filoteo J. V., Song D., Lohr J. B. (2006). Quantitative measurement of handwriting in the assessment of drug-induced parkinsonism. Hum. Mov. Sci. 25, 510–522. 10.1016/j.humov.2006.02.004
    1. Chen R., Lozano A. M., Ashby P. (1999). Mechanism of the silent period following transcranial magnetic stimulation evidence from epidural recordings. Exp. Brain Res. 128, 539–542. 10.1007/s002210050878
    1. Chen W. H., Mima T., Siebner H. R., Oga T., Hara H., Satow T., et al. . (2003). Low-frequency rTMS over lateral premotor cortex induces lasting changes in regional activation and functional coupling of cortical motor areas. Clin. Neurophysiol. 114, 1628–1637. 10.1016/S1388-2457(03)00063-4
    1. Daskalakis Z. J., Möller B., Christensen B. K., Fitzgerald P. B., Gunraj C., Chen R. (2006). The effects of repetitive transcranial magnetic stimulation on cortical inhibition in healthy human subjects. Exp. Brain Res. 174, 403–412. 10.1007/s00221-006-0472-0
    1. Dellon A. L., Kallman C. H. (1983). Evaluation of functional sensation in the hand. J. Hand Surg. Am. 8, 865–870. 10.1016/S0363-5023(83)80083-5
    1. Deng H., Kimberley T. J., Durfee W. K., Dressler B. L., Steil C., Carey J. R. (2013). Combined statistical analysis method assessing fast versus slow movement training in a patient with cerebellar stroke: a single-case study. Phys. Ther. 93, 649–660. 10.2522/ptj.20120121
    1. Di Lazzaro V., Pilato F., Dileone M., Ranieri F., Ricci V., Profice P., et al. . (2006). GABAA receptor subtype specific enhancement of inhibition in human motor cortex. J. Physiol. (Lond). 575, 721–726. 10.1113/jphysiol.2006.114694
    1. Fahn S. (1989). Assessment of the Primary Dystonias, Boston, MA: Butterworths.
    1. Field A. (2009). Discovering Statistics using SPSS. New York, NY: Sage publications.
    1. Fink G. R., Frackowiak R. S., Pietrzyk U., Passingham R. E. (1997). Multiple nonprimary motor areas in the human cortex. J. Neurophysiol. 77, 2164–2174.
    1. Galpern W. R., Coffey C. S., Albanese A., Cheung K., Comella C. L., Ecklund D. J., et al. . (2011). Designing clinical trials for Dystonia. Neurotherapeutics 11, 117–127. 10.1007/s13311-013-0221-6
    1. Gomes-Osman J., Field-Fote E. C. (2015). Improvements in hand function in adults with chronic tetraplegia following a multiday 10-Hz repetitive transcranial magnetic stimulation intervention combined with repetitive task practice. J. Neurol. Phys. Ther. 39, 23–30. 10.1097/NPT.0000000000000062
    1. Hallett M. (2006). Pathophysiology of writer's cramp. Hum. Mov. Sci. 25, 454–463. 10.1016/j.humov.2006.05.004
    1. Hallett M. (2011). Neurophysiology of dystonia: the role of inhibition. Neurobiol. Dis. 42, 177–184. 10.1016/j.nbd.2010.08.025
    1. Hao Z., Wang D., Zeng Y., Liu M. (2013). Repetitive transcranial magnetic stimulation for improving function after stroke. Cochrane Database Syst. Rev. 5:CD008862. 10.1002/14651858.cd008862.pub2
    1. Hess G., Aizenman C. D., Donoghue J. P. (1996). Conditions for the induction of long-term potentiation in layer II/III horizontal connections of the rat motor cortex. J. Neurophys. 75, 1765–1778.
    1. Jung P., Ziemann U. (2009). Homeostatic and nonhomeostatic modulation of learning in human motor cortex. J. Neurosci. 29, 5597–5604. 10.1523/JNEUROSCI.0222-09.2009
    1. Kamper S. J., Maher C. G., Mackay G. (2009). Global rating of change scales: a review of strengths and weaknesses and considerations for design. J. Man. Manipulative Ther. 17, 163–170. 10.1179/jmt.2009.17.3.163
    1. Kendall M. G., Smith B. B. (1939). The problem of m rankings. Ann. Math. Stat. 10, 275–287. 10.1214/aoms/1177732186
    1. Kimberley T. J., Borich M. R., Arora S., Siebner H. R. (2013). Multiple sessions of low-frequency repetitive transcranial magnetic stimulation in focal hand dystonia: clinical and physiological effects. Restor. Neurol. Neurosci. 31, 533–542. 10.3233/RNN-120259
    1. Kimberley T. J., Borich M. R., Prochaska K. D., Mundfrom S. L., Perkins A. E., Poepping J. M. (2009). Establishing the definition and inter-rater reliability of cortical silent period calculation in subjects with focal hand dystonia and healthy controls. Neurosci. Lett. 464, 84–87. 10.1016/j.neulet.2009.08.029
    1. Kimberley T. J., Borich M. R., Schmidt R., Carey J. R., Gillick B. (2015). Focal hand dystonia: individualized intervention with repeated application of repetitive transcranial magnetic stimulation. Arch. Phys. Med. Rehabil. 96, S122–S128. 10.1016/j.apmr.2014.07.426
    1. Kimberley T. J., Di Fabio R. P. (2010). Visualizing the effects of rTMS in a patient sample: small N vs. group level analysis. PLoS ONE 5:e15155. 10.1371/journal.pone.0015155
    1. López-Alonso V., Cheeran B., Río-Rodríguez D., Fernández-del-Olmo M. (2014). Inter-individual variability in response to non-invasive brain stimulation paradigms. Brain Stimul. 7, 372–380. 10.1016/j.brs.2014.02.004
    1. Meunier S., Russmann H., Shamim E., Lamy J. C., Hallett M. (2012). Plasticity of cortical inhibition in dystonia is impaired after motor learning and paired-associative stimulation. Eur. J. Neurosci. 35, 975–986. 10.1111/j.1460-9568.2012.08034.x
    1. Murase N., Rothwell J. C., Kaji R., Urushihara R., Nakamura K., Murayama N., et al. . (2005). Subthreshold low-frequency repetitive transcranial magnetic stimulation over the premotor cortex modulates writer's cramp. Brain 128, 104–115. 10.1093/brain/awh315
    1. Musselman K. E. (2007). Clinical significance testing in rehabilitation research: what, why, and how? Phys. Ther. Rev. 12, 287–296. 10.1179/108331907X223128
    1. Ottenbacher K. J., Maas F. (1999). How to detect effects: statistical power and evidence-based practice in occupational therapy research. Am. J. Occup. Ther. 53, 181–188. 10.5014/ajot.53.2.181
    1. Pomeroy V. M., Cloud G., Tallis R. C., Donaldson C., Nayak V., Miller S. (2007). Transcranial magnetic stimulation and muscle contraction to enhance stroke recovery: a randomized proof-of-principle and feasibility investigation. Neurorehabil. Neural Repair 21, 509–517. 10.1177/1545968307300418
    1. Quartarone A., Rizzo V., Terranova C., Milardi D., Bruschetta D., Ghilardi M. F., et al. . (2014). Sensory abnormalities in focal hand dystonia and non-invasive brain stimulation. Front. Hum. Neurosci. 8:956. 10.3389/fnhum.2014.00956
    1. Ridding M. C., Sheean G., Rothwell J. C., Inzelberg R., Kujirai T. (1995). Changes in the balance between motor cortical excitation and inhibition in focal, task specific dystonia. J. Neurol. Neurosurg. Psychiatry 59, 493–498. 10.1136/jnnp.59.5.493
    1. Rossini P. M., Berardelli A., Deuschl G., Hallett M., Maertens de Noordhout A. M., Paulus W., et al. . (1999). Applications of magnetic cortical stimulation. The International Federation of Clinical Neurophysiology. Electroencephalogr. Clin. Neurophysiol. Suppl. 52, 171–185.
    1. Rossini P. M., Rossi S., Rossini P. M., Rossi S. (2007). Transcranial magnetic stimulation: diagnostic, therapeutic, and research potential. Neurology 68, 484–488. 10.1212/01.wnl.0000250268.13789.b2
    1. Sadnicka A., Hamada M., Bhatia K. P., Rothwell J. C., Edwards M. J. (2014). Cerebellar stimulation fails to modulate motor cortex plasticity in writing dystonia. Mov. Disord. 29, 1304–1307. 10.1002/mds.25881
    1. Siebner H., Tormos J. M., Ceballos-Baumann A. O., Auer C., Catala M. D., Conrad B., et al. . (1999). Low-frequency repetitive transcranial magnetic stimulation of the motor cortex in writer's cramp. Neurology 52, 529–537. 10.1212/WNL.52.3.529
    1. Van Vugt F., Boullet L., Jabusch H.-C., Altenmüller E. (2014). Musician's dystonia in pianists: long-term evaluation of retraining and other therapies. Parkinsonism Relat. Disord. 20, 8–12. 10.1016/j.parkreldis.2013.08.009
    1. Ware J. E., Kosinski M., Dewey J. E., Gandek B. (2000). SF-36 Health survey: Manual and Interpretation Guide. Lincoln, RI: Quality Metric Inc.
    1. Weise D., Schramm A., Beck M., Reiners K., Classen J. (2011). Loss of topographic specificity of LTD-like plasticity is a trait marker in focal dystonia. Neurobiol. Dis. 42, 171–176. 10.1016/j.nbd.2010.11.009
    1. Wissel J., Kabus C., Wenzel R., Klepsch S., Schwarz U., Nebe A., et al. . (1996). Botulinum toxin in writer's cramp: objective response evaluation in 31 patients. J. Neurol. Neurosurg. Psychiatry 61, 172–175. 10.1136/jnnp.61.2.172
    1. World Medical Association. (2013). World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. J. Am. Med. Assoc. 310, 2191. 10.1001/jama.2013.281053
    1. Zeuner K. E., Bara-Jiminez W., Noguchi P. S., Goldstein S. R., Dambrosia J. M., Hallett M. (2002). Sensory training for patients with focal hand dystonia. Ann. Neurol. 51, 593–598. 10.1002/ana.10174
    1. Zeuner K. E., Hallett M., Zeuner K. E., Hallett M. (2003). Sensory training as treatment for focal hand dystonia: a 1-year follow-up. Mov. Disord. 18, 1044–1047. 10.1002/mds.10490
    1. Zeuner K. E., Peller M., Knutzen A., Hallett M., Deuschl G., Siebner H. R. (2008). Motor re-training does not need to be task specific to improve writer's cramp. Mov. Disord. 23, 2319–2327. 10.1002/mds.22222
    1. Zeuner K. E., Peller M., Knutzen A., Holler I., Munchau A., Hallett M., et al. . (2007). How to assess motor impairment in writer's cramp. Mov. Disord. 22, 1102–1109. 10.1002/mds.21294

Source: PubMed

3
Abonner