The Effects of Distributed vs. Condensed Schedule for Robot-Assisted Training with Botulinum Toxin A Injection for Spastic Upper Limbs in Chronic Post-Stroke Subjects

Jen-Wen Hung, Yen-Wei Chen, Yi-Ju Chen, Ya-Ping Pong, Wen-Chi Wu, Ku-Chou Chang, Ching-Yi Wu, Jen-Wen Hung, Yen-Wei Chen, Yi-Ju Chen, Ya-Ping Pong, Wen-Chi Wu, Ku-Chou Chang, Ching-Yi Wu

Abstract

Robot-assisted training (RT) combined with a Botulinum toxin A (BoNT-A) injection has been suggested as a means to optimize spasticity treatment outcomes. The optimal schedule of applying RT after a BoNT-A injection has not been defined. This single-blind, randomized controlled trial compared the effects of two predefined RT approaches as an adjunct to BoNT-A injections of spastic upper limbs in chronic post-stroke subjects. Thirty-six patients received a BoNT-A injection in the affected upper extremity and were randomly assigned to the condensed or distributed RT group. The condensed group received an intervention of four sessions/week for six consecutive weeks. The distributed group attended two sessions/week for 12 consecutive weeks. Each session included 45 min of RT using the InMotion 2.0 robot, followed by 30 min of functional training. The Fugl-Meyer Assessment, Modified Ashworth Scale, Wolf Motor Function Test, Motor Activity Log, and Stroke Self-Efficacy Questionnaire were assessed at pre-training, mid-term, post-training, and at 6 week follow-up, with the exception of the Motor Activity Log, which did not include mid-term measures. After the intervention, both groups had significant improvements in all outcome measures (within-group effects, p < 0.05), with the exception of the Wolf Motor Function Test time score. There were no significant differences between groups and interaction effects in all outcome measures. Our findings suggest that RT provided in a fixed dosage as an adjunct to a BoNT-A injection has a positive effect on participants' impairment and activity levels, regardless of treatment frequency. (ClinicalTrials.gov: NCT03321097).

Keywords: rehabilitation; robotics; spasticity; stroke; upper extremity.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Group means for each assessment time for each outcome measures. Abbreviation: FMA_UE = upper limb subtest of the Fugl-Meyer assessment, SSEQ =Stroke Self-Efficacy Questionnaires, WMFT Time = Wolf Motor Function Test time score, WMFT Function = Wolf Motor Function Test function score, MAL AOU = Motor Activity Log Amount of use score, MAL QOM = Motor Activity Log Quality of movement score, MAS Proximal = Modified Ashworth scale proximal flexors, MAS Distal = Modified Ashworth scale distal flexors.

References

    1. Lundström E., Terént A., Borg J. Prevalence of disabling spasticity 1 year after first-ever stroke. Eur. J. Neurol. 2008;15:533–539. doi: 10.1111/j.1468-1331.2008.02114.x.
    1. Sheean G., Lannin N.A., Turner-Stokes L., Rawicki B., Snow B.J. Botulinum toxin assessment, intervention and after-care for upper limb hypertonicity in adults: International consensus statement. Eur. J. Neurol. 2010;17:74–93. doi: 10.1111/j.1468-1331.2010.03129.x.
    1. Welmer A.-K., Von Arbin M., Holmqvist L.W., Sommerfeld D.K. Spasticity and Its Association with Functioning and Health-Related Quality of Life 18 Months after Stroke. Cerebrovasc. Dis. 2006;21:247–253. doi: 10.1159/000091222.
    1. Andringa A., van de Port I., van Wegen E., Ket J., Meskers C., Kwakkel G. Effectiveness of Botulinum Toxin Treatment for Upper Limb Spasticity Post-stroke Over Different ICF Domains: A Systematic Review and Meta-Analysis. Arch. Phys. Med. Rehabil. 2019;100:1703–1725. doi: 10.1016/j.apmr.2019.01.016.
    1. Esquenazi A., Novak I., Sheean G., Singer B.J., Ward A.B. International consensus statement for the use of botulinum toxin treatment in adults and children with neurological impairments—Iintroduction. Eur. J. Neurol. 2010;17:1–8. doi: 10.1111/j.1468-1331.2010.03125.x.
    1. Bakheit A.M., Zakine B., Maisonobe P., Aymard C., Fhedoroff K., Hefter H., Jacinto J., Jost W.H., Molteni F., Stam H., et al. The profile of patients and current practice of treatment of upper limb muscle spasticity with botulinum toxin type A: An international survey. Int. J. Rehabil. Res. 2010;33:199–204. doi: 10.1097/MRR.0b013e328332f5e0.
    1. Mills P.B., Finlayson H., Sudol M., O’Connor R. Systematic review of adjunct therapies to improve outcomes following botuli-num toxin injection for treatment of limb spasticity. Clin. Rehabil. 2016;30:537–548. doi: 10.1177/0269215515593783.
    1. Brewer B.R., McDowell S.K., Worthen-Chaudhari L.C. Poststroke Upper Extremity Rehabilitation: A Review of Robotic Systems and Clinical Results. Top. Stroke Rehabil. 2007;14:22–44. doi: 10.1310/tsr1406-22.
    1. Gandolfi M., Valè N., Dimitrova E.K., Mazzoleni S., Battini E., Filippetti M., Picelli A., Santamato A., Gravina M., Saltuari L., et al. Effectiveness of Robot-Assisted Upper Limb Training on Spasticity, Function and Muscle Activity in Chronic Stroke Patients Treated With Botulinum Toxin: A Randomized Single-Blinded Controlled Trial. Front. Neurol. 2019;10:41. doi: 10.3389/fneur.2019.00041.
    1. Pennati G.V., Da Re C., Messineo I., Bonaiuti D. How could robotic training and botolinum toxin be combined in chronic post stroke upper limb spasticity? A pilot study. Eur. J. Phys. Rehabil. Med. 2014;51:381–387.
    1. Saita K., Morishita T., Hyakutake K., Fukuda H., Shiota E., Sankai Y., Inoue T. Combined therapy using botulinum toxin A and single-joint hybrid assistive limb for upper-limb disability due to spastic hemiplegia. J. Neurol. Sci. 2017;373:182–187. doi: 10.1016/j.jns.2016.12.056.
    1. Takebayashi T., Amano S., Hanada K., Umeji A., Takahashi K., Koyama T., Domen K. Therapeutic synergism in the treatment of post-stroke arm paresis utilizing botuli-num toxin, robotic therapy, and constraint-induced movement therapy. PM R. 2014;6:1054–1058. doi: 10.1016/j.pmrj.2014.04.014.
    1. Li S. Spasticity, Motor Recovery, and Neural Plasticity after Stroke. Front. Neurol. 2017;8:120. doi: 10.3389/fneur.2017.00120.
    1. Dong Y., Wu T., Hu X., Wang T. Efficacy and safety of botulinum toxin type A for upper limb spasticity after stroke or trau-matic brain injury: A systematic review with meta-analysis and trial sequential analysis. Eur. J. Phys. Rehabil. Med. 2017;53:256–267. doi: 10.23736/S1973-9087.16.04329-X.
    1. Elia A.E., Filippini G., Calandrella D., Albanese A. Botulinum neurotoxins for post-stroke spasticity in adults: A systematic re-view. Mov. Disord. 2009;24:801–812. doi: 10.1002/mds.22452.
    1. Boyd R.N., Pliatsios V., Starr R., Wolfe R., Graham H.K. Biomechanical transformation of the gastroc-soleus muscle with botuli-num toxin A in children with cerebral palsy. Dev. Med. Child. Neurol. 2000;42:32–41. doi: 10.1017/S0012162200000074.
    1. Gandolfi M., Formaggio E., Geroin C., Storti S.F., Boscolo Galazzo I., Bortolami M., Saltuari L., Picelli A., Waldner A., Manganotti P., et al. Quantification of Upper Limb Motor Recovery and EEG Power Changes after Ro-bot-Assisted Bilateral Arm Training in Chronic Stroke Patients: A Prospective Pilot Study. Neural Plast. 2018;2018:8105480. doi: 10.1155/2018/8105480.
    1. Bertani R., Melegari C., De Cola M.C., Bramanti A., Bramanti P., Calabrò R.S. Effects of robot-assisted upper limb rehabilitation in stroke patients: A systematic review with meta-analysis. Neurol. Sci. 2017;38:1561–1569. doi: 10.1007/s10072-017-2995-5.
    1. Veerbeek J.M., Langbroek-Amersfoort A.C., van Wegen E., Meskers C., Kwakkel G. Effects of Robot-Assisted Therapy for the Upper Limb After Stroke. Neurorehabilit. Neural Repair. 2016;31:107–121. doi: 10.1177/1545968316666957.
    1. Verdaasdonk E., Stassen L., Van Wijk R., Dankelman J. The influence of different training schedules on the learning of psy-chomotor skills for endoscopic surgery. Surg. Endosc. 2007;21:214–219. doi: 10.1007/s00464-005-0852-8.
    1. Mackay S., Morgan P., Datta V., Chang A., Darzi A. Practice distribution in procedural skills training. Surg. Endosc. Other Interv. Tech. 2002;16:957–961. doi: 10.1007/s00464-001-9132-4.
    1. Shea C.H., Lai Q., Black C., Park J.-H. Spacing practice sessions across days benefits the learning of motor skills. Hum. Mov. Sci. 2000;19:737–760. doi: 10.1016/S0167-9457(00)00021-X.
    1. Shebilske W.L., Goettl B.P., Corrington K., Day E.A. Interlesson spacing and task-related processing during complex skill acquisi-tion. J. Exp. Psychol. Appl. 1999;5:413–437. doi: 10.1037/1076-898X.5.4.413.
    1. Nadeau S.E., Davis S.E., Wu S.S., Dai Y., Richards L.G. A pilot randomized controlled trial of D-cycloserine and distributed prac-tice as adjuvants to constraint-induced movement therapy after stroke. Neurorehabil Neural Repair. 2014;28:885–895. doi: 10.1177/1545968314532032.
    1. Benjamin A.S., Tullis J. What makes distributed practice effective? Cogn. Psychol. 2010;61:228–247. doi: 10.1016/j.cogpsych.2010.05.004.
    1. Wang G., Grone B., Colas D., Appelbaum L., Mourrain P. Synaptic plasticity in sleep: Learning, homeostasis and disease. Trends Neurosci. 2011;34:452–463. doi: 10.1016/j.tins.2011.07.005.
    1. Wagner T.H., Lo A., Peduzzi P., Bravata D.M., Huang G.D., Krebs H.I., Ringer R.J., Federman D.G., Richards L.G., Haselkorn J.K., et al. An Economic Analysis of Robot-Assisted Therapy for Long-Term Upper-Limb Impairment After Stroke. Stroke. 2011;42:2630–2632. doi: 10.1161/STROKEAHA.110.606442.
    1. Donovan J., Radosevich D. A Meta-Analytic Review of the Distribution of Practice Effect: Now You See It, Now You Don’t. J. Appl. Psychol. 1999;84:795–805. doi: 10.1037/0021-9010.84.5.795.
    1. Simone P.M., Bell M.C., Cepeda N.J. Diminished but Not Forgotten: Effects of Aging on Magnitude of Spacing Effect Benefits. J. Gerontol. Ser. B. 2012;68:674–680. doi: 10.1093/geronb/gbs096.
    1. Foley N., Pereira S., Salter K., Meyer M., Andrew McClure J., Teasell R. Are recommendations regarding inpatient therapy intensity following acute stroke really evidence-based? Top. Stroke Rehabil. 2012;19:96–103. doi: 10.1310/tsr1902-96.
    1. Rose M.L., Pierce J.E., Scharp V.L., Off C.A., Babbitt E.M., Griffin-Musick J.R., Cherney L.R. Developments in the application of Intensive Comprehensive Aphasia Programs: An international survey of practice. Top. Stroke Rehabil. 2013;20:379–387. doi: 10.1310/tsr2005-379.
    1. Wallace A.C., Talelli P., Crook L., Austin D., Farrell R., Hoad D., O’Keeffe A.G., Marsden J.F., Fitzpatrick R., Greenwood R., et al. Exploratory Randomized Double-Blind Placebo-Controlled Trial of Botulinum Therapy on Grasp Release After Stroke (PrOMBiS) Neurorehabilit. Neural Repair. 2019;34:51–60. doi: 10.1177/1545968319887682.
    1. Picelli A., Santamato A., Chemello E., Cinone N., Cisari C., Gandolfi M., Ranieri M., Smania N., Baricich A. Adjuvant treatments associated with botulinum toxin injection for managing spas-ticity: An overview of the literature. Ann. Phys. Rehabil. Med. 2019;62:291–296. doi: 10.1016/j.rehab.2018.08.004.
    1. Dolly O. Synaptic Transmission: Inhibition of Neurotransmitter Release by Botulinum Toxins. Headache. J. Head Face Pain. 2003;43:16–24. doi: 10.1046/j.1526-4610.43.7s.4.x.
    1. Lo A.C., Guarino P.D., Richards L.G., Haselkorn J.K., Wittenberg G.F., Federman D.G., Ringer R.J., Wagner T., Krebs H.I., Volpe B., et al. Robot-Assisted Therapy for Long-Term Upper-Limb Impairment after Stroke. N. Engl. J. Med. 2010;362:1772–1783. doi: 10.1056/NEJMoa0911341.
    1. Rodgers H., Bosomworth H., I Krebs H., van Wijck F., Howel D., Wilson N., Aird L., Alvarado N., Andole S., Cohen D., et al. Robot assisted training for the upper limb after stroke (RATULS): A multicentre randomised controlled trial. Lancet. 2019;394:51–62. doi: 10.1016/S0140-6736(19)31055-4.
    1. Francis H.P., Wade D., Turner-Stokes L., Kingswell R.S., Dott C.S., A Coxon E. Does reducing spasticity translate into functional benefit? An exploratory meta-analysis. J. Neurol. Neurosurg. Psychiatry. 2004;75:1547–1551. doi: 10.1136/jnnp.2003.025551.
    1. Urbaniak G., Plous S. Research Randomizer; Version 4.0; Computer Software. Retrieved on 22 June 2013. [(accessed on 20 May 2021)]; Available online:
    1. Fugl Meyer A.R., Jaasko L., Leyman I. The post stroke hemiplegic patient. I. a method for evaluation of physical performance. Scand. J. Rehabil. Med. 1975;7:13–31.
    1. 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 Fugl-Meyer Test, Action Research Arm Test and Box and Block Test: A multicentre study. Clin. Rehabil. 2005;19:404–411. doi: 10.1191/0269215505cr832oa.
    1. Bohannon R.W., Smith M.B. Interrater Reliability of a Modified Ashworth Scale of Muscle Spasticity. Phys. Ther. 1987;67:206–207. doi: 10.1093/ptj/67.2.206.
    1. Pandyan A.D., Johnson G.R., Price C., Curless R.H., Barnes M.P., Rodgers H. A review of the properties and limitations of the Ashworth and modified Ashworth Scales as measures of spasticity. Clin. Rehabil. 1999;13:373–383. doi: 10.1191/026921599677595404.
    1. Uswatte G., Taub E., Stuss D., Winocur G., Robertson I. Cognitive Neurorehabilitation. Cambridge University Press; New York, NY, USA: 1999. Constraint-induced movement therapy: New approaches to outcome measurement in rehabilitation; pp. 215–229.
    1. Morris D.M., Uswatte G., Crago J.E., Cook E.W., Taub E. The reliability of the Wolf Motor Function Test for assessing upper ex-tremity function after stroke. Arch. Phys. Med. Rehabil. 2001;82:750–755. doi: 10.1053/apmr.2001.23183.
    1. Uswatte G., Taub E., Morris D., Light K., Thompson P.A. The Motor Activity Log-28: Assessing daily use of the hemiparetic arm after stroke. Neurology. 2006;67:1189–1194. doi: 10.1212/01.wnl.0000238164.90657.c2.
    1. Uswatte G., Taub E., Morris D., Vignolo M., McCulloch K. Reliability and Validity of the Upper-Extremity Motor Activity Log-14 for Measuring Real-World Arm Use. Stroke. 2005;36:2493–2496. doi: 10.1161/01.STR.0000185928.90848.2e.
    1. Van der Lee J., Beckerman H., Knol D., De Vet H., Bouter L. Clinimetric properties of the motor activity log for the assessment of arm use in hemiparetic patients. Stroke. 2004;35:1410–1414. doi: 10.1161/01.STR.0000126900.24964.7e.
    1. Jones F., Partridge C., Reid F. The Stroke Self-Efficacy Questionnaire: Measuring individual confidence in functional perfor-mance after stroke. J. Clin. Nurs. 2008;17:244–252. doi: 10.1111/j.1365-2702.2008.02333.x.

Source: PubMed

Sponsorzy i współpracownicy

Warunki medyczne

Interwencje lekowe

3
Subskrybuj