Robot enhanced stroke therapy optimizes rehabilitation (RESTORE): a pilot study

Journal of NeuroEngineering and Rehabilitation - Tập 18 - Trang 1-16 - 2021
Alexa B. Keeling1,2, Mark Piitz2, Jennifer A. Semrau1,2,3, Michael D. Hill1,2, Stephen H. Scott4, Sean P. Dukelow1,2
1Hotchkiss Brain Institute, University of Calgary, Calgary, Canada
2Department of Clinical Neurosciences, University of Calgary, Calgary, Canada
3Department of Kinesiology and Applied Physiology, University of Delaware, Newark, USA
4Department of Biomedical and Molecular Sciences, Queen’s University, Kingston, Canada

Tóm tắt

Robotic rehabilitation after stroke provides the potential to increase and carefully control dosage of therapy. Only a small number of studies, however, have examined robotic therapy in the first few weeks post-stroke. In this study we designed robotic upper extremity therapy tasks for the bilateral Kinarm Exoskeleton Lab and piloted them in individuals with subacute stroke. Pilot testing was focused mainly on the feasibility of implementing these new tasks, although we recorded a number of standardized outcome measures before and after training. Our team developed 9 robotic therapy tasks to incorporate feedback, intensity, challenge, and subject engagement as well as addressing both unimanual and bimanual arm activities. Subacute stroke participants were assigned to a robotic therapy (N = 9) or control group (N = 10) in a matched-group manner. The robotic therapy group completed 1-h of robotic therapy per day for 10 days in addition to standard therapy. The control group participated only in standard of care therapy. Clinical and robotic assessments were completed prior to and following the intervention. Clinical assessments included the Fugl-Meyer Assessment of Upper Extremity (FMA UE), Action Research Arm Test (ARAT) and Functional Independence Measure (FIM). Robotic assessments of upper limb sensorimotor function included a Visually Guided Reaching task and an Arm Position Matching task, among others. Paired sample t-tests were used to compare initial and final robotic therapy scores as well as pre- and post-clinical and robotic assessments. Participants with subacute stroke (39.8 days post-stroke) completed the pilot study. Minimal adverse events occurred during the intervention and adding 1 h of robotic therapy was feasible. Clinical and robotic scores did not significantly differ between groups at baseline. Scores on the FMA UE, ARAT, FIM, and Visually Guided Reaching improved significantly in the robotic therapy group following completion of the robotic intervention. However, only FIM and Arm Position Match improved over the same time in the control group. The Kinarm therapy tasks have the potential to improve outcomes in subacute stroke. Future studies are necessary to quantify the benefits of this robot-based therapy in a larger cohort. Trial registration: ClinicalTrials.gov, NCT04201613, Registered 17 December 2019—Retrospectively Registered, https://clinicaltrials.gov/ct2/show/NCT04201613 .

Tài liệu tham khảo

Cotoi A, Anderson A, Vermeer J, Al-Ibrahim F, McIntyre A, Teasell R. Timing of motor rehabilitation after stroke: evidence from randomized controlled trials (RCTs). Int J Stroke. 2017;12(4S):50–1. Ward NS, Brander F, Kelly K. Intensive upper limb neurorehabilitation in chronic stroke: outcomes from the Queen Square programme. J Neurol Neurosurg Psychiatry. 2019;90:498–506. Daly JJ, McCabe JP, Holcomb J, Monkiewicz M, Gansen J, Pundik S. Long-dose intensive therapy is necessary for strong, clinically significant, upper limb functional gains and retained gains in severe/moderate chronic stroke. Neurorehabil Neural Repair. 2019;33(7):523–37. Kunkel A, Kopp B, Müller G, Villringer K, Villringer A, Taub E, et al. Constraint-induced movement therapy for motor recovery in chronic stroke patients. Arch Phys Med Rehabil. 1999;80(6):624–8. Bernhardt J, Hayward KS, Kwakkel G, Ward NS, Wolf SL, Borschmann K, et al. Agreed definitions and a shared vision for new standards in stroke recovery research: The Stroke Recovery and Rehabilitation Roundtable taskforce. Int J Stroke. 2017;12(5):444–50. Masiero S, Poli P, Rosati G, Zanotto D, Iosa M, Paolucci S, et al. The value of robotic systems in stroke rehabilitation. Expert Rev Med Devices. 2014;11(2):187–98. Han C, Wang Q, Meng P, Qi M. Effects of intensity of arm training on hemiplegic upper extremity motor recovery in stroke patients: a randomized controlled trial. Clin Rehabil. 2013;27(1):75–81. Winstein CJ, Rose DK, Tan SM, Lewthwaite R, Chui HC, Azen SP. A randomized controlled comparison of upper-extremity rehabilitation strategies in acute stroke: a pilot study of immediate and long-term outcomes. Arch Phys Med Rehabil. 2004;85(4):620–8. Kwakkel G, Wagenaar RC, Twisk JWR, Lankhorst GJ, Koetsier JC. Intensity of leg and arm training after primary middle-cerebral-artery stroke: a randomised trial. Lancet. 1999;354(9174):191–6. Aisen ML, Krebs HI, Hogan N, McDowell F, Volpe BT. The effect of robot-assisted therapy and rehabilitation training on motor recovery following stroke. Arch Neurol. 1997;54(4):443–6. Krebs HI, Hogan N, Aisen ML, Volpe B. Robot-aided neurorehabilitation. IEEE Trans Rehabil Eng. 1997;6(1):75–87. Volpe BT, Krebs HI, Hogan N, Edelsteinn L, Diels CM, Aisen ML. Robot training enhanced motor outcome in patients with stroke maintained over 3 years. Neurology. 1999;53(8):1874–6. Masiero S, Armani M, Ferlini G, Rosati G, Rossi A. Randomized trial of a robotic assistive device for the upper extremity during early inpatient stroke rehabilitation. Neurorehabil Neural Repair. 2014;28(4):377–86. Duret C, Gorsmarie A, Krebs HI. Robot-assisted therapy in upper extremity hemiparesis: overview of an evidence-based approach. Front Neurol. 2019;10:412. Fasoli SE, Krebs HI, Hogan N. Robotic technology and stroke rehabilitation: translating research into practice. Top Stroke Rehabil. 2004;11(4):11–9. Hogan N, Krebs HI. Interactive robots for neuro-rehabilitation. Restor Neurol Neurosci. 2004;22:349–58. Veerbeek JM, Langbroek-Amersfoort AC, van Wegen EEH, Meskers CGM, Kwakkel G. Effects of robot-assisted therapy for the upper limb after stroke: a systematic review and meta-analysis. Neurorehabil Neural Repair. 2017;31(2):107–21. Scott SH, Dukelow SP. Potential of robots as next-generation technology for clinical assessment of neurological disorders and upper-limb therapy. J Rehabil Res Dev. 2011;48(4):335–54. Maciejasz P, Eschweiler J, Gerlach-Hahn K, Jansen-Troy A, Leonhardt S. A survey on robotic devices for upper limb rehabilitation. J Neuroeng Rehabil. 2014;11:3. Scott SH. Apparatus for measuring and perturbing shoulder and elbow joint positions and torques during reaching. J Neurosci. 1999;89:119–27. Bourke TC, Lowrey CR, Dukelow SP, Bagg SD, Norman KE, Scott SH. A robot-based behavioural task to quantify impairments in rapid motor decisions and actions after stroke. J Neuroeng Rehabil. 2016;13:91. Coderre AM, Abou Zeid A, Dukelow SP, Demmer MJ, Moore KD, Demers MJ, et al. Assessment of upper-limb sensorimotor function of subacute stroke patients using visually guided reaching. Neurorehabil Neural Repair. 2010;24:528–41. Dukelow SP, Herter TM, Moore KD, Demers MJ, Glasgow JI, Bagg SD, et al. Quantitative assessment of limb position sense following stroke. Neurorehabil Neural Repair. 2010;24(2):178–87. Lowrey CR, Jackson CPT, Bagg SD, Dukelow SP, Scott SH. A novel robotic task for assessing impairments in bimanual coordination post-stroke. Int J Phys Rehabil. 2014. https://doi.org/10.4172/2329-9096.S3-002. Semrau JA, Herter TM, Scott SH, Dukelow SP. Robotic identification of kinesthetic deficits after stroke. Stroke. 2013;44:3414–21. Tyryshkin K, Coderre A, Glasgow JI, Herter TM, Bagg SD, Dukelow SP, et al. A robotic object hitting task to quantify sensorimotor impairments in participants with stroke. J Neuroeng Rehabil. 2014;11(1):47. Simmatis L, Krett J, Scott SH, Jin AY. Robotic exoskeleton assessment of transient ischemic attack. PLoS ONE. 2017;12(12):e0188786. Mang CS, Whitten TA, Cosh MS, Scott SH, Wiley JP, Debert CT, et al. Robotic assessment of motor, sensory, and cognitive function in acute sport-related concussion and recovery. J Neurotrauma. 2019;36(2):308–21. Logan LM, Semrau JA, Debert CT, Kenzie JM, Scott SH, Dukelow SP. Using robotics to quantify impairments in sensorimotor ability, visuospatial attention, working memory, and executive function after traumatic brain injury. J Head Trauma Rehabil. 2018;33(4):61–73. Herter TM, Scott SH, Dukelow SP. Systematic changes in position sense accompany normal aging across adulthood. J Neuroeng Rehabil. 2014;11:43. Semrau JA, Herter TM, Kenzie JM, Findlater SE, Scott SH, Dukelow SP. Robotic characterization of ipsilesional motor function in subacute stroke. Neurorehabil Neural Repair. 2017;31(6):571–82. Kantak S, Jax S, Wittenberg G. Bimanual coordination: a missing piece of arm rehabilitation after stroke. Res Neurol Neurosci. 2017;35:347–64. Sainburg RL, Good D, Przybyla A. Bilateral synergy: a framework for post-stroke rehabilitation. J Neurol Transl Neurosci. 2013;1(3):1025. van Vliet PM, Wulf G. Extrinsic feedback for motor learning after stroke: what is the evidence? Disabil Rehabil. 2006;28(13–14):831–40. Sigrist R, Rauter G, Riener R, Wolf P. Augmented visual, auditory, haptic, and multimodal feedback in motor learning: a review. Psychon Bull Rev. 2013;20:21–53. Piron L, Turolla A, Agostini M, Succconi CS, Ventura L, Tonin P, et al. Motor learning principles for rehabilitation: a pilot randomized controlled study in poststroke patients. Neurorehabil Neural Repair. 2010;24(6):501–8. Teasell RW, Foley NC, Salter KL, Jutai JW. A blueprint for transforming stroke rehabilitation care in Canada: the case for change. Arch Phys Med Rehabil. 2008;89:575–8. Harris JE, Eng JJ, Miller WC, Dawson AS. A self-administered graded repetitive arm supplementary program (GRASP) improves arm function during inpatient stroke rehabilitation. Stroke. 2009;40:2123–8. Guadagnoli MA, Lee TD. Challenge point: a framework for conceptualizing the effects of various practice conditions in motor learning. J Mot Behav. 2004;36(2):212–24. Teasell R, Salbach N, Foley N, Mountain A, Cameron J, de Jong A, et al. Canadian stroke best practice recommendations: rehabilitation, recovery and community participation following stroke. Part One: Rehabilitation and Recovery following Stroke; 6th Edition Update 2019. Int J Stroke. 2020. https://doi.org/10.1177/1747493019897843. Putrino D, Zanders H, Hamilton T, Rykman A, Lee P, Edwards DJ. Patient engagement is related to impairment reduction during digital game-based therapy in stroke. Games Health J. 2017;6(5):295–302. Metzler MJ, Lindsay S, Shi J, Reglin P, Bagg A, Dukelow S. Intensity in tertiary stroke rehabilitation: a quality assurance study. Stroke. 2012;43:115–62. 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 Rehabil Med. 1975;7:13–31. Van der Lee JH, De Groot V, Beckerman H, Wagenaar RC, Lankhorst GJ, Bouter LM. The intra- and interrater reliability of the action research arm test: a practical test of upper extremity in patients with stroke. Arch Phys Med Rehabil. 2001;82:14–9. Keith RA, Granger CV, Hamilton BB, Sherwin FS. The functional independence measure: a new tool for rehabilitation. Adv Clin Rehabil. 1987;1:6–18. Kinarm User Guides and Documentation. https://kinarm.com/support/user-guides-documentation/. Accessed 24 June 2020. IBM Corp. Released 2019. IBM SPSS Statistics for Windows, Version 26.0. Armonk, NY: IBM Corp. Dromerick AW, Lang CE, Birkenmeier RL, Wagner JM, Miller JP, Videen TO, Powers WJ, Wolf SL, Edwards DF. Very early constraint-induced movement during stroke rehabilitation (VECTORS): a single-center RCT. Neurology. 2009;73(3):195–201. Burgar CG, Lum PS, Scremin AME, Garber SL, Van der Loos HFM, Kenney D, Shor P. Robot-assisted upper-limb therapy in acute rehabilitation setting following stroke: Department of Veterans Affairs multisite clinical trial. J Rehabil Res Dev. 2011;48(4):445–58. Mehrholz J, Pohl M, Platz T, Kugler J, Elsner B. Electromechanical and robot-assisted arm training for improving activities of daily living, arm function, and arm muscle strength after stroke. Cochrane Database Syst Rev. 2018. https://doi.org/10.1002/14651858.CD006876.pub5. Kwakkel G, Kollen BJ, Krebs HI. Effects of robot-assisted therapy on upper limb recovery after stroke: a systematic review. Neurorehabil Neural Repair. 2008;22(2):111–21. Lo AC, Guarino PD, Richards LG, Haselkorn JK, Wittenberg GF, Federman DG, et al. Robot-assisted therapy for long-term upper-limb impairment after stroke. N Engl J Med. 2010;362(19):1772–83. Pila O, Duret C, Laborne FX, Gracies JM, Bayle N, Hutin M. Pattern of improvement in upper limb pointing task kinematics after a 3-month training program with robotic assistance in stroke. J Neuroeng Rehabil. 2017;14:105. Massie CL, Du Y, Conroy SS, Krebs HI, Wittenberg GF, Bever CT, et al. A clinically relevant method of analyzing continuous change in robotic upper extremity chronic stroke rehabilitation. Neurorehabil Neural Repair. 2016;30(8):703–12. Goffredo M, Mazzoleni S, Gison A, Infarinato F, Pournajaf S, Galafate D, et al. Kinematic parameters for tracking patient progress during upper limb robot-assisted rehabilitation: an observational study on subacute stroke subjects. Appl Bionics Biomech. 2019. https://doi.org/10.1155/2019/4251089. Rodgers H, Bosomworth H, Krebs HI, van Wijck F, Howel D, Wilson N, et al. Robot assisted training for the upper limb after stroke (RATULS): a multicentre randomised controlled trial. Lancet. 2019;394(10192):51–62. Sanguineti V, Casadio M, Vergaro E, Squeri V, Giannoni P, Morasso PG. Robot therapy for stroke survivors: proprioceptive training and regulation of assistance. Advanced technologies in rehabilitation. In: Gaggioli A, editor. Robots, wearable systems and brain–computer interfaces. Amsterdam: IOS Press; 2009. Vergaro E, Casadio M, Squeri V, Giannoni P, Morasso P, Sanguineti V. Self-adaptive robot training of stroke survivors for continuous tracking movements. J Neuroeng Rehabil. 2010;7:13. Squeri V, Cassadio M, Vergaro E, Giannoni P, Morasso P, Sanguineti V. Bilateral robot therapy based on haptics and reinforcement learning: feasibility study of a new concept for treatment of patients after stroke. J Rehabil Med. 2009;41:961–5. Simkins M, Kim H, Abrams G, Byl N, Rosen J. Robotic unilateral and bilateral upper-limb movement training for stroke survivors afflicted by chronic hemiparesis. IEEE Int Conf Rehabil Robot. 2013. https://doi.org/10.1109/ICORR.2013.6650506. Burgar CG, Lum PS, Shor PC, Van der Loos HFM. Development of robots for rehabilitation therapy: the Palo Alto VA/Stanford experience. J Rehabil Res Dev. 2000;37(6):663–73. Lum PS, Burgar CG, Van der Loos M, Shor PC, Majmundar M, Yap R. MIME robotic device for upper-limb neurorehabilitation in subacute stroke subjects: a follow-up study. J Rehabil Res Dev. 2006;43(5):631–42. Hesse S, Schulte-Tigges G, Konrad M, Bardeleben A, Wener C. Robot-assisted arm trainer for the passive and active practice of bilateral forearm and wrist movements in hemiparetic subjects. Arch Phys Med Rehabil. 2003;84:915–20. Hsieh Y, Wu C, Wang W, Lin K, Chang K, Chen C, et al. Bilateral robotic priming before task-orientated approach in subacute stroke rehabilitation: a pilot randomized controlled trial. Clin Rehabil. 2016;31(2):225–33. Hung C, Hsieh Y, Wu C, Lin K, Lin J, Yeh L. Comparative assessment of two robot-assisted therapies for the upper extremity in people with chronic stroke. Am J Occup Ther. 2019;73(1):7301205010. Yang C, Lin K, Chen H, Wu C, Chen C. Pilot comparative study of unilateral and bilateral robot-assisted training on upper-extremity performance in patients with stroke. Am J Occup Ther. 2012;66:198–206. Hung C, Lin K, Chang W, Huang W, Chang Y, Chen C, et al. Unilateral vs bilateral hybrid approaches for upper limb rehabilitation in chronic stroke: a randomized controlled trial. Arch Phys Med Rehabil. 2019;100(12):2225–32. Wu C, Yang C, Chen M, Lin K, Wu L. Unilateral versus bilateral robot-assisted rehabilitation on arm-trunk control and functions post stroke: randomized controlled trial. J Neuroeng Rehabil. 2013;10(1):35. Toth A, Fazekas G, Arz G, Jurak M, Horvath M. Passive robotic movement therapy of the spastic hemiparetic arm with REHAROB: report of the first clinical test and the follow-up system improvement. ICORR. 2005:127–30. Nef T, Mihelj M, Riener R. ARMin: a robot for patient-cooperative arm therapy. Med Bio Eng Comput. 2007;45:887–900. Rosati G, Gallina P, Masiero S. Design, implementation and clinical tests of a wire-based robot for neurorehabilitation. IEEE Trans Neural Syst Rehabil Eng. 2007;15(4):560–9. Nef T, Quinter G, Müller R, Riener R. Effects of arm training with the robotic device ARMin I in chronic stroke: three single cases. Neurodegener Dis. 2010;27(3):289–94. Kenzie JM, Smerau JA, Hill MD, Scott SH, Dukelow SP. A composite robotic-based measure of upper-limb proprioception. J Neuroeng Rehabil. 2017;14:114. Findlater SE, Dukelow SP. Upper extremity proprioception after stroke: bridging the gap between neuroscience and rehabilitation. J Mot Behav. 2017;49:27–34. Carey LM, Matyas TA, Oke LE. Sensory loss in stroke patients: effective training of tactile and proprioceptive discrimination. Arch Phys Med Rehabil. 1993;74:602–11. Kim G, Lim S, Kim H, Lee B, Seo S, Cho K, et al. Is robot-assisted therapy effective in upper extremity recovery in early stage stroke? A systematic literature review. J Phys Ther Sci. 2017;29(6):1108–12. Lee SH, Park G, Cho DY, Kim HY, Lee J, Kim S, et al. Comparisons between end-effector and exoskeleton rehabilitation robotics regarding upper extremity function among chronic stroke patients with moderate-to-severe upper limb impairment. Sci Rep. 2020;10(1):1806. Erol D, Mallapragada V, Sarkar N, Uswatte G, Taub E. Autonomously adapting robotic assistance for rehabilitation therapy. IEEE/RAS-EMBS International Conference on Biomedical Robotics and Biomechatronics, 2006;567–72. Borghese NA, Pirovano M, Lanzi PL, Wüest S, de Bruin ED. Computational intelligence and game design for effective at-home stroke rehabilitation. Games Health J. 2013;2(2):81–8.