Robotic Kinematic measures of the arm in chronic Stroke: part 1 - Motor Recovery patterns from tDCS preceding intensive training

Caio B Moretti, Dylan J Edwards, Taya Hamilton, Mar Cortes, Avrielle Rykman Peltz, Johanna L Chang, Alexandre C B Delbem, Bruce T Volpe, Hermano I Krebs, Caio B Moretti, Dylan J Edwards, Taya Hamilton, Mar Cortes, Avrielle Rykman Peltz, Johanna L Chang, Alexandre C B Delbem, Bruce T Volpe, Hermano I Krebs

Abstract

Background: Effectiveness of robotic therapy and transcranial direct current stimulation is conventionally assessed with clinical measures. Robotic metrics may be more objective and sensitive for measuring the efficacy of interventions on stroke survivor's motor recovery. This study investigated if robotic metrics detect a difference in outcomes, not seen in clinical measures, in a study of transcranial direct current stimulation (tDCS) preceding robotic therapy. Impact of impairment severity on intervention response was also analyzed to explore optimization of outcomes by targeting patient sub-groups.

Methods: This 2020 study analyzed data from a double-blind, sham-controlled, randomized multi-center trial conducted from 2012 to 2016, including a six-month follow-up. 82 volunteers with single chronic ischemic stroke and right hemiparesis received anodal tDCS or sham stimulation, prior to robotic therapy. Robotic therapy involved 1024 repetitions, alternating shoulder-elbow and wrist robots, for a total of 36 sessions. Shoulder-elbow and wrist kinematic and kinetic metrics were collected at admission, discharge, and follow-up.

Results: No difference was detected between the tDCS or sham stimulation groups in the analysis of robotic shoulder-elbow or wrist metrics. Significant improvements in all metrics were found for the combined group analysis. Novel wrist data showed smoothness significantly improved (P < ·001) while submovement number trended down, overlap increased, and interpeak interval decreased. Post-hoc analysis showed only patients with severe impairment demonstrated a significant difference in kinematics, greater for patients receiving sham stimulation.

Conclusions: Robotic data confirmed results of clinical measures, showing intensive robotic therapy is beneficial, but no additional gain from tDCS. Patients with severe impairment did not benefit from the combined intervention. Wrist submovement characteristics showed a delayed pattern of motor recovery compared to the shoulder-elbow, relevant to intensive intervention-related recovery of upper extremity function in chronic stroke.

Trial registration: http://www.clinicaltrials.gov . Actual study start date September 2012. First registered on 15 November 2012. Retrospectively registered. Unique identifiers: NCT01726673 and NCT03562663 .

Keywords: Kinematics; Outcome measures; Robotics; Stroke; tDCS.

Conflict of interest statement

TH reports personal fees from Bionik Laboratories, outside the submitted work; In addition, TH has a patent “An apparatus and/or method for positioning a hand for rehabilitation” pending to Bionik Laboratories. HIK declares he was the founder of Interactive Motion Technologies and Chairman of the Board (1998–2016). He successfully sold Interactive Motion Technologies on April 2016 to Bionik Laboratories, where he served as Chief Science Officer and Board Member until July 2017. HIK was the founder of 4Motion Robotics. HIK has patents; Interactive Robotic Therapist; US Patent 5,466,213; 1995; Massachusetts Institute of Technology issued, and a patent Wrist And Upper Extremity Motion; US Patent No. 7,618,381; 2009; Massachusetts Institute of Technology licensed to Bionik Laboratories.

© 2021. The Author(s).

Figures

Fig. 1
Fig. 1
CONSORT flow diagram
Fig. 2
Fig. 2
Combined RobottDCS and RobotSham mean and standard error of kinematic and kinetic outcome metrics for the shoulder-elbow (S/E.) Significant changes (P < .0167) between admission (ad), discharge (dc), and follow-up (fu.) are marked with an * Note: The bar-graphs in white background represent the unconstrained trained reaching macro-metrics, the lightest grey shading background represents the unconstrained trained reaching micro-metrics (sm= sub-movement), the slightly darker grey represents the unconstrained untrained circle metrics, and the darkest grey represents the reaching against resistance, isometric stabilization, and kinetic metrics (respectively, see Additional file 1 for further details on the metrics.)
Fig. 3
Fig. 3
Combined RobottDCS and RobotSham mean and standard error of kinematic and kinetic outcome metrics for the wrist. Significant changes (P < .0167) between admission (ad), discharge (dc), and follow-up (fu.) are marked with an * Note: The bar-graphs in white background represent the unconstrained trained pointing macro-metrics, the lightest grey shading background represents the unconstrained trained pointing micro-metrics (sm= sub-movement), and the darkest grey represents the reaching against resistance, isometric stabilization, and kinetic metrics (respectively, see Additional file 1 for further details on the metrics.)
Fig. 4
Fig. 4
Improvements in joint independence over time. To afford direct comparison with Figs. 4 and 5 of (Dipietro et al., 2007), here we employed the same non-corrected significance at P < .05 level. Individual values of joint independence metric (a and b for all patients), sorted by their performance at admission (squares) in comparison to discharge (diamonds), and follow-up (circles). A lower number indicates greater/improving joint independence. Figures c and d represent changes in the joint independence metric, where filled circles indicate significance at discharge (c) and follow-up (d)

References

    1. Agrafiotis DK, Yang E, Littman GS, Byttebier G, Dipietro L, DiBernardo A, et al. Accurate prediction of clinical stroke scales and improved biomarkers of motor impairment from robotic measurements. PLoS One. 2021;16(1):e0245874. 10.1371/journal.pone.0245874.
    1. Bernhardt J, Borschmann KN, Kwakkel G, Burridge JH, Eng JJ, Walker MF, et al. Setting the scene for the second Stroke Recovery and rehabilitation roundtable. Int J Stroke. 2019;14(5):450–6. 10.1177/1747493019851287.
    1. Bolognini N, Vallar G, Casati C, Latif LA, El-Nazer R, Williams J, et al. Neurophysiological and behavioral effects of tDCS combined with constraint-induced movement therapy in poststroke patients. Neurorehabil Neural Repair. 2011;25(9):819–829. doi: 10.1177/1545968311411056.
    1. Bosecker C, Dipietro L, Volpe B, Krebs HI. Kinematic robot-based evaluation scales and clinical counterparts to measure upper limb motor performance in patients with chronic stroke. Neurorehabil Neural Repair. 2010;24(1):62–69. doi: 10.1177/1545968309343214.
    1. Colombo R, Pisano F, Micera S, Mazzone A, Delconte C, Carrozza MC, et al. Robotic techniques for upper limb evaluation and rehabilitation of stroke patients. IEEE Trans Neural Syst Rehabil Eng. 2005;13(3):311–324. doi: 10.1109/TNSRE.2005.848352.
    1. Coupar F, Pollock A, Rowe P, Weir C, Langhorne P. Predictors of upper limb recovery after stroke: A systematic review and meta-analysis. Clin Rehabil. 2012;26(4):291–313. doi: 10.1177/0269215511420305.
    1. Dipietro L, Krebs HI, Fasoli SE, Volpe BT, Stein J, Bever C, et al. Changing Motor Synergies in Chronic Stroke. J Neurophysiol. 2007;98(2):757–768. doi: 10.1152/jn.01295.2006.
    1. Dipietro L, Krebs HI, Volpe BT, Stein J, Bever C, Mernoff ST, et al. Learning, Not Adaptation, Characterizes Stroke Motor Recovery: Evidence From Kinematic Changes Induced by Robot-Assisted Therapy in Trained and Untrained Task in the Same Workspace. IEEE Trans Neural Syst Rehabil Eng. 2012;20(1):48–57. doi: 10.1109/TNSRE.2011.2175008.
    1. Dukelow SP. The potential power of robotics for upper extremity stroke rehabilitation. Int J Stroke. 2017;12(1):7–8. doi: 10.1177/1747493016654483.
    1. Dukelow SP, Herter TM, Bagg SD, Scott SH. The independence of deficits in position sense and visually guided reaching following stroke. J Neuroeng Rehabil. 2012;9(1):72. doi: 10.1186/1743-0003-9-72.
    1. Edwards DJ, Cortes M, Rykman-Peltz A, Chang J, Elder J, Thickbroom G, et al. Clinical improvement with intensive robot-assisted arm training in chronic stroke is unchanged by supplementary tDCS. Restor Neurol Neurosci. 2019;37(2):167–180.
    1. Flash T, Hogan N. The coordination of arm movements: an experimentally confirmed mathematical model. J Neurosci. 1985;5(7):1688–1703. doi: 10.1523/JNEUROSCI.05-07-01688.1985.
    1. Giacobbe V, Krebs HI, Volpe BT, Pascual-Leone A, Rykman A, Zeiarati G, et al. Transcranial direct current stimulation (tDCS) and robotic practice in chronic stroke: the dimension of timing. NeuroRehabilitation. 2013;33(1):49–56. 10.3233/NRE-130927.
    1. Hsieh YW, Lin KC, Wu CY, Shih TY, Li MW, Chen CL. Comparison of proximal versus distal upper-limb robotic rehabilitation on motor performance after stroke: A cluster controlled trial. Sci Rep. 2018;8(1):2091. doi: 10.1038/s41598-018-20330-3.
    1. Kim B, Winstein C. Can Neurological Biomarkers of Brain Impairment Be Used to Predict Poststroke Motor Recovery? A Systematic Review. 31, Neurorehabil Neural Repair. SAGE Publications Inc.; 2017. 3–24.
    1. Krause B, Kadosh RC. Not all brains are created equal: the relevance of individual differences in responsiveness to transcranial electrical stimulation. 8, 25, Front Syst Neurosci. Frontiers Media SA; 2014.
    1. Krebs HI, Aisen ML, Volpe BT, Hogan N. Quantization of continuous arm movements in humans with brain injury. Proc Natl Acad Sci U S A. 1999;96(8):4645–4649. doi: 10.1073/pnas.96.8.4645.
    1. Krebs HI, Krams M, Agrafiotis DK, DiBernardo A, Chavez JC, Littman GS, et al. Robotic Measurement of Arm Movements After Stroke Establishes Biomarkers of Motor Recovery. Stroke. 2014;45(1):200–204. doi: 10.1161/STROKEAHA.113.002296.
    1. Krebs HI, Volpe BT, Ferraro M, Fasoli S, Palazzolo J, Rohrer B, et al. Robot-Aided Neurorehabilitation: From Evidence-Based to Science-Based Rehabilitation. Top Stroke Rehabil. 2002;8(4):54–70. doi: 10.1310/6177-QDJJ-56DU-0NW0.
    1. Lai SM, Studenski S, Duncan PW, Perera S. Persisting consequences of stroke measured by the stroke impact scale. Stroke. 2002;33(7):1840–1844. doi: 10.1161/01.STR.0000019289.15440.F2.
    1. Lawrence ES, Coshall C, Dundas R, Stewart J, Rudd AG, Howard R, et al. Estimates of the prevalence of acute stroke impairments and disability in a multiethnic population. Stroke. 2001;32(6):1279–1284. doi: 10.1161/01.STR.32.6.1279.
    1. Lefebvre S, Liew SL. Anatomical parameters of tDCS to modulate the motor system after stroke: A review. Front Neurol. Frontiers Media S.A.; 2017, 8:29.
    1. 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):1772–1783. doi: 10.1056/NEJMoa0911341.
    1. Lohse KR, Lang CE, Boyd LA. Is more better? Using metadata to explore dose-response relationships in stroke rehabilitation. Stroke. 2014;45(7):2053–2058. doi: 10.1161/STROKEAHA.114.004695.
    1. Mazzoleni S, Sale P, Tiboni M, Franceschini M, Carrozza MC, Posteraro F. Upper limb robot-assisted therapy in chronic and subacute stroke patients: A kinematic analysis. Am J Phys Med Rehabil. 2013;92(10 SUPPL. 1):e26–e37. doi: 10.1097/PHM.0b013e3182a1e852.
    1. Milot MH, Spencer SJ, Chan V, Allington JP, Klein J, Chou C, et al. Corticospinal excitability as a predictor of functional gains at the affected upper limb following robotic training in chronic stroke survivors. Neurorehabil Neural Repair. 2014 Nov 8;28(9):819–27. 10.1177/1545968314527351.
    1. Moretti CB, Delbem AC, Krebs HI. Human-Robot Interaction: Kinematic and Kinetic Data Analysis Framework. In: 2020 8th IEEE RAS/EMBS International Conference for Biomedical Robotics and Biomechatronics (BioRob); 2020. p. 235–9. 10.1109/BioRob49111.2020.9224415.
    1. Ovbiagele B, Goldstein LB, Higashida RT, Howard VJ, Johnston SC, Khavjou OA, et al. Forecasting the future of stroke in the United States: a policy statement from the American heart association and American stroke association. Stroke. 2013;44(8):2361–75. 10.1161/STR.0b013e31829734f2.
    1. Reinkensmeyer DJ, Emken JL, Cramer SC. Robotics, motor learning, and neurologic recovery. Annu Rev Biomed Eng. 2004;6:497–525. doi: 10.1146/annurev.bioeng.6.040803.140223.
    1. Rohrer B, Fasoli S, Krebs HI, Hughes R, Volpe B, Frontera WR, et al. Movement Smoothness Changes during Stroke Recovery. J Neurosci. 2002;22(18):8297–8304. doi: 10.1523/JNEUROSCI.22-18-08297.2002.
    1. Rohrer B, Fasoli S, Krebs HI, Volpe B, Frontera WR, Stein J, et al. Submovements grow larger, fewer, and more blended during stroke recovery. Motor Control. 2004;8(4):472–483. doi: 10.1123/mcj.8.4.472.
    1. 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):335–354. doi: 10.1682/JRRD.2010.04.0057.
    1. Semrau JA, Herter TM, Scott SH, Dukelow SP. Robotic identification of kinesthetic deficits after stroke. Stroke. 2013;44(12):3414–3421. doi: 10.1161/STROKEAHA.113.002058.
    1. Straudi S, Fregni F, Martinuzzi C, Pavarelli C, Salvioli S, Basaglia N. tDCS and robotics on Upper Limb Stroke rehabilitation: effect modification by Stroke duration and type of Stroke. Biomed Res Int. 2016;2016:1–8. doi: 10.1155/2016/5068127.
    1. World Health Organization . World Health Statistics 2012. World Health Organization; 2012. p. 180.

Source: PubMed

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