Novel evaluation of upper-limb motor performance after stroke based on normal reaching movement model

Journal of NeuroEngineering and Rehabilitation - Tập 20 - Trang 1-22 - 2023
James Hyungsup Moon1, Jongbum Kim2, Yeji Hwang1, Sungho Jang3, Jonghyun Kim1
1School of Mechanical Engineering, Sungkyunkwan University, Suwon-si, Republic of Korea
2Department of Robotics and Mechatronics Engineering, Daegu Gyeongbuk Institute of Science and Technology (DGIST), Daegu, Republic of Korea
3Department of Physical Medicine and Rehabilitation, College of Medicine, Yeungnam University, Daegu, Republic of Korea

Tóm tắt

Upper-limb rehabilitation robots provide repetitive reaching movement training to post-stroke patients. Beyond a pre-determined set of movements, a robot-aided training protocol requires optimization to account for the individuals’ unique motor characteristics. Therefore, an objective evaluation method should consider the pre-stroke motor performance of the affected arm to compare one’s performance relative to normalcy. However, no study has attempted to evaluate performance based on an individual’s normal performance. Herein, we present a novel method for evaluating upper limb motor performance after a stroke based on a normal reaching movement model. To represent the normal reaching performance of individuals, we opted for three candidate models: (1) Fitts’ law for the speed-accuracy relationship, (2) the Almanji model for the mouse-pointing task of cerebral palsy, and (3) our proposed model. We first obtained the kinematic data of healthy (n = 12) and post-stroke (n = 7) subjects with a robot to validate the model and evaluation method and conducted a pilot study with a group of post-stroke patients (n = 12) in a clinical setting. Using the models obtained from the reaching performance of the less-affected arm, we predicted the patients’ normal reaching performance to set the standard for evaluating the affected arm. We verified that the proposed normal reaching model identifies the reaching of all healthy (n = 12) and less-affected arm (n = 19; 16 of them showed an R2 > 0.7) but did not identify erroneous reaching of the affected arm. Furthermore, our evaluation method intuitively and visually demonstrated the unique motor characteristics of the affected arms. The proposed method can be used to evaluate an individual’s reaching characteristics based on an individuals normal reaching model. It has the potential to provide individualized training by prioritizing a set of reaching movements.

Tài liệu tham khảo

Wagner JM, Lang CE, Sahrmann SA, Edwards DF, Dromerick AW. Sensorimotor impairments and reaching performance in subjects with poststroke hemiparesis during the first few months of recovery. Phys Ther. 2007;87:751–65. Krebs HI, Krams M, Agrafiotis DK, DiBernardo A, Chavez JC, Littman GS, Yang E, Byttebier G, Dipietro L, Rykman A. Robotic measurement of arm movements after stroke establishes biomarkers of motor recovery. Stroke. 2014;45:200–4. Balasubramanian S, Colombo R, Sterpi I, Sanguineti V, Burdet E. Robotic assessment of upper limb motor function after stroke. Am J Phys Med Rehabil. 2012;91:S255–69. Wright ZA, Lazzaro E, Thielbar KO, Patton JL, Huang FC. Robot training with vector fields based on stroke survivors’ individual movement statistics. IEEE Trans Neural Syst Rehabil Eng. 2018;26:307–23. Krebs HI, Palazzolo JJ, Dipietro L, Ferraro M, Krol J, Rannekleiv K, Volpe BT, Hogan N. Rehabilitation robotics: performance-based progressive robot-assisted therapy. Auton Robot. 2003;15:7–20. Liao W-w, Wu C-y, Hsieh Y-w, Lin K-c, Chang W-y. Effects of robot-assisted upper limb rehabilitation on daily function and real-world arm activity in patients with chronic stroke: a randomized controlled trial. Clin Rehabil. 2012;26:111–20. Burgar CG, Lum PS, Scremin A, Garber SL, Van der Loos H, 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;48:445. Park H, Kim S, Winstein CJ, Gordon J, Schweighofer N. Short-duration and intensive training improves long-term reaching performance in individuals with chronic stroke. Neurorehabil Neural Repair. 2016;30:551–61. Huang FC, Patton JL. Movement distributions of stroke survivors exhibit distinct patterns that evolve with training. J Neuroeng Rehabil. 2016;13:23. Langhorne P, Bernhardt J, Kwakkel G. Stroke rehabilitation. The Lancet. 2011;377:1693–702. Oña E, Cano-de la Cuerda R, Sánchez-Herrera P, Balaguer C, Jardón A. A review of robotics in neurorehabilitation: towards an automated process for upper limb. J Healthc Eng. 2018;2018:1. Morris ME, Matyas TA, Bach TM, Goldie PA. Electrogoniometric feedback: its effect on genu recurvatum in stroke. Arch Phys Med Rehabil. 1992;73:1147–54. Azab M, Al-Jarrah M, Nazzal M, Maayah M, Abu Sammour M, Jamous M. Effectiveness of constraint-induced movement therapy (CIMT) as home-based therapy on Barthel Index in patients with chronic stroke. Top Stroke Rehabil. 2009;16:207–11. Bohannon RW. Physical rehabilitation in neurologic diseases. Curr Opin Neurol. 1993;6:765–72. Jeffers MS, Karthikeyan S, Gomez-Smith M, Gasinzigwa S, Achenbach J, Feiten A, Corbett D. Does stroke rehabilitation really matter? Part B: an algorithm for prescribing an effective intensity of rehabilitation. Neurorehabil Neural Repair. 2018;32:73–83. Semrau JA, Herter TM, Scott SH, Dukelow SP. Robotic identification of kinesthetic deficits after stroke. Stroke. 2013;44:3414–21. Kahn LE, Lum PS, Rymer WZ, Reinkensmeyer DJ. Robot-assisted movement training for the stroke-impaired arm: does it matter what the robot does? J Rehabil Res Dev. 2014;43:619–30. Murphy MA, Willén C, Sunnerhagen KS. Kinematic variables quantifying upper-extremity performance after stroke during reaching and drinking from a glass. Neurorehabil Neural Repair. 2011;25:71–80. Rosenthal O, Wing AM, Wyatt JL, Punt D, Miall RC. Mapping upper-limb motor performance after stroke-a novel method with utility for individualized motor training. J Neuroeng Rehabil. 2017;14:127. Rosenthal O, Wing AM, Wyatt JL, Punt D, Brownless B, Ko-Ko C, Miall RC. Boosting robot-assisted rehabilitation of stroke hemiparesis by individualized selection of upper limb movements–a pilot study. J Neuroeng Rehabil. 2019;16:42. Coderre AM, Zeid AA, Dukelow SP, Demmer MJ, Moore KD, Demers MJ, Bretzke H, Herter TM, Glasgow JI, Norman KE. Assessment of upper-limb sensorimotor function of subacute stroke patients using visually guided reaching. Neurorehabil Neural Repair. 2010;24:528–41. Stewart JC, Gordon J, Winstein CJ. Control of reach extent with the paretic and nonparetic arms after unilateral sensorimotor stroke: kinematic differences based on side of brain damage. Exp Brain Res. 2014;232:2407–19. Stewart JC, Gordon J, Winstein CJ. Control of reach extent with the paretic and nonparetic arms after unilateral sensorimotor stroke II: planning and adjustments to control movement distance. Exp Brain Res. 2014;232:3431–43. Fitts PM. The information capacity of the human motor system in controlling the amplitude of movement. J Exp Psychol. 1954;47:381. Schmidt RA, Zelaznik H, Hawkins B, Frank JS, Quinn JT Jr. Motor-output variability: a theory for the accuracy of rapid motor acts. Psychol Rev. 1979;86:415. Almanji A, Payne AR, Amor R, Davies TC. A nonlinear model for mouse pointing task movement time analysis based on both system and human effects. IEEE Trans Neural Syst Rehabil Eng. 2015;23:1003–11. Zimmerli L, Krewer C, Gassert R, Müller F, Riener R, Lünenburger L. Validation of a mechanism to balance exercise difficulty in robot-assisted upper-extremity rehabilitation after stroke. J Neuroeng Rehabil. 2012;9:6. Guiard Y. The problem of consistency in the design of Fitts’ law experiments: Consider either target distance and width or movement form and scale. In Proceedings of the sigchi conference on human factors in computing systems. 2009: 1809–1818. Giang C, Pirondini E, Kinany N, Pierella C, Panarese A, Coscia M, Miehlbradt J, Magnin C, Nicolo P, Guggisberg A. Motor improvement estimation and task adaptation for personalized robot-aided therapy: a feasibility study. Biomed Eng Online. 2020;19:1–25. Gori J, Rioul O, Guiard Y. Speed-accuracy tradeoff: a formal information-theoretic transmission scheme (fitts). ACM Trans Comput-Human Interact (TOCHI). 2018;25:1–33. Hsieh Y-w, Lin K-c, Wu C-y, Shih T-y, Li M-w, Chen C-l. Comparison of proximal versus distal upper-limb robotic rehabilitation on motor performance after stroke: a cluster controlled trial. Sci Rep. 2018;8:1–11. MacKenzie IS. A note on the information-theoretic basis for Fitts’ law. J Mot Behav. 1989;21:323–30. Liao JY, Kirsch RF. Characterizing and predicting submovements during human three-dimensional arm reaches. PLoS ONE. 2014;9: e103387. McCrea PH, Eng JJ. Consequences of increased neuromotor noise for reaching movements in persons with stroke. Exp Brain Res. 2005;162:70–7. Mottet D, van Dokkum LEH, Froger J, Gouaïch A, Laffont I. Trajectory formation principles are the same after mild or moderate stroke. PLoS ONE. 2017;12: e0173674. Choi Y, Qi F, Gordon J, Schweighofer N. Performance-based adaptive schedules enhance motor learning. J Mot Behav. 2008;40:273–80. Bellgrove MA, Phillips JG, Bradshaw JL, Gallucci RM. Response (re-) programming in aging: a kinematic analysis. J Gerontol A Biol Sci Med Sci. 1998;53:M222–7. Vasylenko O, Gorecka MM, Rodríguez-Aranda C. Manual dexterity in young and healthy older adults. 1. Age-and gender-related differences in unimanual and bimanual performance. Dev Psychobiol. 2018;60:407–27. Cooke JD, Brown SH, Cunningham DA. Kinematics of arm movements in elderly humans. Neurobiol Aging. 1989;10:159–65. Ketcham CJ, Seidler RD, Van Gemmert AW, Stelmach GE. Age-related kinematic differences as influenced by task difficulty, target size, and movement amplitude. J Gerontol B Psychol Sci Soc Sci. 2002;57:P54–64. Gelman A, Hwang J, Vehtari A. Understanding predictive information criteria for Bayesian models. Stat Comput. 2014;24:997–1016. Watanabe S, Opper M. Asymptotic equivalence of Bayes cross validation and widely applicable information criterion in singular learning theory. J Machine Learn Res 2010; 11. Aguilar VS, van de Gronde JJ, Lamoth CJ, Maurits NM, Roerdink JB. Assessing dynamic balance performance during exergaming based on speed and curvature of body movements. IEEE Trans Neural Syst Rehabil Eng. 2017;26:171–80. Gordon J, Ghilardi MF, Cooper SE, Ghez C. Accuracy of planar reaching movements. Exp Brain Res. 1994;99:112–30. Smyrnis N, Evdokimidis I, Constantinidis T, Kastrinakis G. Speed-accuracy trade-off in the performance of pointing movements in different directions in two-dimensional space. Exp Brain Res. 2000;134:21–31. Soukoreff RW, MacKenzie IS. Towards a standard for pointing device evaluation, perspectives on 27 years of Fitts’ law research in HCI. Int J Hum Comput Stud. 2004;61:751–89. Moore DS, Notz WI, Fligner MA. The basic practice of statistics. Macmillan Higher Education; 2015. Metrot J, Froger J, Hauret I, Mottet D, van Dokkum L, Laffont I. Motor recovery of the ipsilesional upper limb in subacute stroke. Arch Phys Med Rehabil. 2013;94:2283–90. 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;31:571–82. Caimmi M, Carda S, Giovanzana C, Maini ES, Sabatini AM, Smania N, Molteni F. Using kinematic analysis to evaluate constraint-induced movement therapy in chronic stroke patients. Neurorehabil Neural Repair. 2008;22:31–9. Park H, Schweighofer N. Nonlinear mixed-effects model reveals a distinction between learning and performance in intensive reach training post-stroke. J Neuroeng Rehabil. 2017;14:1–12. Wittmann F, Lambercy O, Gonzenbach RR, van Raai MA, Höver R, Held J, Starkey ML, Curt A, Luft A, Gassert R. Assessment-driven arm therapy at home using an IMU-based virtual reality system. In 2015 IEEE international conference on rehabilitation robotics (ICORR). IEEE; 2015: 707–712. Moore Z, Sifferman C, Tullis S, Ma M, Proffitt R, Skubic M. Depth Sensor-Based In-Home Daily Activity Recognition and Assessment System for Stroke Rehabilitation. In 2019 IEEE International Conference on Bioinformatics and Biomedicine (BIBM). IEEE; 2019: 1051–1056. Hwang Y, Lee S, Hong J, Kim J. A novel end-effector robot system enabling to monitor upper-extremity posture during robot-aided planar reaching movements. IEEE Robot Autom Lett. 2020;5:3035–41. Lee S, Lee Y-S, Kim J. Automated evaluation of upper-limb motor function impairment using Fugl-Meyer assessment. IEEE Trans Neural Syst Rehabil Eng. 2017;26:125–34.