Performance-Based Robotic Training in Individuals with Subacute Stroke: Differences between Responders and Non-Responders
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design and Sample
2.2. Interventions
2.3. Data Measurement
- -
- velocity: defined as the distance traveled divided by the movement time (in cm/s);
- -
- distance: defined as the distance between the center of the pointing task and the orthogonal projection on the axis (center-target) of the position of the end-effector at the end of the movement (in cm);
- -
- smoothness: defined as the number of peaks in the velocity profile;
- -
- accuracy: defined as the root mean square error from the straight line (in cm).
2.4. Statistical Analysis
3. Results
3.1. Baseline Characteristics
3.2. Clinical Outcomes
3.3. Kinematic Outcomes
3.4. Robot-Based Outcomes with All Physical Modalities Pooled
3.5. Robot-Based Outcomes for Each Physical Modality
4. Discussion
4.1. Factors Influencing Favorable Motor Outcomes
4.2. Toward a Meaningful and Multidimensional Description of Administered Treatment Dose
4.3. Repeated Movements and Difficulty: Synergy and Misunderstanding?
4.4. Robotic Assistance for Individuals with Severe Motor Impairment: Facilitator or Deleterious to Motor Recovery?
4.5. Limitations
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Langhorne, P.; Coupar, F.; Pollock, A. Motor Recovery after Stroke: A Systematic Review. Lancet Neurol. 2009, 8, 741–754. [Google Scholar] [CrossRef] [PubMed]
- Dromerick, A.W.; Lang, C.E.; Birkenmeier, R.; Hahn, M.G.; Sahrmann, S.A.; Edwards, D.F. Relationships between Upper-Limb Functional Limitation and Self-Reported Disability 3 Months after Stroke. J. Rehabil. Res. Dev. 2006, 43, 401–408. [Google Scholar] [CrossRef] [PubMed]
- Franceschini, M.; La Porta, F.; Agosti, M.; Massucci, M. Is Health-Related-Quality of Life of Stroke Patients Influenced by Neurological Impairments at One Year after Stroke? Eur. J. Phys. Rehabil. Med. 2010, 46, 389–399. [Google Scholar] [PubMed]
- Nichols-larsen, D.S.; Clark, P.C.; Zeringue, A.; Greenspan, A.; Blanton, S. Factors Influencing Stroke Survivors’ Quality of Life during Subacute Recovery. Stroke 2005, 36, 1480–1484. [Google Scholar] [CrossRef] [PubMed]
- Duncan, P.W.; Goldstein, L.B.; Matchar, D.; Divine, G.W.; Feussner, J. Measurement of Motor Recovery after Stroke Outcome Assessment and Sample Size Requirements. Stroke 1992, 23, 1084–1089. [Google Scholar] [CrossRef]
- Kwakkel, G.; Kollen, B.; Twisk, J. Impact of Time on Improvement of Outcome after Stroke. Stroke 2006, 37, 2348–2353. [Google Scholar] [CrossRef]
- Wade, D.T.; Langton-Hewer, R.; Wood, V.A.; Skilbeck, C.E.; Ismail, H.M. The Hemiplegic Arm after Stroke: Measurement and Recovery. J. Neurol. Neurosurg. Psychiatry 1983, 46, 521–524. [Google Scholar] [CrossRef]
- Prabhakaran, S.; Zarahn, E.; Riley, C.; Speizer, A.; Chong, J.Y.; Lazar, R.M.; Marshall, R.S.; Krakauer, J.W. Inter-Individual Variability in the Capacity for Motor Recovery after Ischemic Stroke. Neurorehabil. Neural Repair 2008, 22, 64–71. [Google Scholar] [CrossRef]
- Stinear, C.M.; Byblow, W.D.; Ackerley, S.J.; Smith, M.C.; Borges, V.M.; Barber, P.A. Proportional Motor Recovery After Stroke: Implications for Trial Design. Stroke 2017, 48, 795–798. [Google Scholar] [CrossRef]
- Winters, C.; Van Wegen, E.E.H.; Daffertshofer, A.; Kwakkel, G. Generalizability of the Proportional Recovery Model for the Upper Extremity after an Ischemic Stroke. Neurorehabil. Neural Repair 2015, 29, 614–622. [Google Scholar] [CrossRef]
- Senesh, M.R.; Reinkensmeyer, D.J. Breaking Proportional Recovery after Stroke. Neurorehabil. Neural Repair 2019, 33, 888–901. [Google Scholar] [CrossRef] [PubMed]
- Hope, T.M.H.; Friston, K.; Price, C.J.; Leff, A.P.; Rotshtein, P.; Bowman, H. Recovery after Stroke: Not so Proportional after All? Brain 2019, 142, 15–22. [Google Scholar] [CrossRef] [PubMed]
- Byblow, W.D.; Stinear, C.M.; Barber, P.A.; Petoe, M.A.; Ackerley, S.J. Proportional Recovery after Stroke Depends on Corticomotor Integrity. Ann. Neurol. 2015, 78, 848–859. [Google Scholar] [CrossRef] [PubMed]
- Krakauer, J.W.; Carmichael, S.T.; Corbett, D.; Wittenberg, G.F. Getting Neurorehabilitation Right: What Can Be Learned from Animal Models? Neurorehabil. Neural Repair 2012, 26, 923–931. [Google Scholar] [CrossRef]
- Nudo, R.J.; Milliken, G.W. Reorganization of Movement Representations in Primary Motor Cortex Following Focal Ischemic Infarcts in Adult Squirrel Monkeys. J. Neurophysiol. 1996, 75, 2144–2149. [Google Scholar] [CrossRef]
- Classen, J.; Liepert, J.; Wise, S.P.; Hallett, M.; Cohen, L.G. Rapid Plasticity of Human Cortical Movement Representation Induced by Practice. J. Neurophysiol. 1998, 79, 1117–1123. [Google Scholar] [CrossRef]
- Jensen, J.L.; Marstrand, P.C.D.; Nielsen, J.B. Motor Skill Training and Strength Training Are Associated with Different Plastic Changes in the Central Nervous System. J. Appl. Physiol. 2005, 99, 1558–1568. [Google Scholar] [CrossRef]
- Okabe, N.; Narita, K.; Miyamoto, O. Axonal Remodeling in the Corticospinal Tract after Stroke: How Does Rehabilitative Training Modulate It? Neural Regen. Res. 2017, 12, 185–192. [Google Scholar] [CrossRef]
- Warraich, Z.; Kleim, J.A. Neural Plasticity: The Biological Substrate for Neurorehabilitation. PM&R 2010, 2, S208–S219. [Google Scholar] [CrossRef]
- Han, C.; Wang, Q.; Meng, P.P.; Qi, M.Z. Effects of Intensity of Arm Training on Hemiplegic Upper Extremity Motor Recovery in Stroke Patients: A Randomized Controlled Trial. Clin. Rehabil. 2013, 27, 75–81. [Google Scholar] [CrossRef]
- Lohse, K.R.; Lang, C.E.; Boyd, L.A. Is More Better? Using Metadata to Explore Dose—Response Relationships in Stroke Rehabilitation. Stroke 2014, 45, 2053–2058. [Google Scholar] [CrossRef] [PubMed]
- Bütefisch, C.; Hummelsheim, H.; Denzler, P.; Mauritz, K.H. Repetitive Training of Isolated Movements Improves the Outcome of Motor Rehabilitation of the Centrally Paretic Hand. J. Neurol. Sci. 1995, 130, 59–68. [Google Scholar] [CrossRef] [PubMed]
- Feys, H.; De Weerdt, W.; Verbeke, G.; Steck, G.C.; Capiau, C.; Kiekens, C.; Dejaeger, E.; Van Hoydonck, G.; Vermeersch, G.; Cras, P. Early and Repetitive Stimulation of the Arm Can Substantially Improve the Long-Term Outcome after Stroke: A 5-Year Follow-up Study of a Randomized Trial. Stroke 2004, 35, 924–929. [Google Scholar] [CrossRef] [PubMed]
- Kwakkel, G.; Wagenaar, R.C.; Twisk, J.W.R.; Lankhorst, G.J.; Koetsier, J.C. Intensity of Leg and Arm Training after Primary Middle-Cerebral-Artery Stroke: A Randomised Trial. Lancet 1999, 354, 191–196. [Google Scholar] [CrossRef]
- Kwakkel, G.; Van Peppen, R.; Wagenaar, R.C.; Dauphinee, S.W.; Richards, C.; Ashburn, A.; Miller, K.; Lincoln, N.; Partridge, C.; Wellwood, I.; et al. Effects of Augmented Exercise Therapy Time after Stroke: A Meta-Analysis. Stroke 2004, 35, 2529–2539. [Google Scholar] [CrossRef]
- Lang, C.E.; Lohse, K.R.; Birkenmeier, R.L. Dose and Timing in Neurorehabilitation: Prescribing Motor Therapy after Stroke. Curr. Opin. Neurol. 2016, 28, 549–555. [Google Scholar] [CrossRef]
- Duret, C.; Grosmaire, A.G.; Krebs, H.I. Robot-Assisted Therapy in Upper Extremity Hemiparesis: Overview of an Evidence-Based Approach. Front. Neurol. 2019, 10, 412. [Google Scholar] [CrossRef]
- MacClellan, L.R.; Bradham, D.D.; Whitall, J.; Volpe, B.; Wilson, P.D.; Ohlhoff, J.; Meister, C.; Hogan, N.; Krebs, H.I.; Bever, C.T. Robotic Upper-Limb Neurorehabilitation in Chronic Stroke Patients. J. Rehabil. Res. Dev. 2005, 42, 717–722. [Google Scholar] [CrossRef]
- Lim, J.Y.; Oh, M.K.; Park, J.; Paik, N.J. Does Measurement of Corticospinal Tract Involvement Add Value to Clinical Behavioral Biomarkers in Predicting Motor Recovery after Stroke? Neural Plast. 2020, 2020, 8883839. [Google Scholar] [CrossRef]
- Jamin, P.; Duret, C.; Hutin, E.; Bayle, N.; Koeppel, T.; Gracies, J.M.; Pila, O. Using Robot-Based Variables during Upper Limb Robot-Assisted Training in Subacute Stroke Patients to Quantify Treatment Dose. Sensors 2022, 22, 2989. [Google Scholar] [CrossRef]
- Arya, K.N.; Verma, R.; Garg, R.K. Estimating the Minimal Clinically Important Difference of an Upper Extremity Recovery Measure in Subacute Stroke Patients. Top. Stroke Rehabil. 2011, 18, 599–610. [Google Scholar] [CrossRef] [PubMed]
- Pila, O.; Laborne, F.-X.; Hutin, E.; Duret, C.; Gracies, J.-M.; Bayle, N.; Hutin, É.; Duret, C.; Gracies, J.-M.; Bayle, N. 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, 42. [Google Scholar] [CrossRef] [PubMed]
- Koeppel, T.; Pila, O. Test-Retest Reliability of Kinematic Assessments for Upper Limb Robotic Rehabilitation. IEEE Trans. Neural Syst. Rehabil. Eng. 2020, 28, 2035–2042. [Google Scholar] [CrossRef] [PubMed]
- Coupar, F.; Pollock, A.; Rowe, P.; Weir, C.; Langhorne, P.; Weir, C.; Langhorne, P. Predictors of Upper Limb Recovery after Stroke: A Systematic Review and Meta-Analysis. Clin. Rehabil. 2012, 26, 291–313. [Google Scholar] [CrossRef] [PubMed]
- Duncan, P.W.; Min Lai, S.; Keighley, J. Defining Post-Stroke Recovery: Implications for Design and Interpretation of Drug Trials. Neuropharmacology 2000, 39, 835–841. [Google Scholar] [CrossRef]
- Oosterveer, D.M.; Wermer, M.J.H.; Volker, G.; Vlieland, T.P.M.V. Are There Differences in Long-Term Functioning and Recovery Between Hemorrhagic and Ischemic Stroke Patients Receiving Rehabilitation? J. Stroke Cerebrovasc. Dis. 2022, 31, 106294. [Google Scholar] [CrossRef]
- Boyd, L.A.; Hayward, K.S.; Ward, N.S.; Stinear, C.M.; Rosso, C.; Fisher, R.J.; Carter, A.R.; Leff, A.P.; Copland, D.A.; Carey, L.M.; et al. Biomarkers of Stroke Recovery: Consensus-Based Core Recommendations from the Stroke Recovery and Rehabilitation Roundtable. Int. J. Stroke 2017, 12, 480. [Google Scholar] [CrossRef]
- Milot, M.H.; Spencer, S.J.; Chan, V.; Allington, J.P.; Klein, J.; Chou, C.; Pearson-Fuhrhop, K.; Bobrow, J.E.; Reinkensmeyer, D.J.; Cramer, S.C. Corticospinal Excitability as a Predictor of Functional Gains at the Affected Upper Limb Following Robotic Training in Chronic Stroke Survivors. Neurorehabil. Neural Repair 2014, 28, 819–827. [Google Scholar] [CrossRef]
- Rowe, J.B.; Chan, V.; Ingemanson, M.L.; Cramer, S.C.; Wolbrecht, E.T.; Reinkensmeyer, D.J. Hebbian Model: A Randomized Controlled Trial. Neurorehabil. Neural Repair 2017, 31, 769–780. [Google Scholar] [CrossRef]
- Rosso, C.; Lamy, J.C. Prediction of Motor Recovery after Stroke: Being Pragmatic or Innovative? Curr. Opin. Neurol. 2020, 33, 482–487. [Google Scholar] [CrossRef]
- Jeffers, M.S.; 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. [Google Scholar] [CrossRef] [PubMed]
- MacLellan, C.L.; Keough, M.B.; Granter-Button, S.; Chernenko, G.A.; Butt, S.; Corbett, D. A Critical Threshold of Rehabilitation Involving Brain-Derived Neurotrophic Factor Is Required for Poststroke Recovery. Neurorehabil. Neural Repair 2011, 25, 740–748. [Google Scholar] [CrossRef] [PubMed]
- Lang, C.E.; Macdonald, J.R.; Reisman, D.S.; Boyd, L.A.; Kimberley, T.J.; Schindler-Ivens, S.M.; Hornby, T.G.; Ross, S.A.; Scheets, P.L. Observation of Amounts of Movement Practice Provided during Stroke Rehabilitation. Arch. Phys. Med. Rehabil. 2009, 90, 1692–1698. [Google Scholar] [CrossRef]
- English, C.; Veerbeek, J. Is More Physiotherapy Better after Stroke? Int. J. Stroke 2015, 10, 465–466. [Google Scholar] [CrossRef] [PubMed]
- Hayward, K.S.; Churilov, L.; Dalton, E.J.; Brodtmann, A.; Campbell, B.C.V.; Copland, D.; Dancause, N.; Godecke, E.; Hoffmann, T.C.; Lannin, N.A.; et al. Advancing Stroke Recovery through Improved Articulation of Nonpharmacological Intervention Dose. Stroke 2021, 52, 761–769. [Google Scholar] [CrossRef]
- Sale, P.; Franceschini, M.; Mazzoleni, S.; Palma, E.; Agosti, M.; Posteraro, F. Effects of Upper Limb Robot-Assisted Therapy on Motor Recovery in Subacute Stroke Patients. J. Neuroeng. Rehabil. 2014, 11, 104. [Google Scholar] [CrossRef]
- Kahn, L.E.; Zygman, M.L.; Rymer, W.Z.; Reinkensmeyer, D.J. Effect of Robot-Assisted and Unassisted Exercise on Functional Reaching in Chronic Hemiparesis. In Proceedings of the Annual International Conference of the IEEE Engineering in Medicine and Biology Society, Istanbul, Turkey, 25–28 October 2001; Volume 2, pp. 1344–1347. [Google Scholar] [CrossRef]
- Lotze, M.; Braun, C.; Birbaumer, N.; Anders, S.; Cohen, L.G. Motor Learning Elicited by Voluntary Drive. Brain 2003, 126, 866–872. [Google Scholar] [CrossRef]
- Plautz, E.J.; Milliken, G.W.; Nudo, R.J. Effects of Repetitive Motor Training on Movement Representations in Adult Squirrel Monkeys: Role of Use versus Learning. Neurobiol. Learn. Mem. 2000, 74, 27–55. [Google Scholar] [CrossRef]
- Perez, M.A.; Lungholt, B.K.S.; Nyborg, K.; Nielsen, J.B. Motor Skill Training Induces Changes in the Excitability of the Leg Cortical Area in Healthy Humans. Exp. Brain Res. 2004, 159, 197–205. [Google Scholar] [CrossRef]
- Miyai, I.; Suzuki, M.; Hatakenaka, M.; Kubota, K. Effect of Body Weight Support on Cortical Activation during Gait in Patients with Stroke. Exp. Brain Res. 2006, 169, 85–91. [Google Scholar] [CrossRef]
- Kahn, L.E.; Zygman, M.L.; Rymer, W.Z.; Reinkensmeyer, D.J. Robot-Assisted Reaching Exercise Promotes Arm Movement Recovery in Chronic Hemiparetic Stroke: A Randomized Controlled Pilot Study. J. Neuroeng. Rehabil. 2006, 3, 12. [Google Scholar] [CrossRef] [PubMed]
- Takebayashi, T.; Takahashi, K.; Okita, Y.; Kubo, H.; Hachisuka, K.; Domen, K. Impact of the Robotic-Assistance Level on Upper Extremity Function in Stroke Patients Receiving Adjunct Robotic Rehabilitation: Sub-Analysis of a Randomized Clinical Trial. J. NeuroEngineering Rehabil. 2022, 19, 25. [Google Scholar] [CrossRef] [PubMed]
- Emken, J.L.; Bobrow, J.E.; Reinkensmeyer, D.J. Robotic Movement Training as an Optimization Problem: Designing a Controller That Assists Only as Needed. In Proceedings of the 9th International Conference on Rehabilitation Robotics, Chicago, IL, USA, 28 June–1 July 2005; pp. 307–312. [Google Scholar]
- Reinkensmeyer, D.J.; Wolbrecht, E.T.; Bobrow, J.E. A Computational Model of Human-Robot Load Sharing during Robot-Assisted Arm Movement Training after Stroke. Proc. Int. Conf. IEEE Eng. Med. Biol. 2007, 2007, 4019–4023. [Google Scholar]
Non-Responders (n = 16) | Responders (n = 20) | |
---|---|---|
Age (years) | 62 (16) | 56 (16) |
Sex (n females/n males) | 7/9 | 8/12 |
Side of paresis (n right/n left) | 10/6 | 9/11 |
Type of stroke (n ischemia/n hemorrhage) | 14/2 | 11/9 |
Time since stroke at RT initiation (days) | 63 (31) | 48 (20) |
FMA score (66 pts) | 22 (18) | 24 (16) |
Velocity (%) | 19 (17) | 18 (20) |
Distance (%) | 37 (49) | 25 (50) |
Smoothness (%) | 447 (230) | 329 (158) |
Accuracy (%) | 689 (497) | 657 (580) |
Actual Practice Time (%) | Number of Movements (n) | Total Distance Covered (cm) | ||||
---|---|---|---|---|---|---|
NR | R | NR | R | NR | R | |
S1 | 44 (14) | 50 (18) | 609 (299) | 636 (322) | 6004 (4540) | 7375 (4506) |
S2 | 42 (10) | 57 (12) | 592 (211) | 740 (288) | 5521 (3389) | 8713 (4737) |
S3 | 47 (17) | 51 (15) | 692 (360) | 662 (294) | 7155 (5788) | 7737 (4357) |
S4 | 48 (12) | 47 (16) | 711 (276) | 681 (292) | 7017 (4280) | 7746 (4641) |
S5 | 46 (13) | 47 (11) | 745 (310) | 710 (216) | 7683 (4778) | 8051 (3817) |
S6 | 51 (11) | 49 (15) | 826 (369) | 695 (265) | 8827 (5624) b | 8254 (4107) |
S7 | 49 (15) | 51 (14) | 827 (395) | 728 (251) | 9043 (6388) b | 8977 (3830) |
S8 | 50 (12) | 49 (14) | 831 (405) | 724 (270) | 10,041 (6165) b | 8921 (4057) |
S9 | 54 (11) | 48 (19) | 893 (365) ab | 720 (345) | 10,385 (6673) ab | 8776 (5108) |
S10 | 57 (13) b | 47 (16) | 892 (411) ab | 685 (296) | 10,830 (7613) abd | 8617 (4358) |
S11 | 55 (11) | 48 (17) | 897 (508) ab | 732 (250) | 9094 (6222) abcd | 9256 (3929) |
S12 | 51 (14) | 48 (14) | 798 (429) | 719 (259) | 10,819 (7683) b | 9098 (3795) |
S13 | 55 (13) | 50 (12) | 898 (524) ab | 732 (227) | 10,499 (6242) abcd | 9532 (3461) |
S14 | 54 (8) | 46 (15) | 902 (426) ab | 711 (289) | 10,104 (5677) abcd | 9599 (4148) |
S15 | 52 (12) | 42 (12) b | 898 (477) ab | 657 (222) | 10,567 (6785) abcd | 8814 (3301) |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Pila, O.; Duret, C.; Koeppel, T.; Jamin, P. Performance-Based Robotic Training in Individuals with Subacute Stroke: Differences between Responders and Non-Responders. Sensors 2023, 23, 4304. https://doi.org/10.3390/s23094304
Pila O, Duret C, Koeppel T, Jamin P. Performance-Based Robotic Training in Individuals with Subacute Stroke: Differences between Responders and Non-Responders. Sensors. 2023; 23(9):4304. https://doi.org/10.3390/s23094304
Chicago/Turabian StylePila, Ophélie, Christophe Duret, Typhaine Koeppel, and Pascal Jamin. 2023. "Performance-Based Robotic Training in Individuals with Subacute Stroke: Differences between Responders and Non-Responders" Sensors 23, no. 9: 4304. https://doi.org/10.3390/s23094304
APA StylePila, O., Duret, C., Koeppel, T., & Jamin, P. (2023). Performance-Based Robotic Training in Individuals with Subacute Stroke: Differences between Responders and Non-Responders. Sensors, 23(9), 4304. https://doi.org/10.3390/s23094304