Robotic Rehabilitation in Spinal Cord Injury: A Pilot Study on End-Effectors and Neurophysiological Outcomes.
End-effector devices
Functional connectivity (FC)
Resting state networks (RSN)
Robot-aided gait training (RAGT)
Spinal cord injury (SCI)
Journal
Annals of biomedical engineering
ISSN: 1573-9686
Titre abrégé: Ann Biomed Eng
Pays: United States
ID NLM: 0361512
Informations de publication
Date de publication:
Feb 2021
Feb 2021
Historique:
received:
18
04
2020
accepted:
02
09
2020
pubmed:
13
9
2020
medline:
6
10
2021
entrez:
12
9
2020
Statut:
ppublish
Résumé
Robot-aided gait training (RAGT) has been implemented to provide patients with spinal cord injury (SCI) with a physiological limb activation during gait, cognitive engagement, and an appropriate stimulation of peripheral receptors, which are essential to entrain neuroplasticity mechanisms supporting functional recovery. We aimed at assessing whether RAGT by means of an end-effector device equipped with body weight support could improve functional ambulation in patients with subacute, motor incomplete SCI. In this pilot study, 15 patients were provided with six RAGT sessions per week for eight consecutive weeks. The outcome measures were muscle strength, ambulation, going upstairs, and disease burden. Furthermore, we estimated the activation patterns of lower limb muscles during RAGT by means of surface electromyography and the resting state networks' functional connectivity (RSN-FC) before and after RAGT. Patients achieved a clinically significant improvement in the clinical outcome measures substantially up to six months post-treatment. These data were paralleled by an improvement in the stair-climbing cycle and a potentiating of frequency-specific and area-specific RSN-FC patterns. Therefore, RAGT, by means of an end-effector device equipped with body weight support, is promising in improving gait in patients with subacute, motor incomplete SCI, and it could produce additive benefit for the neuromuscular reeducation to gait in SCI when combined with conventional physiotherapy.
Identifiants
pubmed: 32918105
doi: 10.1007/s10439-020-02611-z
pii: 10.1007/s10439-020-02611-z
doi:
Types de publication
Clinical Trial
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
732-745Références
Alcobendas-Maestro, M., A. Esclarín-Ruz, R. M. Casado-López, A. Muñoz-González, G. Pérez-Mateos, E. González-Valdizán, and J. L. Martín. Lokomat robotic-assisted versus overground traing within 3 to 6 months of incomplete spinal cord lesion: randomized controlled trial. Neurorehabil. Neural Repair 26(9):1058–1063, 2012.
pubmed: 22699827
Anderson, K. D., M. E. Acuff, B. G. Arp, D. Backus, S. Chun, K. Fisher, et al. United States (US) multi-center study to assess the validity and reliability of the Spinal Cord Independence Measure (SCIM III). Spinal Cord 49(8):880–885, 2011.
pubmed: 21445081
Astolfi, L., H. Bakardjian, F. Cincotti, D. Mattia, M. G. Marciani, F. De Vico Fallani, A. Colosimo, S. Salinari, F. Miwakeichi, Y. Yamaguchi, P. Martinez, A. Cichocki, A. Tocci, and F. Babiloni. Estimate of causality between independent cortical spatial patterns during movement volition in spinal cord injured patients. Brain Topogr. 19(3):107–123, 2007.
pubmed: 17577652
Athanasiou, A., M. A. Klados, N. Pandria, N. Foroglou, K. R. Kavazidi, K. Polyzoidis, and P. D. Bamidis. A systematic review of investigations into functional brain connectivity following spinal cord injury. Front. Hum. Neurosci. 11:517, 2017.
pubmed: 29163098
pmcid: 5669283
Athanasiou, A., M. A. Klados, C. Styliadis, N. Foroglou, K. Polyzoidis, and P. D. Bamidis. Investigating the role of α and β rhythms in functional motor networks. Neuroscience 378:54–70, 2016.
pubmed: 27241945
Awai, L., M. Bolliger, A. R. Ferguson, G. Courtine, and A. Curt. Influence of spinal cord integrity on gait control in human spinal cord injury. Neurorehabil. Neural Repair 30(6):562–572, 2016.
pubmed: 26428035
Barrière, G., H. Leblond, J. Provencher, and S. Rossignol. Prominent role of the spinal central pattern generator in the recovery of locomotion after partial spinal cord injuries. J. Neurosci. 28(15):3976–3987, 2008.
pubmed: 18400897
pmcid: 6670475
Benito-Penalva, J., D. J. Edwards, E. Opisso, M. Cortes, R. Lopez-Blazquez, N. Murillo, U. Costa, J. M. Tormos, J. Vidal-Samsó, J. Valls-Solé, European Multicenter Study about Human Spinal Cord Injury Study Group, and J. Medina. Gait training in human spinal cord injury using electromechanical systems: effect of device type and patient characteristics. Arch. Phys. Med. Rehabil. 93(3):404–412, 2012.
pubmed: 22209475
Blanc, Y., and U. Dimanico. Electrode placement in surface electromyography (sEMG) “minimal crosstalk area” (MCA). Open Rehabil. J. 3:110–126, 2010.
Bönstrup, M., L. Krawinkel, R. Schulz, B. Cheng, J. Feldheim, G. Thomalla, L. G. Cohen, and C. Gerloff. Low-frequency brain oscillations track motor recovery in human stroke. Ann. Neurol. 86(6):853–865, 2019.
pubmed: 31604371
Burns, A. S., R. J. Marino, S. Kalsi-Ryan, J. W. Middleton, L. A. Tetreault, J. R. Dettori, K. E. Mihalovich, and M. G. Fehlings. Type and timing of rehabilitation following acute and subacute spinal cord injury: a systematic review. Global Spine J. 7(3 Suppl):175S–194S, 2017.
pubmed: 29164023
pmcid: 5684843
Calabrò, R. S., A. Cacciola, F. Bertè, A. Manuli, A. Leo, A. Bramanti, A. Naro, D. Milardi, and P. Bramanti. Robotic gait rehabilitation and substitution devices in neurological disorders: where are we now? Neurol. Sci. 37(4):503–514, 2016.
pubmed: 26781943
Calabrò, R. S., A. Naro, M. Russo, P. Bramanti, L. Carioti, T. Balletta, A. Buda, A. Manuli, S. Filoni, and A. Bramanti. Shaping neuroplasticity by using powered exoskeletons in patients with stroke: a randomized clinical trial. J. Neuroeng. Rehabil. 15(1):35, 2018.
pubmed: 29695280
pmcid: 5918557
Cardoso, J. Source separation using higher order moments.International Conference on Acoustics, Speech, and Signal Processing (Glasgow, UK), vol. 4, pp. 2109–2112, 1989.
Chen, I. H., Y. R. Yang, C. F. Lu, and R. Y. Wang. Novel gait training alters functional brain connectivity during walking in chronic stroke patients: a randomized controlled pilot trial. J. Neuroeng. Rehabil. 16(1):33, 2019.
pubmed: 30819259
pmcid: 6396471
Cheng, P. Y., and P. Y. Lai. Comparison of exoskeleton robots and end-effector robots on training methods and gait biomechanics. In: Intelligent Robotics and Applications: ICIRA 2013: Lecture Notes in Computer Science, Vol. 8102, edited by J. Lee, M. C. Lee, H. Liu, and J. H. Ryu. Berlin, Heidelberg: Springer, 2013.
Cichocki, A., and S. Amari. Adaptive Blind Signal and Image Processing. Learning Algorithms and Applications. NewYork, NY: Wiley, 2002.
De Vico Fallani, F., L. Astolfi, F. Cincotti, D. Mattia, M. G. Marciani, S. Salinari, J. Kurths, S. Gao, A. Cichocki, A. Colosimo, and F. Babiloni. Cortical functional connectivity networks in normal and spinal cord injured patients: evaluation by graph analysis. Hum. Brain Mapp. 28(12):1334–1346, 2007.
pubmed: 17315225
De Vico Fallani, F., L. Astolfi, F. Cincotti, D. Mattia, A. Tocci, M. G. Marciani, A. Colosimo, S. Salinari, S. Gao, A. Cichocki, and F. Babiloni. Extracting information from cortical connectivity patterns estimated from high resolution EEG recordings: a theoretical graph approach. Brain Topogr. 19(3):125–136, 2007.
pubmed: 17587170
De Vico Fallani, F., F. A. Rodrigues, L. da Fontoura Costa, L. Astolfi, F. Cincotti, D. Mattia, S. Salinari, and F. Babiloni. Multiple pathways analysis of brain functional networks from EEG signals: an application to real data. Brain Topogr. 23(4):344–354, 2011.
pubmed: 20614232
Dietz, V., R. Müller, and G. Colombo. Locomotor activity in spinal man: significance of afferent input from joint and load receptors. Brain 125(Pt 12):2626–2634, 2002.
pubmed: 12429590
Espenhahn, S., B. van Wijk, H. E. Rossiter, A. O. de Berker, N. D. Redman, J. Rondina, J. Diedrichsen, and N. S. Ward. Cortical beta oscillations are associated with motor performance following visuomotor learning. NeuroImage 195:340–353, 2019.
pubmed: 30954709
pmcid: 6547051
Fang, C. Y., J. L. Tsai, G. S. Li, A. S. Lien, and Y. J. Chang. Effects of robot-assisted gait training in individuals with spinal cord injury: a meta-analysis. Biomed. Res. Int. 2020:2102785, 2020.
pubmed: 32280681
pmcid: 7115057
Fuchs, M., J. Kastner, M. Wagner, S. Hawes, and J. S. Ebersole. A standardized boundary element method volume conductor model. Clin. Neurophysiol. 113(5):702–712, 2002.
pubmed: 11976050
Gassert, R., and V. Dietz. Rehabilitation robots for the treatment of sensorimotor deficits: a neurophysiological perspective. J. Neuroeng. Rehabil. 15:46, 2018.
pubmed: 29866106
pmcid: 5987585
Ghapanchizadeh, H., A. Siti Aqlima, I. Asnor Juraiza, and A. Maged Saleh Saeed. Review of surface electrode placement for recording electromyography signals. Biomed. Res. 2017:S1–S7, 2016.
Goffredo, M., C. Iacovelli, E. Russo, S. Pournajaf, C. Blasi, D. Galafate, L. Pellicciari, M. Agosti, S. Filoni, I. Aprile, and M. Franceschini. Stroke gait rehabilitation: a comparison of end-effector, overground exoskeleton, and conventional gait training. Appl. Sci. 9:2627, 2019.
Goñi, J., M. P. van den Heuvel, A. Avena-Koenigsberger, N. Velez de Mendizabal, R. F. Betzel, A. Griffa, P. Hagmann, B. Corominas-Murtra, J. P. Thiran, and O. Sporns. Resting-brain functional connectivity predicted by analytic measures of network communication. Proc. Natl. Acad. Sci. U.S.A. 111(2):833–838, 2014.
pubmed: 24379387
Grillner, S., and A. El Manira. Current principles of motor control, with special reference to vertebrate locomotion. Physiol. Rev. 100(1):271–320, 2020.
pubmed: 31512990
Harnie, J., A. Doelman, E. de Vette, J. Audet, E. Desrochers, N. Gaudreault, and A. Frigon. The recovery of standing and locomotion after spinal cord injury does not require task-specific training. Life 8:e50134, 2019.
Hesse, S., N. Schattat, J. Mehrholz, and C. Werner. Evidence of end-effector based gait machines in gait rehabilitation after CNS lesion. NeuroRehabilitation 33(1):77–84, 2013.
pubmed: 23949037
Hou, J. M., T. S. Sun, Z. M. Xiang, J. Z. Zhang, Z. C. Zhang, M. Zhao, J. F. Zhong, J. Liu, H. Zhang, H. L. Liu, R. B. Yan, and H. T. Li. Alterations of resting-state regional and network-level neural function after acute spinal cord injury. Neuroscience 277:446–454, 2014.
pubmed: 25086312
Ilvesmäki, T., E. Koskinen, A. Brander, T. Luoto, J. Öhman, and H. Eskola. Spinal cord injury induces widespread chronic changes in cerebral white matter. Hum. Brain Mapp. 38(7):3637–3647, 2017.
pubmed: 28429407
pmcid: 6866745
Jonmohamadi, Y., G. Poudel, C. Innes, and R. Jones. Source-space ICA for EEG source separation, localization, and time-course reconstruction. NeuroImage 101:720–737, 2014.
pubmed: 25108125
Kaushal, M., A. Oni-Orisan, G. Chen, W. Li, J. Leschke, B. D. Ward, B. Kalinosky, M. D. Budde, B. D. Schmit, S. J. Li, V. Muqeet, and S. N. Kurpad. Evaluation of whole-brain resting-state functional connectivity in spinal cord injury: a large-scale network analysis using network-based statistic. J. Neurotrauma 34(6):1278–1282, 2017.
pubmed: 27937140
Khorasanizadeh, M., M. Yousefifard, M. Eskian, Y. Lu, M. Chalangari, J. S. Harrop, S. B. Jazayeri, S. Seyedpour, B. Khodaei, M. Hosseini, and V. Rahimi-Movaghar. Neurological recovery following traumatic spinal cord injury: a systematic review and meta-analysis. J. Neurosurg. Spine 15:1–17, 2019.
Klarner, T., and E. P. Zehr. Sherlock Holmes and the curious case of the human locomotor central pattern generator. J. Neurophysiol. 120(1):53–77, 2018.
pubmed: 29537920
pmcid: 6093959
Lam, T., K. Pauhl, A. Krassioukov, and J. J. Eng. Using robot-applied resistance to augment body-weight-supported treadmill training in an individual with incomplete spinal cord injury. Phys. Ther. 91(1):143–151, 2011.
pubmed: 21127165
Lamont, E. V., and E. P. Zehr. Task-specific modulation of cutaneous reflexes expressed at functionally relevant gait cycle phases during level and incline walking and stair climbing. Exp. Brain Res. 173:185–192, 2006.
pubmed: 16821052
Lee, S. H., G. Park, D. Y. Cho, et al. Comparisons between end-effector and exoskeleton rehabilitation robots regarding upper extremity function among chronic stroke patients with moderate-to-severe upper limb impairment. Sci. Rep. 10:1806, 2020.
pubmed: 32019981
pmcid: 7000418
Lencioni, T., I. Carpinella, M. Rabuffetti, et al. Human kinematic, kinetic and EMG data during different walking and stair ascending and descending tasks. Sci. Data 6:309, 2019.
pubmed: 31811148
pmcid: 6897988
Lu, T. W., and C. F. Chang. Biomechanics of human movement and its clinical applications. Kaohsiung J. Med. Sci. 28:S13–S25, 2012.
pubmed: 22301008
Mattia, D., F. Cincotti, L. Astolfi, F. de Vico Fallani, G. Scivoletto, M. G. Marciani, and F. Babiloni. Motor cortical responsiveness to attempted movements in tetraplegia: evidence from neuroelectrical imaging. Clin. Neurophysiol. 120(1):181–189, 2009.
pubmed: 19010081
Mazziotta, J., A. Toga, A. Evans, P. Fox, J. Lancaster, K. Zilles, et al. A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 356(1412):1293–1322, 2001.
Mehrholz, J., L. A. Harvey, S. Thomas, and B. Elsner. Is body-weight-supported treadmill training or robotic-assisted gait training superior to overground gait training and other forms of physiotherapy in people with spinal cord injury? A systematic review. Spinal Cord 55(8):722–729, 2017.
pubmed: 28398300
Mehrholz, J., C. Werner, S. Hesse, and M. Pohl. Immediate and long-term functional impact of repetitive locomotor training as an adjunct to conventional physiotherapy for non-ambulatory patients after stroke. Disabil. Rehabil. 30(11):830–836, 2008.
pubmed: 17852272
Mekki, M., A. D. Delgado, A. Fry, D. Putrino, and V. Huang. Robotic rehabilitation and spinal cord injury: a narrative review. Neurotherapeutics 15(3):604–617, 2018.
pubmed: 29987763
pmcid: 6095795
Mıdık, M., N. Paker, D. Buğdaycı, and A. C. Mıdık. Effects of robot-assisted gait training on lower extremity strength, functional independence, and walking function in men with incomplete traumatic spinal cord injury. Turk. J. Phys. Med. Rehabil. 66(1):54–59, 2020.
pubmed: 32318675
pmcid: 7171894
Min, Y. S., Y. Chang, J. W. Park, J. M. Lee, J. Cha, J. J. Yang, C. H. Kim, J. M. Hwang, J. N. Yoo, and T. D. Jung. Change of brain functional connectivity in patients with spinal cord injury: graph theory based approach. Ann. Rehabil. Med. 39(3):374–383, 2015.
pubmed: 26161343
pmcid: 4496508
Min, Y. S., J. W. Park, S. U. Jin, K. E. Jang, H. U. Nam, Y. S. Lee, T. D. Jung, and Y. Chang. Alteration of resting-state brain sensorimotor connectivity following spinal cord injury: a resting-state functional magnetic resonance imaging study. J. Neurotrauma 32(18):1422–1427, 2015.
pubmed: 25945389
Mirbagheri, M. M., M. Kindig, X. Niu, D. Varoqui, and P. Conaway. Robotic-locomotor training as a tool to reduce neuromuscular abnormality in spinal cord injury: the application of system identification and advanced longitudinal modeling. IEEE International Conference on Rehabilitation Robotics: [Proceedings], 6650497, 2013.
Molteni, F., G. Gasperini, G. Cannaviello, and E. Guanziroli. Exoskeleton and end-effector robots for upper and lower limbs rehabilitation: narrative review. PM & R 10(9 Suppl 2):S174–S188, 2018.
Nardone, R., Y. Höller, F. Brigo, M. Seidl, M. Christova, J. Bergmann, et al. Functional brain reorganization after spinal cord injury: systematic review of animal and human studies. Brain Res. 1504:58–73, 2013.
pubmed: 23396112
Oni-Orisan, A., M. Kaushal, W. Li, J. Leschke, B. D. Ward, A. Vedantam, B. Kalinosky, M. D. Budde, B. D. Schmit, S. J. Li, V. Muqeet, and S. N. Kurpad. Alterations in cortical sensorimotor connectivity following complete cervical spinal cord injury: a prospective resting-state fMRI study. PLoS ONE 11(3):e0150351, 2016.
pubmed: 26954693
pmcid: 4783046
Pan, Y., W. B. Dou, Y. H. Wang, H. W. Luo, Y. X. Ge, S. Y. Yan, Q. Xu, Y. Y. Tu, Y. Q. Xiao, Q. Wu, Z. Z. Zheng, and H. L. Zhao. Non-concomitant cortical structural and functional alterations in sensorimotor areas following incomplete spinal cord injury. Neural Regen. Res. 12(12):2059–2066, 2017.
pubmed: 29323046
pmcid: 5784355
Paolucci, S., M. Bragoni, P. Coiro, D. De Angelis, F. R. Fusco, D. Morelli, V. Venturiero, and L. Pratesi. Quantification of the probability of reaching mobility independence at discharge from a rehabilitation hospital in nonwalking early ischemic stroke patients: a multivariate study. Cerebrovasc. Dis. (Basel, Switzerland) 26(1):16–22, 2008.
Pascual-Marqui, R. D. iscrete, 3D distributed, linear imaging methods of electric neuronal activity. Part 1: exact, zero error localization. arXiv:0710.3341, 2007.
Pascual-Marqui, R. D., and R. J. Biscay-Lirio. Interaction patterns of brain activity across space, time and frequency. Part I: methods. arXiv:1103.2852v2, 2011.
Rossignol, S. Plasticity of connections underlying locomotor recovery after central and/or peripheral lesions in the adult mammals. Philos. Trans. R Soc. B 361:1647–1671, 2006.
Rossignol, S., R. Dubuc, and J. P. Gossard. Dynamic sensorimotor interactions in locomotion. Physiol. Rev. 86:89–154, 2006.
pubmed: 16371596
Sale, P., M. Franceschini, A. Waldner, and S. Hesse. Use of the robot assisted gait therapy in rehabilitation of patients with stroke and spinal cord injury. Eur. J. Phys. Rehabil. Med. 48(1):111–121, 2012.
pubmed: 22543557
Samaha, J., O. Gosseries, and B. R. Postle. Distinct oscillatory frequencies underlie excitability of human occipital and parietal cortex. J. Neurosci. 37:2824–2833, 2017.
pubmed: 28179556
pmcid: 5354329
Schmidt, H., C. Werner, R. Bernhardt, S. Hesse, and J. Krüger. Gait rehabilitation machines based on programmable footplates. J. Neuroeng. Rehabil. 4:2, 2007.
pubmed: 17291335
pmcid: 1804273
Sharififar, S., H. K. Vincent, J. Shuster, and M. Bishop. Quantifying poststroke gait deviations: a meta-analysis of observational and cross-sectional experimental trials. J. Stroke Med. 2(1):23–31, 2019.
Swinnen, E., S. Duerinck, J. P. Baeyens, and R. Meeusen. Effectiveness of robot-assisted gait training in persons with spinal cord injury: a systematic review. J. Rehabil. Med. 42:520–526, 2010.
pubmed: 20549155
Youssofzadeh, V., D. Zanotto, K. Wong-Lin, S. K. Agrawal, and G. Prasad. Directed functional connectivity in fronto-centroparietal circuit correlates with motor adaptation in gait training. IEEE Trans. Neural Syst Rehabil. Eng. 24(11):1265–1275, 2016.
pubmed: 27071181
Zheng, W., Q. Chen, X. Chen, L. Wan, W. Qin, Z. Qi, N. Chen, and K. Li. Brain white matter impairment in patients with spinal cord injury. Neural Plast. 2017:4671607, 2017.
pubmed: 28255458
pmcid: 5309430