Effectiveness of action observation therapy based on virtual reality technology in the motor rehabilitation of paretic stroke patients: a randomized clinical trial

Antonino Errante, Donatella Saviola, Matteo Cantoni, Katia Iannuzzelli, Settimio Ziccarelli, Fabrizio Togni, Marcello Simonini, Carolina Malchiodi, Debora Bertoni, Maria Grazia Inzaghi, Francesca Bozzetti, Roberto Menozzi, Annamaria Quarenghi, Paola Quarenghi, Daniele Bosone, Leonardo Fogassi, Gian Piero Salvi, Antonio De Tanti, Antonino Errante, Donatella Saviola, Matteo Cantoni, Katia Iannuzzelli, Settimio Ziccarelli, Fabrizio Togni, Marcello Simonini, Carolina Malchiodi, Debora Bertoni, Maria Grazia Inzaghi, Francesca Bozzetti, Roberto Menozzi, Annamaria Quarenghi, Paola Quarenghi, Daniele Bosone, Leonardo Fogassi, Gian Piero Salvi, Antonio De Tanti

Abstract

Background: The rehabilitation of paretic stroke patients uses a wide range of intervention programs to improve the function of impaired upper limb. A new rehabilitative approach, called action observation therapy (AOT) is based on the discovery of mirror neurons and has been used to improve the motor functions of adult stroke patients and children with cerebral palsy. Recently, virtual reality (VR) has provided the potential to increase the frequency and effectiveness of rehabilitation treatment by offering challenging and motivating tasks. METHODS: The purpose of the present project is to design a randomized controlled six-month follow-up trial (RCT) to evaluate whether action observation (AO) added to standard VR (AO + VR) is effective in improving upper limb function in patients with stroke, compared with a control treatment consisting of observation of naturalistic scenes (CO) without any action content, followed by VR training (CO + VR).

Discussion: AO + VR treatment may provide an addition to the rehabilitative interventions currently available for recovery after stroke and could be utilized within standard sensorimotor training or in individualized tele-rehabilitation.

Trial registration: The trial has been prospectively registered on ClinicalTrials.gov. NCT05163210 . 17 December 2021.

Keywords: Action observation therapy; Mirror neuron system; Motor learning; Stroke; Virtual reality.

Conflict of interest statement

The authors declare that they have no competing interests.

© 2022. The Author(s).

Figures

Fig. 1
Fig. 1
Flow diagram of AOT based on VR study according to CONSORT guidelines. Abbreviations: BBT = Box and Block Test; AO + VR = experimental intervention based on action observation therapy based on virtual reality techniques; CO + VR = control intervention based on observation of control videos followed by the execution of actions using virtual reality
Fig. 2
Fig. 2
(A) Experimental setting for both AO + VR and CO + VR interventions. (B1) Static frame showing an example of video-clip to be used for the experimental treatment AO + VR based on observation of actions performed by a model followed by subsequent imitation. (B2) Static frame of a video-clip illustrating natural scene, to be used in the CO + VR control treatment

References

    1. Kwakkel G, Kollen BJ, Van der Grond JV, Prevo AJH. Probability of regaining dexterity in the flaccid upper limb: Impact of severity of paresis and time since onset in acute stroke. Stroke. 2003;34:2181–2186. doi: 10.1161/.
    1. Wallace AC, Talelli P, Dileone M, Oliver R, Ward N, Cloud G, et al. Standardizing the intensity of upper limb treatment in rehabilitation medicine. Clin Rehabil. 2010;24:471–478. doi: 10.1177/0269215509358944.
    1. French B, Thomas L, Leathley M, Sutton C, McAdam J, Forster A, et al. Does repetitive task training improve functional activity after stroke? A Cochrane systematic review and meta-analysis. J Rehabil Med. 2010;42:9–15. doi: 10.2340/16501977-0473.
    1. Garrison KA, Winstein CJ, Aziz-Zadeh L. The mirror neuron system: A neural substrate for methods in stroke rehabilitation. Neurorehabil Neural Repair. 2010;24:404–412. doi: 10.1177/1545968309354536.
    1. Buccino G. Action observation treatment: A novel tool in neurorehabilitation. Philos Trans R Soc B Biol Sci. 2014;369:20130185. doi: 10.1098/rstb.2013.0185.
    1. Buchignani B, Beani E, Pomeroy V, Iacono O, Sicola E, Perazza S, et al. Action observation training for rehabilitation in brain injuries: a systematic review and meta-analysis. BMC Neurol. 2019;19(1):344. doi: 10.1186/s12883-019-1533-x.
    1. Borges LR, Fernandes AB, Melo LP, Guerra RO, Campos TF. Action observation for upper limb rehabilitation after stroke. Cochrane Database Syst Rev. 2018;10(10):CD011887. doi: 10.1002/14651858.CD011887.pub2.
    1. Rizzolatti G, Cattaneo L, Fabbri-Destro M, Rozzi S. Cortical mechanisms underlying the organization of goal-directed actions and mirror neuron-based action understanding. Physiol Rev. 2014;94:655–706. doi: 10.1152/physrev.00009.2013.
    1. Rizzolatti G, Fogassi L. The mirror mechanism: recent findings and perspectives. Philos Trans R Soc Lond B Biol Sci. 2014;369(1644):20130420. doi: 10.1098/rstb.2013.0420.
    1. Molenberghs P, Cunnington R, Mattingley JB. Brain regions with mirror properties: A meta-analysis of 125 human fMRI studies. Neurosci Biobehav Rev. 2012;36:341–349. doi: 10.1016/j.neubiorev.2011.07.004.
    1. Gazzola V, Keysers C. The observation and execution of actions share motor and somatosensory voxels in all tested subjects: Single-subject analyses of unsmoothed fMRI data. Cereb Cortex. 2009;19:1239–1255. doi: 10.1093/cercor/bhn181.
    1. Hardwick RM, Caspers S, Eickhoff SB, Swinnen SP. Neural correlates of action: Comparing meta-analyses of imagery, observation, and execution. Neurosci Biobehav Rev. 2018;94:31–44. doi: 10.1016/j.neubiorev.2018.08.003.
    1. Ertelt D, Small S, Solodkin A, Dettmers C, McNamara A, Binkofski F, et al. Action observation has a positive impact on rehabilitation of motor deficits after stroke. Neuroimage. 2007;36(SUPPL):2.
    1. Franceschini M, Ceravolo MG, Agosti M, Cavallini P, Bonassi S, Dall’Armi V, et al. Clinical relevance of action observation in upper-limb stroke rehabilitation: A possible role in recovery of functional dexterity. A randomized clinical trial. Neurorehabil Neural Repair. 2012;26:456–62. doi: 10.1177/1545968311427406.
    1. Franceschini M, Agosti M, Cantagallo A, Sale P, Mancuso M, Buccino G. Mirror neurons: Action observation treatment as a tool in stroke rehabilitation. Eur J Phys Rehabil Med. 2010;46:517–523.
    1. Pelosin E, Avanzino L, Bove M, Stramesi P, Nieuwboer A, Abbruzzese G. Action observation improves freezing of gait in patients with Parkinson’s disease. Neurorehabil Neural Repair. 2010;24:746–752. doi: 10.1177/1545968310368685.
    1. Caligiore D, Mustile M, Spalletta G, Baldassarre G. Action observation and motor imagery for rehabilitation in Parkinson’s disease: A systematic review and an integrative hypothesis. Neurosci Biobehav Rev. 2017;72:210–222. doi: 10.1016/j.neubiorev.2016.11.005.
    1. Buccino G, Arisi D, Gough P, Aprile D, Ferri C, Serotti L, et al. Improving upper limb motor functions through action observation treatment: A pilot study in children with cerebral palsy. Dev Med Child Neurol. 2012;54:822–828. doi: 10.1111/j.1469-8749.2012.04334.x.
    1. Sgandurra G, Ferrari A, Cossu G, Guzzetta A, Fogassi L, Cioni G. Randomized trial of observation and execution of upper extremity actions versus action alone in children with unilateral cerebral palsy. Neurorehabil Neural Repair. 2013;27:808–815. doi: 10.1177/1545968313497101.
    1. Sgandurra G, Biagi L, Fogassi L, Ferrari A, Sicola E, Guzzetta A, et al. Reorganization of action observation and sensory-motor networks after action observation therapy in children with congenital hemiplegia: A pilot study. Dev Neurobiol. 2020;80:351–360. doi: 10.1002/dneu.22783.
    1. Alamer A, Melese H, Adugna B. Effectiveness of Action Observation Training on Upper Limb Motor Function in Children with Hemiplegic Cerebral Palsy: A Systematic Review of Randomized Controlled Trials. Pediatr Heal Med Ther. 2020;11:335–46.
    1. Buccino G, Molinaro A, Ambrosi C, Arisi D, Mascaro L, Pinardi C, et al. Action Observation Treatment Improves Upper Limb Motor Functions in Children with Cerebral Palsy: a Combined Clinical and Brain Imaging Study. Neural Plast. 2018;2018:4843985. doi: 10.1155/2018/4843985.
    1. Bellelli G, Buccino G, Bernardini B, Padovani A, Trabucchi M. Action observation treatment improves recovery of postsurgical orthopedic patients: Evidence for a top-down effect? Arch Phys Med Rehabil. 2010;91:1489–1494. doi: 10.1016/j.apmr.2010.07.013.
    1. Fluet GG, Deutsch JE. Virtual Reality for Sensorimotor Rehabilitation Post-Stroke: The Promise and Current State of the Field. Curr Phys Med Rehabil Reports. 2013;1:9–20. doi: 10.1007/s40141-013-0005-2.
    1. Da Silva Cameiro M, Bermúdez I, Badia S, Duarte E, Verschure PFMJ. Virtual reality based rehabilitation speeds up functional recovery of the upper extremities after stroke: A randomized controlled pilot study in the acute phase of stroke using the Rehabilitation Gaming System. Restor Neurol Neurosci. 2011;29:287–98.
    1. Saposnik G, Teasell R, Mamdani M, Hall J, McIlroy W, Cheung D, et al. Effectiveness of virtual reality using wii gaming technology in stroke rehabilitation: A pilot randomized clinical trial and proof of principle. Stroke. 2010;41:1477–1484. doi: 10.1161/STROKEAHA.110.584979.
    1. Turolla A, Dam M, Ventura L, Tonin P, Agostini M, Zucconi C, et al. Virtual reality for the rehabilitation of the upper limb motor function after stroke: A prospective controlled trial. J Neuroeng Rehabil. 2013;10:85. doi: 10.1186/1743-0003-10-85.
    1. Laver KE, Lange B, George S, Deutsch JE, Saposnik G, Crotty M. Virtual reality for stroke rehabilitation. Cochrane Database Syst Rev. 2017;11(11):CD008349.
    1. Mancuso M, Damora A, Abbruzzese L, Navarrete E, Basagni B, Galardi G, et al. A new standardization of the Bells Test: An Italian multi-center normative study. Front Psychol. 2019;9:2745. doi: 10.3389/fpsyg.2018.02745.
    1. De Renzi E, Motti F, Nichelli P. Imitating Gestures: A Quantitative Approach to Ideomotor Apraxia. Arch Neurol. 1980;37:6–10. doi: 10.1001/archneur.1980.00500500036003.
    1. Mathiowetz V, Volland G, Kashman N, Weber K. Adult norms for the Box and Block Test of manual dexterity. Am J Occup Ther Off Publ Am Occup Ther Assoc. 1985;39:386–391. doi: 10.5014/ajot.39.6.386.
    1. Chen HM, Chen CC, Hsueh IP, Huang SL, Hsieh CL. Test-retest reproducibility and smallest real difference of 5 hand function tests in patients with stroke. Neurorehabil Neural Repair. 2009;23:435–440. doi: 10.1177/1545968308331146.
    1. Pandyan AD, Johnson GR, Price CIM, Curless RH, Barnes MP, Rodgers H. A review of the properties and limitations of the Ashworth and modified Ashworth Scales as measures of spasticity. Clin Rehabil. 1999;13:373–383. doi: 10.1191/026921599677595404.
    1. Bohannon RW, Smith MB. Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther. 1987;67:206–207. doi: 10.1093/ptj/67.2.206.
    1. Demeurisse G, Demol O, Robaye E. Motor evaluation in vascular hemiplegia. Eur Neurol. 1980;19:382–389. doi: 10.1159/000115178.
    1. Wilson JTL, Hareendran A, Hendry A, Potter J, Bone I, Muir KW. Reliability of the modified Rankin Scale across multiple raters: Benefits of a structured interview. Stroke. 2005;36:777–781. doi: 10.1161/01.STR.0000157596.13234.95.
    1. Shah S, Vanclay F, Cooper B. Improving the sensitivity of the Barthel Index for stroke rehabilitation. J Clin Epidemiol. 1989;42:703–709. doi: 10.1016/0895-4356(89)90065-6.
    1. Weller C, McNeil J. CONSORT 2010 statement: Updated guidelines can improve wound care. J Wound Care. 2010;19:347–353. doi: 10.12968/jowc.2010.19.8.77713.
    1. Schulz KF, Altman DG, Moher D. CONSORT 2010 Statement: Updated guidelines for reporting parallel group randomised trials. BMJ. 2010;340:698–702. doi: 10.1136/bmj.c332.

Source: PubMed

Patrocinadores e Colaboradores

Condições médicas

Intervenções de drogas

3
Se inscrever