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CC BY-NC-ND 4.0 · Arq Neuropsiquiatr 2018; 76(10): 654-662
DOI: 10.1590/0004-282X20180104
Article

Effects of virtual reality therapy on upper limb function after stroke and the role of neuroimaging as a predictor of a better response

Efeitos da terapia de realidade virtual na função do membro superior após AVC e o papel da neuroimagem como preditor de melhor resposta
Maicon Gabriel Gonçalves
1   Universidade Estadual Paulista, Faculdade de Medicina de Botucatu, Botucatu SP, Brasil;
,
Mariana Floriano Luiza Piva
1   Universidade Estadual Paulista, Faculdade de Medicina de Botucatu, Botucatu SP, Brasil;
,
Carlos Leonardo Sacomani Marques
1   Universidade Estadual Paulista, Faculdade de Medicina de Botucatu, Botucatu SP, Brasil;
,
Rafael Dalle Molle da Costa
1   Universidade Estadual Paulista, Faculdade de Medicina de Botucatu, Botucatu SP, Brasil;
,
Rodrigo Bazan
3   Universidade Estadual Paulista, Faculdade de Medicina de Botucatu, Departamento de Neurologia, Psicologia e Psiquiatria, Botucatu SP, Brasil.
,
Gustavo José Luvizutto
2   Universidade Federal do Triângulo Mineiro, Departamento de Fisioterapia Aplicada, Uberaba MG, Brasil;
,
Luiz Eduardo Gomes Garcia Betting
3   Universidade Estadual Paulista, Faculdade de Medicina de Botucatu, Departamento de Neurologia, Psicologia e Psiquiatria, Botucatu SP, Brasil.
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ABSTRACT

Background: Virtual reality therapy (VRT) is an interactive intervention that induces neuroplasticity. The aim was to evaluate the effects of VRT associated with conventional rehabilitation for an upper limb after stroke, and the neuroimaging predictors of a better response to VRT.

Methods: Patients with stroke were selected, and clinical neurological, upper limb function, and quality of life were evaluated. Statistical analysis was performed using a linear model comparing pre- and post-VRT. Lesions were segmented in the post-stroke computed tomography. A voxel-based lesion-symptom mapping approach was used to investigate the relationship between the lesion and upper limb function.

Results: Eighteen patients were studied (55.5 ± 13.9 years of age). Quality of life, functional independence, and dexterity of the upper limb showed improvement after VRT (p < 0.001). Neuroimaging analysis showed negative correlations between the internal capsule lesion and functional recovery.

Conclusion: VRT showed benefits for patients with stroke, but when there was an internal capsule lesion, a worse response was observed.

RESUMO

Introdução: A realidade virtual (RV) é uma intervenção interativa que induz a neuroplasticidade. O objetivo deste estudo foi avaliar os efeitos da RV associado à reabilitação convencional na função do membro superior após o AVC e as características preditores de neuroimagem de melhor resposta a esta terapia.

Métodos: os pacientes com AVC foram selecionados, e as características neurológicas, a função do membro superior e a qualidade de vida foram avaliadas. A análise estatística foi realizada por meio de modelo linear geral comparando resultados pré e pós-intervenção. As lesões foram segmentadas na tomografia computadorizada após o AVC. A abordagem de mapeamento da lesão-sintoma baseada em voxel foi utilizada para avaliar a relação entre a lesão e a função do membro superior.

Resultados: Foram estudados 18 pacientes (8 mulheres, 55,5 ± 13,9 anos). A qualidade de vida, independência funcional, características funcionais e destreza do membro superior apresentaram melhora após RV (p < 0,001). A análise de imagem mostrou correlações negativas principalmente entre a cápsula interna e a recuperação funcional do membro superior.

Conclusão: A RV mostrou benefícios para pacientes com AVC, mas quando houve lesão da cápsula interna apresentaram pior resposta à terapia.

Keywords:

Stroke - neuroimaging - virtual reality exposure therapy

Palavras-chave:

Acidente vascular cerebral - neuroimagem - terapia de exposição à realidade virtual

Support

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP). Processo 2016/17914-3.




Publication History

Received: 07 February 2018

Accepted: 29 June 2018

Article published online:
22 August 2023

© 2023. Academia Brasileira de Neurologia. This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commecial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/)

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  • References

  • 1 Sacco RL, Kasner SE, Broderick JP, Caplan LR, Connors JJ, Culebras A et al. An updated definition of stroke for the 21st century: a statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2013 Jul;44(7):2064-89. https://doi.org/10.1161/STR.0b013e318296aeca
  • 2 Abdul Aziz AF, Mohd Nordin NA, Ali MF, Abd Aziz NA, Sulong S, Aljunid SM. The integrated care pathway for post stroke patients (iCaPPS): a shared care approach between stakeholders in areas with limited access to specialist stroke care services. BMC Health Serv Res. 2017 Jan;17(1):35. https://doi.org/10.1186/s12913-016-1963-8
  • 3 Donnan GA, Fisher M, Macleod M, Davis SM. Stroke. Lancet. 2008 May;371(9624):1612-23. https://doi.org/10.1016/S0140-6736(08)60694-7
  • 4 Nijland RH, Wegen EE, Harmeling-Van Der Wel BC, Kwakkel G. Presence of finger extension and shoulder abduction within 72 hours after stroke: The EPOS cohort study stroke predicts functional recovery: Early prediction of functional outcome. Stroke. 2010;41(4):745-50. https://doi.org/10.1161/STROKEAHA.109.572065
  • 5 Saposnik G, Mamdani M, Bayley M, Thorpe KE, Hall J, Cohen LG et al. Effectiveness of Virtual Reality Exercises in STroke Rehabilitation (EVREST): rationale, design, and protocol of a pilot randomized clinical trial assessing the Wii gaming system. Int J Stroke. 2010 Feb;5(1):47-51. https://doi.org/10.1111/j.1747-4949.2009.00404.x
  • 6 Prochnow D, Bermúdez i Badia S, Schmidt J, Duff A, Brunheim S, Kleiser R et al. A functional magnetic resonance imaging study of visuomotor processing in a virtual reality-based paradigm: Rehabilitation Gaming System. Eur J Neurosci. 2013 May;37(9):1441-7. https://doi.org/10.1111/ejn.12157
  • 7 You SH, Jang SH, Kim YH, Hallett M, Ahn SH, Kwon YH et al. Virtual reality-induced cortical reorganization and associated locomotor recovery in chronic stroke: an experimenter-blind randomized study. Stroke. 2005 Jun;36(6):1166-71. https://doi.org/10.1161/01.STR.0000162715.43417.91
  • 8 Cameirão MS, Badia SB, Oller ED, Verschure PF. Neurorehabilitation using the virtual reality based rehabilitation gaming system: methodology, design, psychometrics, usability and validation. J Neuroeng Rehabil. 2010;7:48. https://doi.org/10.1186/1743-0003-7-48
  • 9 Good DC, Bettermann K, Reichwein RK. Stroke rehabilitation. Continuum (Minneap Minn). 2011;17(3 Neurorehabilitation):545-67. https://doi.org/10.1212/01.CON.0000399072.61943.38
  • 10 Harris JE, Eng JJ. Strength training improves upper-limb function in individuals with stroke: a meta-analysis. Stroke. 2010 Jan;41(1):136-40. https://doi.org/10.1161/STROKEAHA.109.567438
  • 11 Lange B, Koenig S, Chang CY, McConnell E, Suma E, Bolas M et al. Designing informed game-based rehabilitation tasks leveraging advances in virtual reality. Disabil Rehabil. 2012;34(22):1863-70. https://doi.org/10.3109/09638288.2012.670029
  • 12 Cameirão MS, Badia SB, Duarte E, Frisoli A, Verschure PF. The combined impact of virtual reality neurorehabilitation and its interfaces on upper extremity functional recovery in patients with chronic stroke. Stroke. 2012 Oct;43(10):2720-8. https://doi.org/10.1161/STROKEAHA.112.653196
  • 13 Saposnik G, Cohen LG, Mamdani M, Pooyania S, Ploughman M, Cheung D et al. Efficacy and safety of non-immersive virtual reality exercising in stroke rehabilitation (EVREST): a randomised, multicentre, single-blind, controlled trial. Lancet Neurol. 2016 Sep;15(10):1019-27. https://doi.org/10.1016/S1474-4422(16)30121-1
  • 14 Laver KE, Lange B, George S, Deutsch JE, Saposnik G, Crotty M. Virtual reality for stroke rehabilitation. Cochrane Database Syst Rev. 2017 Nov;11(11):CD008349. https://doi.org/10.1002/14651858.CD008349.pub2
  • 15 Aşkın A, Atar E, Koçyiğit H, Tosun A. Effects of Kinect-based virtual reality game training on upper extremity motor recovery in chronic stroke. Somatosens Mot Res. 2018 Mar;35(1):25-32. https://doi.org/10.1080/08990220.2018.1444599
  • 16 Kiper P, Szczudlik A, Agostini M, Opara J, Nowobilski R, Ventura L et al. Virtual reality for upper limb rehabilitation in subacute and chronic stroke: a randomized controlled trial. Arch Phys Med Rehabil. 2018 May;99(5):834-842.e4. https://doi.org/10.1016/j.apmr.2018.01.023
  • 17 Cincura C, Pontes-Neto OM, Neville IS, Mendes HF, Menezes DF, Mariano DC et al. Validation of the National Institutes of Health Stroke Scale, modified Rankin Scale and Barthel Index in Brazil: the role of cultural adaptation and structured interviewing. Cerebrovasc Dis. 2009;27(2):119-22. https://doi.org/10.1159/000177918
  • 18 Luvizutto GJ, Monteiro TA, Braga G, Pontes-Neto OM, Resende LAL, Bazan R. Validation of the scandinavian stroke scale in a multicultural population in Brazil. Cerebrovasc Dis Extra. 2012 Jan;2(1):121-6. https://doi.org/10.1159/000345948
  • 19 Gowland C, Stratford P, Ward M, Moreland J, Torresin W, Van Hullenaar S et al. Measuring physical impairment and disability with the Chedoke-McMaster Stroke Assessment. Stroke. 1993 Jan;24(1):58-63. https://doi.org/10.1161/01.STR.24.1.58
  • 20 Mathiowetz V, Volland G, Kashman N, Weber K. Adult norms for the Box and Block Test of manual dexterity. Am J Occup Ther. 1985 Jun;39(6):386-91. https://doi.org/10.5014/ajot.39.6.386
  • 21 Miller KJ, Slade AL, Pallant JF, Galea MP. Evaluation of the psychometric properties of the upper limb subscales of the Motor Assessment Scale using a Rasch analysis model. J Rehabil Med. 2010 Apr;42(4):315-22. https://doi.org/10.2340/16501977-0519
  • 22 Carod-Artal FJ, Coral LF, Trizotto DS, Moreira CM. The stroke impact scale 3.0: evaluation of acceptability, reliability, and validity of the Brazilian version. Stroke. 2008 Sep;39(9):2477-84. https://doi.org/10.1161/STROKEAHA.107.513671
  • 23 Yushkevich PA, Piven J, Hazlett HC, Smith RG, Ho S, Gee JC et al. User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage. 2006 Jul;31(3):1116-28. https://doi.org/10.1016/j.neuroimage.2006.01.015
  • 24 Rorden C, Bonilha L, Fridriksson J, Bender B, Karnath HO. Age-specific CT and MRI templates for spatial normalization. Neuroimage. 2012 Jul;61(4):957-65. https://doi.org/10.1016/j.neuroimage.2012.03.020
  • 25 Friston KJ, Penny WD, Ashburner JK, Stefan J, Nichols TE. Statistical parametric mapping: the analysis of functional brain images. London: Elsevier; 2006.
  • 26 Matlab. Statistics toolbox release. Natick: The Mathworks; 2012.
  • 27 Rorden C, Brett M. Stereotaxic display of brain lesions. Behav Neurol. 2000;12(4):191-200. https://doi.org/10.1155/2000/421719
  • 28 Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the mni MRI single-subject brain. 2002;15(1):273-89. https://doi.org/10.1006/nimg.2001.0978
  • 29 Mori S, Wakana S, Nagae-Poetscher LM, Zijl PCM. MRI Atlas of human white matter. Amsterdam: Elsevier; 2005.
  • 30 Bates E, Wilson SM, Saygin AP, Dick F, Sereno MI, Knight RT et al. Voxel-based lesion-symptom mapping. Nat Neurosci. 2003 May;6(5):448-50. https://doi.org/10.1038/nn1050
  • 31 Kleim JA, Jones TA. Principles of experience-dependent neural plasticity: implications for rehabilitation after brain damage. J Speech Lang Hear Res. 2008 Feb;51(1):S225-39. https://doi.org/10.1044/1092-4388(2008/018)
  • 32 Sisto SA, Forrest GF, Glendinning D. Virtual reality applications for motor rehabilitation after stroke. Top Stroke Rehabil. 2002;8(4):11-23. https://doi.org/10.1310/YABD-14KA-159P-MN6F
  • 33 Shumway-Cook A, Woollacott M. Motor control: theory and practical applications. 2nd ed. Maryland: Lippincott Williams & Wilkins; 2001.
  • 34 Eng K, Siekierka E, Pyk P, Chevrier E, Hauser Y, Cameirao M et al. Interactive visuo-motor therapy system for stroke rehabilitation. Med Biol Eng Comput. 2007 Sep;45(9):901-7. https://doi.org/10.1007/s11517-007-0239-1
  • 35 August K, Lewis JA, Chandar G, Merians A, Biswal B, Adamovich S. FMRI analysis of neural mechanisms underlying rehabilitation in virtual reality: activating secondary motor areas. Conf Proc IEEE Eng Med Biol Soc. 2006;1(1):3692-5. https://doi.org/10.1109/IEMBS.2006.260144
  • 36 Small SL, Buccino G, Solodkin A. The mirror neuron system and treatment of stroke. Dev Psychobiol. 2012 Apr;54(3):293-310. https://doi.org/10.1002/dev.20504
  • 37 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 Dec;46(4):517-23.
  • 38 Praamstra P, Torney L, Rawle CJ, Miall RC. Misconceptions about mirror-induced motor cortex activation. Cereb Cortex. 2011 Aug;21(8):1935-40. https://doi.org/10.1093/cercor/bhq270
  • 39 Reid D, Hirji T. The influence of a virtual reality leisure intervention program on the motivation of older adult stroke survivors: a pilot study. Phys Occup Ther Geriatr. 2004;21(4):1-19. https://doi.org/10.1080/J148v21n04_01
  • 40 Chao YY, Scherer YK, Montgomery CA. Effects of using Nintendo Wii™ exergames in older adults: a review of the literature. J Aging Health. 2015 Apr;27(3):379-402. https://doi.org/10.1177/0898264314551171
  • 41 Yang M, Yang YR, Li HJ, Lu XS, Shi YM, Liu B et al. Combining diffusion tensor imaging and gray matter volumetry to investigate motor functioning in chronic stroke. PLoS One. 2015 May;10(5):e0125038. https://doi.org/10.1371/journal.pone.0125038
  • 42 Barlow SJ. Identifying the brain regions associated with acute spasticity in patients diagnosed with an ischemic stroke. Somatosens Mot Res. 2016 Jun;33(2):104-11. https://doi.org/10.1080/08990220.2016.1197114
  • 43 Puentes S, Kaido T, Hanakawa T, Ichinohe N, Otsuki T, Seki K. Internal capsule stroke in the common marmoset. Neuroscience. 2015 Jan;284(284):400-11. https://doi.org/10.1016/j.neuroscience.2014.10.015