Virtual reality for the upper limb motor rehabilitation after stroke_West China Medical Journal

Authors：

ZHU Shijie ¹ , LIN Shuyan ² , XU Shiying ² ,  YANG Yonghong ^1,3

1. Department of Rehabilitation Medicine, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;
2. West China School of Medicine, Sichuan University, Chengdu, Sichuan 610041, P. R. China;
3. Key Laboratory of Rehabilitation Medicine in Sichuan Province, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;

Corresponding author：

YANG Yonghong, Email: Nicole308@126.com

Keywords：

Virtual reality; Stroke; Rehabilitation; Upper limbs

DOI：

10.7507/1002-0179.201912179

Video：

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Stroke can lead to dysfunction of movement, sensation, cognition and other functions, eventually affect the quality of life of patients. Many patients suffer from severe and persistent upper limb dysfunction. Upper limb rehabilitation has always been a focus in clinical practice and scientific research of rehabilitation field. As an emerging technology, virtual reality (VR) provides simulated environments for patients to enhance their participation and experience, and has been more and more widely used in stroke rehabilitation. This paper reviews the application and research progress of VR in upper limb rehabilitation after stroke, discusses the current evidences based on both the independent application of VR and the application of VR combined with other rehabilitation interventions, and indicates that VR can play a positive role in promoting the upper limb strength and coordination of stroke patients and enhancing their motivation to participant in rehabilitation. In the future, more high-quality studies are needed to further confirm the efficacy and optimal parameter settings.

Citation： ZHU Shijie, LIN Shuyan, XU Shiying, YANG Yonghong. Virtual reality for the upper limb motor rehabilitation after stroke. West China Medical Journal, 2021, 36(8): 1120-1125. doi: 10.7507/1002-0179.201912179 Copy

1.	王陇德, 刘建民, 杨弋, 等. 《中国脑卒中防治报告 2018》概要. 中国循环杂志, 2019, 34: 105-119.
2.	Zhang T, Zhao J, Li X, et al. Chinese Stroke Association guidelines for clinical management of cerebrovascular disorders: executive summary and 2019 update of clinical management of stroke rehabilitation. Stroke Vasc Neurol, 2020, 5(3): 250-259.
3.	Rand D, Eng JJ. Disparity between functional recovery and daily use of the upper and lower extremities during subacute stroke rehabilitation. Neurorehabil Neural Repair, 2012, 26(1): 76-84.
4.	Langhorne P, Bernhardt J, Kwakkel G. Stroke rehabilitation. Lancet, 2011, 377(9778): 1693-1702.
5.	Veerbeek JM, van Wegen E, van Peppen R, et al. What is the evidence for physical therapy poststroke? A systematic review and meta-analysis. PLoS One, 2014, 9(2): e87987.
6.	Risedal A, Mattsson B, Dahlqvist P, et al. Environmental influences on functional outcome after a cortical infarct in the rat. Brain Res Bull, 2002, 58(3): 315-321.
7.	Lewis GN, Rosie JA. Virtual reality games for movement rehabilitation in neurological conditions: how do we meet the needs and expectations of the users?. Disabil Rehabil, 2012, 34(22): 1880-1886.
8.	Ikbali Afsar S, Mirzayev I, Umit Yemisci O, et al. Virtual reality in upper extremity rehabilitation of stroke patients: a randomized controlled trial. J Stroke Cerebrovasc Dis, 2018, 27(12): 3473-3478.
9.	You S, Jang S, Kim Y, et al. Virtual reality-induced cortical reorganization and associated locomotor recovery in chronic stroke: an experimenter-blind randomized study. Stroke, 2005, 36(6): 1166-1171.
10.	Choi YH, Paik NJ. Mobile game-based virtual reality program for upper extremity stroke rehabilitation. J Vis Exp, 2018(133): e56241.
11.	Tunik E, Saleh S, Adamovich SV. Visuomotor discordance during visually-guided hand movement in virtual reality modulates sensorimotor cortical activity in healthy and hemiparetic subjects. IEEE Trans Neural Syst Rehabil Eng, 2013, 21(2): 198-207.
12.	Bagce HF, Saleh S, Adamovich SV, et al. Visuomotor gain distortion alters online motor performance and enhances primary motor cortex excitability in patients with stroke. Neuromodulation, 2012, 15(4): 361-366.
13.	Simsek T, Cekok K. The effects of Nintendo WiiT M-based balance and upper extremity training on activities of daily living and quality of life in patients with sub-acute stroke: a randomized controlled study. Int J Neurosci, 2016, 126(12): 61-70.
14.	Lohse KR, Hilderman CG, Cheung KL, et al. Virtual reality therapy for adults post-stroke: a systematic review and meta-analysis exploring virtual environments and commercial games in therapy. PLoS One, 2014, 9(3): e93318.
15.	Mumford N, Duckworth J, Thomas PR, et al. Upper-limb virtual rehabilitation for traumatic brain injury: a preliminary within-group evaluation of the elements system. Brain Inj, 2012, 26(2): 166-176.
16.	Laver KE, George S, Thomas S, et al. Virtual reality for stroke rehabilitation. Cochrane Database Syst Rev, 2015, 2015(2): CD008349.
17.	Kim WS, Cho S, Park SH, et al. A low cost kinect-based virtual rehabilitation system for inpatient rehabilitation of the upper limb in patients with subacute stroke: a randomized, double-blind, sham-controlled pilot trial. Medicine, 2018, 97(25): e11173.
18.	Zhang H, Austin H, Buchanan S, et al. Feasibility studies of robot-assisted stroke rehabilitation at clinic and home settings using RUPERT. IEEE Int Conf Rehabil Robot, 2011(7/8): 5975440.
19.	Cao S, Kazuki N, Quan C, et al. On robotic rehabilitation of human dual arms’ coornative function. Int J Appl Electrom Mechan, 2016, 52(3/4): 943-950.
20.	Zhang YB, Wang ZX, Ji LH, et al. The clinical application of the upper limb extremity compound movements rehabilitation training robots//9th international conference an rehabilitation robotics. Chicago: IEEE, 2005: 91-94.
21.	Aminov A, Rogers JM, Middleton S, et al. What do randomized controlled trials say about virtual rehabilitation in stroke? A systematic literature review and meta-analysis of upper-limb and cognitive outcomes. J Neuroeng Rehabil, 2018, 15(1): 29-25.
22.	Matt C, Howard. A meta-analysis and systematic literature review of virtual reality rehabilitation programs. Comput Human Behav, 2017, 70: 317-327.
23.	Norouzi-Gheidari N, Archambault PS, Fung J. Effects of robot-assisted therapy on stroke rehabilitation in upper limbs: systematic review and meta-analysis of the literature. J Rehabil Res Dev, 2012, 49(4): 479-496.
24.	Park DS, Lee DG, Lee K, et al. Effects of virtual reality training using Xbox kinect on motor function in stroke survivors: a preliminary study. J Stroke Cerebrovasc Dis, 2017, 26(10): 2313-2319.
25.	Lee S, Kim Y, Lee BH. Effect of virtual reality-based bilateral upper extremity training on upper extremity function after stroke: a randomized controlled clinical trial. Occup Ther Int, 2016, 23(4): 357-368.
26.	官娉, 陈妍, 张韶辉. 虚拟现实技术对脑卒中患者偏瘫上肢肱二肌和肱三头肌表面肌电的影响. 临床和实验医学杂志, 2018, 3(3): 324-327.
27.	Schuster-Amft C, Eng K, Suica Z, et al. Effect of a four-week virtual reality-based training versus conventional therapy on upper limb motor function after stroke: a multicenter parallel group randomized trial. PLoS One, 2018, 13(10): e0204455.
28.	Vourvopoulos A, Pardo OM, Lefebvre S, et al. Effects of a brain-computer interface with virtual reality (VR) neurofeedback: a pilot study in chronic stroke patients. Front Hum Neurosci, 2019, 13: 210.
29.	Lee G. Effects of training using video games on the muscle strength, muscle tone, and activities of daily living of chronic stroke patients. J Phys Ther Sci, 2013, 25(5): 595-597.
30.	Singh DK, Mohd NN, Abd AA, et al. Effects of substituting a portion of standard physiotherapy time with virtual reality games among community-dwelling stroke survivors. BMC Neurol, 2013, 13(1): 199-205.
31.	Lee HS, Park YJ, Park SW. The effects of virtual reality training on function in chronic stroke patients: a systematic review and meta-analysis. Biomed Res Int, 2019, 2019: 7595639.
32.	Bedwell WL, Pavlas D, Heyne K, et al. Toward a taxonomy linking game attributes to learning an empirical study. Simul Gaming, 2012, 43(6): 729-760.
33.	郑婵娟, 杨英武, 夏文广, 等. 虚拟情景互动训练结合作业疗法对脑卒中患者上肢功能恢复的影响. 中华物理医学与康复杂志, 2014, 36(5): 360-362.
34.	Dimbwadyo-Terrer I, Gil-Agudo A, Segura-Fragoso A, et al. Effectiveness of the virtual reality system toyra on upper limb function in people with tetraplegia: a pilot randomized clinical trial. Biomed Res Int, 2016, 2016: 6397828.
35.	Iosa M, Morone G, Fusco A, et al. Leap motion controlled videogame-based therapy for rehabilitation of elderly patients with subacute stroke: a feasibility pilot study. Top Stroke Rehabil, 2015, 22(4): 306-316.
36.	Charles D, Holmes D, Charles T, et al. Virtual reality design for stroke rehabilitation. Adv Exp Med Biol, 2020, 1235: 53-87.
37.	Rohrbach N, Chicklis E, Levac D. What is the impact of user affect on motor learning in virtual environments after stroke? A scoping review. J Neuroeng Rehabil, 2019, 16(1): 79-92.
38.	Yu N, Xu C, Li H, et al. Fusion of haptic and gesture sensors for rehabilitation of bimanual coordination and dexterous manipulation. Sensors (Basel), 2016, 16(3): 395-414.
39.	Winstein CJ, Stein J, Arena R, et al. Guidelines for adult stroke rehabilitation and recovery: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke, 2016, 47(6): e98-e169.
40.	Invernizzi M, Negrini S, Carda S, et al. The value of adding mirror therapy for upper limb motor recovery of subacute stroke patients: a randomized controlled trial. Eur J Phys Rehabil Med, 2013, 49(3): 311-317.
41.	Choi HS, Shin WS, Bang DH. Mirror therapy using gesture recognition for upper limb function, neck discomfort, and quality of life after chronic stroke: a single-blind randomized controlled trial. Med Sci Monit, 2019, 25(10): 3271-3278.
42.	Weber LM, Nilsen DM, Gillen G, et al. Immersive virtual reality mirror therapy for upper limb recovery after stroke: a pilot study. Am J Phys Med Rehabil, 2019, 98(9): 783-788.
43.	Bassolino M, Franza M, Bello RJ, et al. Non-invasive brain stimulation of motor cortex induces embodiment when integrated with virtual reality feedback. Eur J Neurosci, 2018, 47(7): 790-799.
44.	Avenanti A, Coccia M, Ladavas E, et al. Low-frequency rTMS promotes use-dependent motor plasticity in chronic stroke: a randomized trial. Neurology, 2012, 78(4): 256-264.
45.	崔海超, 翟宏伟, 张明, 等. 虚拟现实技术联合重复经颅磁刺激对脑卒中偏瘫患者上肢运动功能的影响. 临床与病理杂志, 2017, 37(11): 2439-2444.
46.	Housman SJ, Scott KM, Reinkensmeyer DJ. A randomized controlled trial of gravity-supported, computer-enhanced arm exercise for individuals with severe hemiparesis. Neurorehabil Neural Repair, 2009, 23(5): 505-514.
47.	Rogers JM, Duckworth J, Middleton S, et al. Elements virtual rehabilitation improves motor, cognitive, and functional outcomes in adult stroke: evidence from a randomized controlled pilot study. J Neuroeng Rehabil, 2019, 16(1): 56.
48.	Perez-Marcos D, Chevalley O, Schmidlin T, et al. Increasing upper limb training intensity in chronic stroke using embodied virtual reality: a pilot study. J Neuroeng Rehabil, 2017, 14(1): 119-132.
49.	Palma GC, Freitas TB, Bonuzzi GM, et al. Effects of virtual reality for stroke individuals based on the International Classification of Functioning and Health: a systematic review. Top Stroke Rehabil, 2017, 24(4): 269-278.
50.	Muratori LM, Lamberg EM, Quinn L, et al. Applying principles of motor learning and control to upper extremity rehabilitation. J Hand Ther, 2013, 26(2): 94-102.
51.	Winstein CJ, Wolf SL, Dromerick AW, et al. Effect of a task-oriented rehabilitation program on upper extremity recovery following motor stroke: the ICARE randomized clinical trial. JAMA, 2016, 315(6): 571-581.

1. 王陇德, 刘建民, 杨弋, 等. 《中国脑卒中防治报告 2018》概要. 中国循环杂志, 2019, 34: 105-119.
2. Zhang T, Zhao J, Li X, et al. Chinese Stroke Association guidelines for clinical management of cerebrovascular disorders: executive summary and 2019 update of clinical management of stroke rehabilitation. Stroke Vasc Neurol, 2020, 5(3): 250-259.
3. Rand D, Eng JJ. Disparity between functional recovery and daily use of the upper and lower extremities during subacute stroke rehabilitation. Neurorehabil Neural Repair, 2012, 26(1): 76-84.
4. Langhorne P, Bernhardt J, Kwakkel G. Stroke rehabilitation. Lancet, 2011, 377(9778): 1693-1702.
5. Veerbeek JM, van Wegen E, van Peppen R, et al. What is the evidence for physical therapy poststroke? A systematic review and meta-analysis. PLoS One, 2014, 9(2): e87987.
6. Risedal A, Mattsson B, Dahlqvist P, et al. Environmental influences on functional outcome after a cortical infarct in the rat. Brain Res Bull, 2002, 58(3): 315-321.
7. Lewis GN, Rosie JA. Virtual reality games for movement rehabilitation in neurological conditions: how do we meet the needs and expectations of the users?. Disabil Rehabil, 2012, 34(22): 1880-1886.
8. Ikbali Afsar S, Mirzayev I, Umit Yemisci O, et al. Virtual reality in upper extremity rehabilitation of stroke patients: a randomized controlled trial. J Stroke Cerebrovasc Dis, 2018, 27(12): 3473-3478.
9. You S, Jang S, Kim Y, et al. Virtual reality-induced cortical reorganization and associated locomotor recovery in chronic stroke: an experimenter-blind randomized study. Stroke, 2005, 36(6): 1166-1171.
10. Choi YH, Paik NJ. Mobile game-based virtual reality program for upper extremity stroke rehabilitation. J Vis Exp, 2018(133): e56241.
11. Tunik E, Saleh S, Adamovich SV. Visuomotor discordance during visually-guided hand movement in virtual reality modulates sensorimotor cortical activity in healthy and hemiparetic subjects. IEEE Trans Neural Syst Rehabil Eng, 2013, 21(2): 198-207.
12. Bagce HF, Saleh S, Adamovich SV, et al. Visuomotor gain distortion alters online motor performance and enhances primary motor cortex excitability in patients with stroke. Neuromodulation, 2012, 15(4): 361-366.
13. Simsek T, Cekok K. The effects of Nintendo WiiT M-based balance and upper extremity training on activities of daily living and quality of life in patients with sub-acute stroke: a randomized controlled study. Int J Neurosci, 2016, 126(12): 61-70.
14. Lohse KR, Hilderman CG, Cheung KL, et al. Virtual reality therapy for adults post-stroke: a systematic review and meta-analysis exploring virtual environments and commercial games in therapy. PLoS One, 2014, 9(3): e93318.
15. Mumford N, Duckworth J, Thomas PR, et al. Upper-limb virtual rehabilitation for traumatic brain injury: a preliminary within-group evaluation of the elements system. Brain Inj, 2012, 26(2): 166-176.
16. Laver KE, George S, Thomas S, et al. Virtual reality for stroke rehabilitation. Cochrane Database Syst Rev, 2015, 2015(2): CD008349.
17. Kim WS, Cho S, Park SH, et al. A low cost kinect-based virtual rehabilitation system for inpatient rehabilitation of the upper limb in patients with subacute stroke: a randomized, double-blind, sham-controlled pilot trial. Medicine, 2018, 97(25): e11173.
18. Zhang H, Austin H, Buchanan S, et al. Feasibility studies of robot-assisted stroke rehabilitation at clinic and home settings using RUPERT. IEEE Int Conf Rehabil Robot, 2011(7/8): 5975440.
19. Cao S, Kazuki N, Quan C, et al. On robotic rehabilitation of human dual arms’ coornative function. Int J Appl Electrom Mechan, 2016, 52(3/4): 943-950.
20. Zhang YB, Wang ZX, Ji LH, et al. The clinical application of the upper limb extremity compound movements rehabilitation training robots//9th international conference an rehabilitation robotics. Chicago: IEEE, 2005: 91-94.
21. Aminov A, Rogers JM, Middleton S, et al. What do randomized controlled trials say about virtual rehabilitation in stroke? A systematic literature review and meta-analysis of upper-limb and cognitive outcomes. J Neuroeng Rehabil, 2018, 15(1): 29-25.
22. Matt C, Howard. A meta-analysis and systematic literature review of virtual reality rehabilitation programs. Comput Human Behav, 2017, 70: 317-327.
23. Norouzi-Gheidari N, Archambault PS, Fung J. Effects of robot-assisted therapy on stroke rehabilitation in upper limbs: systematic review and meta-analysis of the literature. J Rehabil Res Dev, 2012, 49(4): 479-496.
24. Park DS, Lee DG, Lee K, et al. Effects of virtual reality training using Xbox kinect on motor function in stroke survivors: a preliminary study. J Stroke Cerebrovasc Dis, 2017, 26(10): 2313-2319.
25. Lee S, Kim Y, Lee BH. Effect of virtual reality-based bilateral upper extremity training on upper extremity function after stroke: a randomized controlled clinical trial. Occup Ther Int, 2016, 23(4): 357-368.
26. 官娉, 陈妍, 张韶辉. 虚拟现实技术对脑卒中患者偏瘫上肢肱二肌和肱三头肌表面肌电的影响. 临床和实验医学杂志, 2018, 3(3): 324-327.
27. Schuster-Amft C, Eng K, Suica Z, et al. Effect of a four-week virtual reality-based training versus conventional therapy on upper limb motor function after stroke: a multicenter parallel group randomized trial. PLoS One, 2018, 13(10): e0204455.
28. Vourvopoulos A, Pardo OM, Lefebvre S, et al. Effects of a brain-computer interface with virtual reality (VR) neurofeedback: a pilot study in chronic stroke patients. Front Hum Neurosci, 2019, 13: 210.
29. Lee G. Effects of training using video games on the muscle strength, muscle tone, and activities of daily living of chronic stroke patients. J Phys Ther Sci, 2013, 25(5): 595-597.
30. Singh DK, Mohd NN, Abd AA, et al. Effects of substituting a portion of standard physiotherapy time with virtual reality games among community-dwelling stroke survivors. BMC Neurol, 2013, 13(1): 199-205.
31. Lee HS, Park YJ, Park SW. The effects of virtual reality training on function in chronic stroke patients: a systematic review and meta-analysis. Biomed Res Int, 2019, 2019: 7595639.
32. Bedwell WL, Pavlas D, Heyne K, et al. Toward a taxonomy linking game attributes to learning an empirical study. Simul Gaming, 2012, 43(6): 729-760.
33. 郑婵娟, 杨英武, 夏文广, 等. 虚拟情景互动训练结合作业疗法对脑卒中患者上肢功能恢复的影响. 中华物理医学与康复杂志, 2014, 36(5): 360-362.
34. Dimbwadyo-Terrer I, Gil-Agudo A, Segura-Fragoso A, et al. Effectiveness of the virtual reality system toyra on upper limb function in people with tetraplegia: a pilot randomized clinical trial. Biomed Res Int, 2016, 2016: 6397828.
35. Iosa M, Morone G, Fusco A, et al. Leap motion controlled videogame-based therapy for rehabilitation of elderly patients with subacute stroke: a feasibility pilot study. Top Stroke Rehabil, 2015, 22(4): 306-316.
36. Charles D, Holmes D, Charles T, et al. Virtual reality design for stroke rehabilitation. Adv Exp Med Biol, 2020, 1235: 53-87.
37. Rohrbach N, Chicklis E, Levac D. What is the impact of user affect on motor learning in virtual environments after stroke? A scoping review. J Neuroeng Rehabil, 2019, 16(1): 79-92.
38. Yu N, Xu C, Li H, et al. Fusion of haptic and gesture sensors for rehabilitation of bimanual coordination and dexterous manipulation. Sensors (Basel), 2016, 16(3): 395-414.
39. Winstein CJ, Stein J, Arena R, et al. Guidelines for adult stroke rehabilitation and recovery: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke, 2016, 47(6): e98-e169.
40. Invernizzi M, Negrini S, Carda S, et al. The value of adding mirror therapy for upper limb motor recovery of subacute stroke patients: a randomized controlled trial. Eur J Phys Rehabil Med, 2013, 49(3): 311-317.
41. Choi HS, Shin WS, Bang DH. Mirror therapy using gesture recognition for upper limb function, neck discomfort, and quality of life after chronic stroke: a single-blind randomized controlled trial. Med Sci Monit, 2019, 25(10): 3271-3278.
42. Weber LM, Nilsen DM, Gillen G, et al. Immersive virtual reality mirror therapy for upper limb recovery after stroke: a pilot study. Am J Phys Med Rehabil, 2019, 98(9): 783-788.
43. Bassolino M, Franza M, Bello RJ, et al. Non-invasive brain stimulation of motor cortex induces embodiment when integrated with virtual reality feedback. Eur J Neurosci, 2018, 47(7): 790-799.
44. Avenanti A, Coccia M, Ladavas E, et al. Low-frequency rTMS promotes use-dependent motor plasticity in chronic stroke: a randomized trial. Neurology, 2012, 78(4): 256-264.
45. 崔海超, 翟宏伟, 张明, 等. 虚拟现实技术联合重复经颅磁刺激对脑卒中偏瘫患者上肢运动功能的影响. 临床与病理杂志, 2017, 37(11): 2439-2444.
46. Housman SJ, Scott KM, Reinkensmeyer DJ. A randomized controlled trial of gravity-supported, computer-enhanced arm exercise for individuals with severe hemiparesis. Neurorehabil Neural Repair, 2009, 23(5): 505-514.
47. Rogers JM, Duckworth J, Middleton S, et al. Elements virtual rehabilitation improves motor, cognitive, and functional outcomes in adult stroke: evidence from a randomized controlled pilot study. J Neuroeng Rehabil, 2019, 16(1): 56.
48. Perez-Marcos D, Chevalley O, Schmidlin T, et al. Increasing upper limb training intensity in chronic stroke using embodied virtual reality: a pilot study. J Neuroeng Rehabil, 2017, 14(1): 119-132.
49. Palma GC, Freitas TB, Bonuzzi GM, et al. Effects of virtual reality for stroke individuals based on the International Classification of Functioning and Health: a systematic review. Top Stroke Rehabil, 2017, 24(4): 269-278.
50. Muratori LM, Lamberg EM, Quinn L, et al. Applying principles of motor learning and control to upper extremity rehabilitation. J Hand Ther, 2013, 26(2): 94-102.
51. Winstein CJ, Wolf SL, Dromerick AW, et al. Effect of a task-oriented rehabilitation program on upper extremity recovery following motor stroke: the ICARE randomized clinical trial. JAMA, 2016, 315(6): 571-581.

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Virtual reality for the upper limb motor rehabilitation after stroke

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