Immersive virtual reality to assess unilateral spatial neglect in stroke patients: a preliminary study
DOI:
https://doi.org/10.2340/jrm.v57.41195Keywords:
Neglect, stroke, cancellation test, virtual realityAbstract
Objectives: The conventional test to detect unilateral spatial neglect (USN) is the Bells Test performed in a paper-and-pencil format. While several studies showed immersive virtual reality (VR) tests may provide greater sensitivity in revealing the presence of USN using visual scanning tasks, none has investigated the Bells Test in VR. This study compares the Bells Test performed in paper-and-pencil format (PP) and in VR in conventional (CVR) and ecological (EVR) format, which differ by the size of the display, in stroke patients.
Design: Cross-sectional study.
Setting: Stroke patients.
Participants: A convenience sample of 32 stroke patients.
Interventions: VR assessments were performed using an immersive system with a head-mounted display. In CVR, the Bells Test is reproduced in the same format as PP (A4 sheet), while in EVR, the targets are displayed in a wider space corresponding to a hemisphere of 1-m radius.
Results: The number of cancelled targets out of 35 was 32.5 (3.5) for PP, 33 (4) for CVR, and 34 (2) for EVR (mean [SD]), with a significant difference between PP and EVR (p < 0.05). The time to complete the Bells Test was 186 (69) s for PP, 184 (65) s for CVR, and 170 (58) s for EVR, without differences between modalities (p > 0.05). Bells Tests in the 3 modalities revealed the presence of USN, except for 1 patient in EVR.
Conclusion: VR assessment of USN could be used in the same way as conventional cancellations tests. Moreover, VR could provide additional information on the type of USN through the different testing modalities available.
Downloads
References
Heilman KM, Valenstein E. Mechanisms underlying hemispatial neglect. Ann Neurol 1979; 5: 166‑170.
https://doi.org/10.1002/ana.410050210 DOI: https://doi.org/10.1002/ana.410050210
Sobrinho KRF, Santini ACM, Marques CLS, Gabriel MG, Neto E de M, de Souza LAPS, et al. Impact of unilateral spatial neglect on chronic patient's post-stroke quality of life. Somatosens Mot Res 2018; 35: 199‑203.
https://doi.org/10.1080/08990220.2018.1521791 DOI: https://doi.org/10.1080/08990220.2018.1521791
Esposito E, Shekhtman G, Chen P. Prevalence of spatial neglect post-stroke: A systematic review. Ann Phys Rehabil Med 2021; 64: 101459.
https://doi.org/10.1016/j.rehab.2020.10.010 DOI: https://doi.org/10.1016/j.rehab.2020.10.010
Rode G, Pagliari C, Huchon L, Rossetti Y, Pisella L. Semiology of neglect: an update. Ann Phys Rehabil Med 2017; 60: 177‑185.
https://doi.org/10.1016/j.rehab.2016.03.003 DOI: https://doi.org/10.1016/j.rehab.2016.03.003
Gammeri R, Iacono C, Ricci R, Salatino A. Unilateral spatial neglect after stroke: current insights. Neuropsychiatr Dis Treat 2020; 16: 131‑152.
https://doi.org/10.2147/NDT.S171461 DOI: https://doi.org/10.2147/NDT.S171461
Williams LJ, Kernot J, Hillier SL, Loetscher T. Spatial neglect subtypes, definitions and assessment tools: a scoping review. Front Neurol 2021; 12: 742365.
https://doi.org/10.3389/fneur.2021.742365 DOI: https://doi.org/10.3389/fneur.2021.742365
Giannakou I, Lin D, Punt D. Computer-based assessment of unilateral spatial neglect: a systematic review. Front Neurosci 2022; 16: 912626.
https://doi.org/10.3389/fnins.2022.912626 DOI: https://doi.org/10.3389/fnins.2022.912626
Guilbert A. Clinical assessment of unilateral spatial neglect dissociations and heterogeneities: A narrative synthesis. Neuropsychology 2023; 37: 450‑462.
https://doi.org/10.1037/neu0000841 DOI: https://doi.org/10.1037/neu0000841
Azouvi P. The ecological assessment of unilateral neglect. Ann Phys Rehabil Med 2017; 60: 186‑190.
https://doi.org/10.1016/j.rehab.2015.12.005 DOI: https://doi.org/10.1016/j.rehab.2015.12.005
Halligan PW, Marshall JC, Wade DT. Visuospatial neglect: underlying factors and test sensitivity. Lancet Lond Engl 1989; 2: 908‑911.
https://doi.org/10.1016/S0140-6736(89)91561-4 DOI: https://doi.org/10.1016/S0140-6736(89)91561-4
Albert ML. A simple test of visual neglect. Neurology 1973; 23: 658‑664.
https://doi.org/10.1212/WNL.23.6.658 DOI: https://doi.org/10.1212/WNL.23.6.658
Halligan P, Wilson B, Cockburn J. A short screening test for visual neglect in stroke patients. Int Disabil Stud 1990; 12: 95‑99.
https://doi.org/10.3109/03790799009166260 DOI: https://doi.org/10.3109/03790799009166260
Gauthier L, Dehaut F, Joanette Y. The Bells Test: A quantitative and qualitative test for visual neglect. Int J Clin Neuropsychol 1989; 11: 49‑54.
https://doi.org/10.1037/t28075-000 DOI: https://doi.org/10.1037/t28075-000
Terruzzi S, Albini F, Massetti G, Etzi R, Gallace A, Vallar G. The neuropsychological assessment of unilateral spatial neglect through computerized and virtual reality tools: a scoping review. Neuropsychol Rev 2024; 34: 363‑401.
https://doi.org/10.1007/s11065-023-09586-3 DOI: https://doi.org/10.1007/s11065-023-09586-3
Aimola L, Schindler I, Venneri A. Task- and response related dissociations between neglect in near and far space: a morphometric case study. Behav Neurol 2013; 27: 245‑257.
https://doi.org/10.1155/2013/198460 DOI: https://doi.org/10.1155/2013/198460
Mazurek J, Kiper P, Cieślik B, Rutkowski S, Mehlich K, Turolla A, et al. Virtual reality in medicine: a brief overview and future research directions. Hum Mov 2019; 20: 16‑22.
https://doi.org/10.5114/hm.2019.83529 DOI: https://doi.org/10.5114/hm.2019.83529
Jäncke L, Cheetham M, Baumgartner T. Virtual reality and the role of the prefrontal cortex in adults and children. Front Neurosci 2009; 3: 52‑59.
https://doi.org/10.3389/neuro.01.006.2009 DOI: https://doi.org/10.3389/neuro.01.006.2009
Slobounov SM, Ray W, Johnson B, Slobounov E, Newell KM. Modulation of cortical activity in 2D versus 3D virtual reality environments: an EEG study. Int J Psychophysiol Off J Int Organ Psychophysiol 2015; 95: 254‑260.
https://doi.org/10.1016/j.ijpsycho.2014.11.003 DOI: https://doi.org/10.1016/j.ijpsycho.2014.11.003
Chen J, Or Ck, Chen T. Effectiveness of using virtual reality-supported exercise therapy for upper extremity motor rehabilitation in patients with stroke: systematic review and meta-analysis of randomized controlled trials. J Med Internet Res 2022; 24: e24111.
https://doi.org/10.2196/24111 DOI: https://doi.org/10.2196/24111
Tsirlin I, Dupierrix E, Chokron S, Coquillart S, Ohlmann T. Uses of virtual reality for diagnosis, rehabilitation and study of unilateral spatial neglect: review and analysis. Cyberpsychology Behav Impact Internet Multimed Virtual Real Behav Soc 2009; 12: 175‑181.
https://doi.org/10.1089/cpb.2008.0208 DOI: https://doi.org/10.1089/cpb.2008.0208
Jannink MJA, Aznar M, de Kort AC, van de Vis W, Veltink P, van der Kooij H. Assessment of visuospatial neglect in stroke patients using virtual reality: a pilot study. Int J Rehabil Res Int Z Rehabil Rev Int Rech Readaptation 2009; 32: 280‑286.
https://doi.org/10.1097/MRR.0b013e3283013b1c DOI: https://doi.org/10.1097/MRR.0b013e3283013b1c
Kim K, Kim J, Ku J, Kim DY, Chang WH, Shin DI, et al. A virtual reality assessment and training system for unilateral neglect. Cyberpsychology Behav Impact Internet Multimed Virtual Real Behav Soc 2004; 7: 742‑749.
https://doi.org/10.1089/cpb.2004.7.742 DOI: https://doi.org/10.1089/cpb.2004.7.742
Myers RL, Bierig T. Virtual reality and left hemineglect: A technology for assessment and therapy. Cyberpsychol Behav 2000; 3: 465‑468.
https://doi.org/10.1089/10949310050078922 DOI: https://doi.org/10.1089/10949310050078922
Folstein MF, Robins LN, Helzer JE. The mini-mental state examination. Arch Gen Psychiatry 1983; 40: 812.
https://doi.org/10.1001/archpsyc.1983.01790060110016 DOI: https://doi.org/10.1001/archpsyc.1983.01790060110016
Bergego C, Azouvi P, Samuel C, Marchal F, Louis-Dreyfus A, Jokic C, et al. Validation d'une échelle d'évaluation fonctionnelle de l'héminégligence dans la vie quotidienne: l'échelle CB. Ann Réadapt Médecine Phys 1995; 38: 183‑189.
https://doi.org/10.1016/0168-6054(96)89317-2 DOI: https://doi.org/10.1016/0168-6054(96)89317-2
Pflueger M, Gschwandtner U. Testbatterie zur Aufmerksamkeitsprüfung (TAP) Version1.7. Z Klin Psychol Psychother - Z Klin Psychol Psychother 2003; 32: 155‑157.
https://doi.org/10.1026//1616-3443.32.2.155 DOI: https://doi.org/10.1026//1616-3443.32.2.155
Azouvi P, Bartolomeo P, Beis Jm, Perennou D, Pradat-Diehl P, Rousseaux M. A battery of tests for the quantitative assessment of unilateral neglect. Restor Neurol Neurosci 2006; 24: 273-285. DOI: https://doi.org/10.3233/RNN-2006-00351
Hyzy M, Bond R, Mulvenna M, Bai L, Dix A, Leigh S, et al. System usability scale benchmarking for digital health apps: meta-analysis. JMIR MHealth UHealth 2022; 10: e37290.
https://doi.org/10.2196/37290 DOI: https://doi.org/10.2196/37290
Rousseaux M, Beis JM, Pradat-Diehl P, Martin Y, Bartolomeo P, Bernati T, et al. Presenting a battery for assessing spatial neglect. Norms and effects of age, educational level, sex, hand and laterality. Rev Neurol 2001; 157: 1385‑1400.
Ogourtsova T, Souza Silva W, Archambault PS, Lamontagne A. Virtual reality treatment and assessments for post-stroke unilateral spatial neglect: a systematic literature review. Neuropsychol Rehabil 2017; 27: 409‑454.
https://doi.org/10.1080/09602011.2015.1113187 DOI: https://doi.org/10.1080/09602011.2015.1113187
Osawa A, Maeshima S. Unilateral Spatial Neglect Due to Stroke. In: Dehkharghani S, éditeur. Stroke. Brisbane (AU): Exon Publications; 2021.
https://doi.org/10.36255/exonpublications.stroke.spatialneglect.2021 DOI: https://doi.org/10.36255/exonpublications.stroke.spatialneglect.2021
Ronchi R, Perez-Marcos D, Giroux A, Thomasson M, Serino A, Saj A, et al. Use of immersive virtual reality to detect unilateral spatial neglect in chronic stroke. Ann Phys Rehabil Med 2018; 61: e90‑1.
https://doi.org/10.1016/j.rehab.2018.05.193 DOI: https://doi.org/10.1016/j.rehab.2018.05.193
Pallavicini F, Pedroli E, Serino S, Dell'Isola A, Cipresso P, Cisari C, et al. Assessing Unilateral Spatial Neglect using advanced technologies: The potentiality of mobile virtual reality. Technol Health Care Off J Eur Soc Eng Med 2015; 23: 795‑807.
https://doi.org/10.3233/THC-151039 DOI: https://doi.org/10.3233/THC-151039
Chan KCS, Hui CLM, Suen YN, Lee EHM, Chang WC, Chan SKW, et al. Application of immersive virtual reality for assessment and intervention in psychosis: a systematic review. Brain Sci 2023; 13: 471.
https://doi.org/10.3390/brainsci13030471 DOI: https://doi.org/10.3390/brainsci13030471
Buxbaum LJ, Dawson AM, Linsley D. Reliability and validity of the Virtual Reality Lateralized Attention Test in assessing hemispatial neglect in right-hemisphere stroke. Neuropsychology 2012; 26: 430‑441.
https://doi.org/10.1037/a0028674 DOI: https://doi.org/10.1037/a0028674
Cook N, Winkler SL. Acceptance, usability and health applications of virtual worlds by older adults: a feasibility study. JMIR Res Protoc 2016; 5: e81.
https://doi.org/10.2196/resprot.5423 DOI: https://doi.org/10.2196/resprot.5423
Naef AC, Gerber SM, Single M, Müri RM, Haenggi M, Jakob SM, et al. Effects of immersive virtual reality on sensory overload in a random sample of critically ill patients. Front Med. 2023; 10: 1268659.
https://doi.org/10.3389/fmed.2023.1268659 DOI: https://doi.org/10.3389/fmed.2023.1268659
Weech S, Kenny S, Barnett-Cowan M. Presence and cybersickness in virtual reality are negatively related: a review. Front Psychol 2019; 10: 158.
https://doi.org/10.3389/fpsyg.2019.00158 DOI: https://doi.org/10.3389/fpsyg.2019.00158
Biernacki MP, Kennedy RS, Dziuda Ł. [Simulator sickness and its measurement with Simulator Sickness Questionnaire (SSQ)]. Med Pr 2016; 67: 545‑555 (in Polish).
https://doi.org/10.13075/mp.5893.00512 DOI: https://doi.org/10.13075/mp.5893.00512
Garcia-Agundez A, Reuter C, Becker H, Konrad R, Caserman P, Miede A, et al. Development of a classifier to determine factors causing cybersickness in virtual reality environments. Games Health J 2019; 8: 439‑444.
https://doi.org/10.1089/g4h.2019.0045 DOI: https://doi.org/10.1089/g4h.2019.0045
Published
How to Cite
License
Copyright (c) 2025 Chloé Sauvage, Pierre Chaulet, Luana Rivas Lopez, Johanne Garbusinski, Pierre Cabaraux, Zachary Duvigneaud, Stéphane Baudry
This work is licensed under a Creative Commons Attribution 4.0 International License.
All digitalized JRM contents is available freely online. The Foundation for Rehabilitation Medicine owns the copyright for all material published until volume 40 (2008), as from volume 41 (2009) authors retain copyright to their work and as from volume 49 (2017) the journal has been published Open Access, under CC-BY-NC licences (unless otherwise specified). The CC-BY-NC licenses allow third parties to copy and redistribute the material in any medium or format and to remix, transform, and build upon the material for non-commercial purposes, provided proper attribution to the original work.
From 2024, articles are published under the CC-BY licence. This license permits sharing, adapting, and using the material for any purpose, including commercial use, with the condition of providing full attribution to the original publication.