Walking in fully immersive virtual environments: an evaluation of potential adverse effects in older adults and individuals with Parkinson's disease

Aram Kim, Nora Darakjian, James M Finley, Aram Kim, Nora Darakjian, James M Finley

Abstract

Background: Virtual reality (VR) has recently been explored as a tool for neurorehabilitation to enable individuals with Parkinson's disease (PD) to practice challenging skills in a safe environment. Current technological advances have enabled the use of affordable, fully immersive head-mounted displays (HMDs) for potential therapeutic applications. However, while previous studies have used HMDs in individuals with PD, these were only used for short bouts of walking. Clinical applications of VR for gait training would likely involve an extended exposure to the virtual environment, which has the potential to cause individuals with PD to experience simulator-related adverse effects due to their age or pathology. Thus, our objective was to evaluate the safety of using an HMD for longer bouts of walking in fully immersive VR for older adults and individuals with PD.

Methods: Thirty-three participants (11 healthy young, 11 healthy older adults, and 11 individuals with PD) were recruited for this study. Participants walked for 20 min while viewing a virtual city scene through an HMD (Oculus Rift DK2). Safety was evaluated using the mini-BESTest, measures of center of pressure (CoP) excursion, and questionnaires addressing symptoms of simulator sickness (SSQ) and measures of stress and arousal.

Results: Most participants successfully completed all trials without any discomfort. There were no significant changes for any of our groups in symptoms of simulator sickness or measures of static and dynamic balance after exposure to the virtual environment. Surprisingly, measures of stress decreased in all groups while the PD group also increased the level of arousal after exposure.

Conclusions: Older adults and individuals with PD were able to successfully use immersive VR during walking without adverse effects. This provides systematic evidence supporting the safety of immersive VR for gait training in these populations.

Keywords: Gait; Head-mounted display; Parkinson’s disease; Simulator sickness; Virtual reality.

Figures

Fig. 1
Fig. 1
Experimental protocol. Pre-test evaluation involved a set of clinical assessments (MDS-UPDRS for the PD group, mini-BESTest, 10 m walk test, MoCA), static postural stability measures (CoP during eyes open and closed) and questionnaires (SSQ, SAC). The test consisted of walking for a total of 20 min with breaks taken every 5 min for participants to complete a short symptom checklist and for measures of blood pressure (BP) to be monitored. Post-test evaluation involved an additional set of clinical assessments (mini-BESTest, 10 m walk test), static postural stability measures and questionnaires (SSQ, SAC, PQ)
Fig. 2
Fig. 2
Representative images of the virtual environment. The environment consisted of a cityscape including buildings, avatars and a 800 m pedestrian path. A first person views (a) up, (b) front, (c) left, and (d) right
Fig. 3
Fig. 3
Pre- (dark gray bar) and post-test (white bar) average simulator sickness questionnaire total score and sub-category scores with standard deviation. Asterisks represent statistical significance (**: p < 0.01, ***: p < 0.005). a Average total score of SSQ. b Average Nausea score. c Average Oculomotor discomfort score. d Average Disorientation score
Fig. 4
Fig. 4
CoP sway area. Pre- (black bar) and post-test (dark gray bar) during eyes open (EO) and pre- (light gray bar) and post-test (white bar) during eyes closed (EC). Vertical bars represent standard deviations. Asterisks represent statistical significance (*: p < 0.05)
Fig. 5
Fig. 5
Average presence questionnaire scores are shown with individual scores. a Average total score. b Average sub-category scores; Involvement/Control, visual fidelity, adaptation/Immersion and interface quality for HY (dark gray bar), HO (light gray bar), and PD (white bar). Vertical bars represent standard deviations. Asterisks represent statistical significance (*: p < 0.05)

References

    1. Ross GW, Abbott RD. Living and dying with Parkinson’s disease. Mov Disord. 2014;29:1571–1573. doi: 10.1002/mds.25955.
    1. Weintraub D, Comella CL, Horn S. Parkinson’s disease—Part 1: Pathophysiology, symptoms, burden, diagnosis, and assessment. Am J Manag Care. 2008;14:S40–S48.
    1. Grimbergen YAM, Munneke M, Bloem BR. Falls in Parkinson’s disease. Curr Opin Neurol. 2004;17:405–415. doi: 10.1097/01.wco.0000137530.68867.93.
    1. Grabli D, Karachi C, Welter M-L, Lau B, Hirsch EC, Vidailhet M, et al. Normal and pathological gait: what we learn from Parkinson’s disease. J Neurol Neurosurg Psychiatry. 2012. doi:10.1136/jnnp-2012-302263.
    1. Kleim JA, Jones TA. Principles of experience-dependent neural plasticity: implications for rehabilitation after brain damage. J Speech Lang Hear Res. 2008;51:S225–S239. doi: 10.1044/1092-4388(2008/018).
    1. Petzinger GM, Fisher BE, Van Leeuwen J-E, Vukovic M, Akopian G, Meshul CK, et al. Enhancing neuroplasticity in the basal ganglia: the role of exercise in Parkinson’s disease. Mov Disord. 2010;25(Suppl 1):S141–S145. doi: 10.1002/mds.22782.
    1. Herman T, Giladi N, Gruendlinger L, Hausdorff JM. Six Weeks of Intensive Treadmill Training Improves Gait and Quality of Life in Patients With Parkinson’s Disease: A Pilot Study. Arch Phys Med Rehabil. 2007;88:1154–1158. doi: 10.1016/j.apmr.2007.05.015.
    1. de Goede CJT, Keus SHJ, Kwakkel G, Wagenaar RC. The effects of physical therapy in Parkinson’s Disease: A research synthesis. Arch Phys Med Rehabil. 2001;82:509–515. doi: 10.1053/apmr.2001.22352.
    1. Mirelman A, Maidan I, Herman T, Deutsch JE, Giladi N, Hausdorff JM. Virtual reality for gait training: can it induce motor learning to enhance complex walking and reduce fall risk in patients with Parkinson’s disease? J Gerontol A Biol Sci Med Sci. 2011;66:234–240. doi: 10.1093/gerona/glq201.
    1. Yang Y-R, Tsai M-P, Chuang T-Y, Sung W-H, Wang R-Y. Virtual reality-based training improves community ambulation in individuals with stroke: a randomized controlled trial. Gait Posture. 2008;28:201–206. doi: 10.1016/j.gaitpost.2007.11.007.
    1. Jaffe DL, Brown DA, Pierson-Carey CD, Buckley EL, Lew HL. Stepping over obstacles to improve walking in individuals with poststroke hemiplegia. J Rehabil Res Dev. 2004;41:283–292. doi: 10.1682/JRRD.2004.03.0283.
    1. Parijat P, Lockhart TE, Liu J. Effects of perturbation-based slip training using a virtual reality environment on slip-induced falls. Ann Biomed Eng. 2015;43:958–967. doi: 10.1007/s10439-014-1128-z.
    1. Shema S, Brozgol M, Dorfman M, Maidan I, Yannai OW, Giladi N, et al. 2013 International Conference on Virtual Rehabilitation (ICVR) 2013. Clinical experience using a 5 week treadmill training program with virtual reality to enhance gait; pp. 249–253.
    1. Fung J, Richards CL, Malouin F, McFadyen BJ, Lamontagne A. A treadmill and motion coupled virtual reality system for gait training post-stroke. Cycberpsychol Behav. 2006;9:157–162. doi: 10.1089/cpb.2006.9.157.
    1. Rizzo A, Kim GJ. A SWOT Analysis of the Field of Virtual Reality Rehabilitation and Therapy. Presence Teleop Virt. 2005;14:119–146. doi: 10.1162/1054746053967094.
    1. Mirelman A, Rochester L, Reelick M, Nieuwhof F, Pelosin E, Abbruzzese G, et al. V-TIME: a treadmill training program augmented by virtual reality to decrease fall risk in older adults: study design of a randomized controlled trial. BMC Neurol. 2013;13:15. doi: 10.1186/1471-2377-13-15.
    1. Mirelman A, Rochester L, Maidan I, Del Din S, Alcock L, Nieuwhof F, et al. Addition of a non-immersive virtual reality component to treadmill training to reduce fall risk in older adults (V-TIME): a randomised controlled trial. Lancet. 2016. doi:10.1016/S0140-6736(16)31325-3.
    1. Cruz-Neira C, Sandin DJ, DeFanti TA, Kenyon RV, Hart JC. The CAVE: Audio Visual Experience Automatic Virtual Environment. Commun ACM. 1992;35:64–72. doi: 10.1145/129888.129892.
    1. Cruz-Neira C, Sandin DJ, DeFanti TA. Proceedings of the 20th Annual Conference on Computer Graphics and Interactive Techniques. New York: ACM; 1993. Surround-screen Projection-based Virtual Reality: The Design and Implementation of the CAVE; pp. 135–142.
    1. Denisova A, Cairns P. Proceedings of the 33rd Annual ACM Conference on Human Factors in Computing Systems. New York: ACM; 2015. First Person vs. Third Person Perspective in Digital Games: Do Player Preferences Affect Immersion? pp. 145–148.
    1. Kozhevnikov M, Dhond RP. Understanding Immersivity: Image Generation and Transformation Processes in 3D Immersive Environments. Front Psychol. 2012;3. doi:10.3389/fpsyg.2012.00284.
    1. Riva G, Davide F, IJsselsteijn WA. Being There: Concepts, Effects and Measurements of User Presence in Synthetic Environments. Amsterdam; Washington, D.C.; Tokyo: Ios Press; 2003.
    1. Rand D, Kizony R, Feintuch U, Katz N, Josman N, Rizzo A, Weiss PL. Comparison of Two VR Platforms for Rehabilitation: Video Capture versus HMD. Presence Teleop Virt. 2005;14:147–60. doi:10.1162/1054746053967012.
    1. Witmer BG, Singer MJ. Measuring Presence in Virtual Environments: A Presence Questionnaire. Presence Teleop Virt. 1998;7:225–240. doi: 10.1162/105474698565686.
    1. Schultheis MT, Rizzo AA. The application of virtual reality technology in rehabilitation. Rehabil Psychol. 2001;46:296–311. doi: 10.1037/0090-5550.46.3.296.
    1. Bailenson J, Patel K, Nielsen A, Bajscy R, Jung S-H, Kurillo G. The Effect of Interactivity on Learning Physical Actions in Virtual Reality. Med Psychol. 2008;11:354–376. doi: 10.1080/15213260802285214.
    1. Kennedy RS, Lilienthal MG, Berbaum KS, Baltzley DR, McCauley ME. Simulator sickness in U.S. Navy flight simulators. Aviat Space Environ Med. 1989;60:10–16.
    1. Regan EC, Price KR. The frequency of occurrence and severity of side-effects of immersion virtual reality. Aviat Space Environ Med. 1994;65:527–530.
    1. Sharples S, Cobb S, Moody A, Wilson JR. Virtual reality induced symptoms and effects (VRISE): Comparison of head mounted display (HMD), desktop and projection display systems. Displays. 2008;29:58–69. doi: 10.1016/j.displa.2007.09.005.
    1. Treleaven J, Battershill J, Cole D, Fadelli C, Freestone S, Lang K, et al. Simulator sickness incidence and susceptibility during neck motion-controlled virtual reality tasks. Virtual Reality. 2015;1–9. doi:10.1007/s10055-015-0266-4.
    1. Young MK, Gaylor GB, Andrus SM, Bodenheimer B. Proceedings of the ACM Symposium on Applied Perception. New York: ACM; 2014. A Comparison of Two Cost-differentiated Virtual Reality Systems for Perception and Action Tasks; pp. 83–90.
    1. Johnson DM. Introduction to and review of simulator sickness research. Fort Rucker: Rotary-Wing Aviation Research Unit, U.S. Army Research Institute for the Behavioral and Social Sciences; 2005.
    1. Reason J, Brand JJ. In: Motion sickness. Reason JT, Brand JJ, editors. London, New York: Academic; 1975.
    1. Reason JT. Motion sickness adaptation: a neural mismatch model. J R Soc Med. 1978;71:819–829.
    1. Brooks JO, Goodenough RR, Crisler MC, Klein ND, Alley RL, Koon BL, et al. Simulator sickness during driving simulation studies. Accid Anal Prev. 2010;42:788–796. doi: 10.1016/j.aap.2009.04.013.
    1. Patel N, Jankovic J, Hallett M. Sensory aspects of movement disorders. Lancet Neurol. 2014;13:100–112. doi: 10.1016/S1474-4422(13)70213-8.
    1. Hwang S, Agada P, Grill S, Kiemel T, Jeka JJ. A central processing sensory deficit with Parkinson’s disease. Exp Brain Res. 2016;234:2369–2379. doi: 10.1007/s00221-016-4642-4.
    1. Boecker H, Ceballos-Baumann A, Bartenstein P, Weindl A, Siebner HR, Fassbender T, et al. Sensory processing in Parkinson’s and Huntington’s disease. Brain. 1999;122:1651–1665. doi: 10.1093/brain/122.9.1651.
    1. Stoffregen TA, Smart LJ. Postural instability precedes motion sickness. Brain Res Bull. 1998;47:437–448. doi: 10.1016/S0361-9230(98)00102-6.
    1. Stoffregen TA, Hettinger LJ, Haas MW, Roe MM, Smart LJ. Postural Instability and Motion Sickness in a Fixed-Base Flight Simulator. Hum Factors. 2000;42:458–469. doi: 10.1518/001872000779698097.
    1. Schmit JM, Riley MA, Dalvi A, Sahay A, Shear PK, Shockley KD, et al. Deterministic center of pressure patterns characterize postural instability in Parkinson’s disease. Exp Brain Res. 2006;168:357–367. doi: 10.1007/s00221-005-0094-y.
    1. Błaszczyk JW, Orawiec R, Duda-Kłodowska D, Opala G. Assessment of postural instability in patients with Parkinson’s disease. Exp Brain Res. 2007;183:107–114. doi: 10.1007/s00221-007-1024-y.
    1. Benatru I, Vaugoyeau M, Azulay J-P. Postural disorders in Parkinson’s disease. Neurophysiol Clin. 2008;38:459–465. doi: 10.1016/j.neucli.2008.07.006.
    1. Ehgoetz Martens KA, Ellard CG, Almeida QJ. Does manipulating the speed of visual flow in virtual reality change distance estimation while walking in Parkinson’s disease? Exp Brain Res. 2015;233:787–795. doi: 10.1007/s00221-014-4154-z.
    1. Ehgoetz Martens KA, Ellard CG, Almeida QJ. Virtually-induced threat in Parkinson’s: Dopaminergic interactions between anxiety and sensory-perceptual processing while walking. Neuropsychologia. 2015;79:322–331. doi: 10.1016/j.neuropsychologia.2015.05.015.
    1. Ehgoetz Martens KA, Ellard CG, Almeida QJ. Anxiety-provoked gait changes are selectively dopa-responsive in Parkinson’s disease. Eur J Neurosci. 2015;42:2028–2035. doi: 10.1111/ejn.12928.
    1. Mehrholz J, Friis R, Kugler J, Twork S, Storch A, Pohl M. Treadmill training for patients with Parkinson’s disease. Cochrane Database Syst Rev. 2010;CD007830. doi:10.1002/14651858.CD007830.pub2.
    1. Nasreddine ZS, Phillips NA, Bédirian V, Charbonneau S, Whitehead V, Collin I, et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc. 2005;53:695–699. doi: 10.1111/j.1532-5415.2005.53221.x.
    1. Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P, et al. Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): Scale presentation and clinimetric testing results. Mov Disord. 2008;23:2129–2170. doi: 10.1002/mds.22340.
    1. Bohannon RW. Comfortable and maximum walking speed of adults aged 20–79 years: reference values and determinants. Age Ageing. 1997;26:15–19. doi: 10.1093/ageing/26.1.15.
    1. Steffen T, Seney M. Test-retest reliability and minimal detectable change on balance and ambulation tests, the 36-item short-form health survey, and the unified Parkinson disease rating scale in people with parkinsonism. Phys Ther. 2008;88:733–746. doi: 10.2522/ptj.20070214.
    1. Godi M, Franchignoni F, Caligari M, Giordano A, Turcato AM, Nardone A. Comparison of reliability, validity, and responsiveness of the mini-BESTest and Berg Balance Scale in patients with balance disorders. Phys Ther. 2013;93:158–167. doi: 10.2522/ptj.20120171.
    1. Lajoie Y, Gallagher SP. Predicting falls within the elderly community: comparison of postural sway, reaction time, the Berg balance scale and the Activities-specific Balance Confidence (ABC) scale for comparing fallers and non-fallers. Arch Gerontol Geriatr. 2004;38:11–26. doi: 10.1016/S0167-4943(03)00082-7.
    1. Robert S, Kennedy NEL. Simulator Sickness Questionnaire: An Enhanced Method for Quantifying Simulator Sickness. Int J Aviat Psychol. 1993;3:203–220. doi: 10.1207/s15327108ijap0303_3.
    1. Kennedy RS, Drexler JM, Compton DE, Stanney KM, Lanham S, Harm DL. Configural Scoring of Simulator Sickness, Cybersickness and Space Adaptation Syndrome: Similarities and Differences? [Internet]. 2001. Available: . Accessed 16 Feb 2017.
    1. Cox T, Mackay C. The measurement of self-reported stress and arousal. Br J Psychol. 1985;76:183–186. doi: 10.1111/j.2044-8295.1985.tb01941.x.
    1. Watts C, Cox T, Robson J. Morningness-Eveningness and Diurnal Variations in Self-Reported Mood. J Psychol. 1983;113:251–256. doi: 10.1080/00223980.1983.9923583.
    1. Wilson JR, Corlett N. Evaluation of Human Work. 3rd ed. Boca Raton: CRC Press; 2005.
    1. Cobb SVG, Nichols S, Ramsey A, Wilson JR. Virtual Reality-Induced Symptoms and Effects (VRISE) Presence Teleop Virt. 1999;8:169–186. doi: 10.1162/105474699566152.
    1. Witmer BG, Jerome CJ, Singer MJ. The Factor Structure of the Presence Questionnaire. Presence Teleop Virt. 2005;14:298–312. doi: 10.1162/105474605323384654.
    1. Duarte M, Zatsiorsky VM. Effects of body lean and visual information on the equilibrium maintenance during stance. Exp Brain Res. 2002;146:60–69. doi: 10.1007/s00221-002-1154-1.
    1. Chaudhuri KR, Schapira AH. Non-motor symptoms of Parkinson’s disease: dopaminergic pathophysiology and treatment. Lancet Neurol. 2009;8:464–474. doi: 10.1016/S1474-4422(09)70068-7.
    1. Chaudhuri KR, Healy DG, Schapira AH. Non-motor symptoms of Parkinson’s disease: diagnosis and management. Lancet Neurol. 2006;5:235–245. doi: 10.1016/S1474-4422(06)70373-8.
    1. Kennedy RS, Stanney KM. Postural instability induced by virtual reality exposure: Development of a certification protocol. Int J Hum Comput Interact. 1996;8:25–47. doi: 10.1080/10447319609526139.
    1. O’Hoski S, Winship B, Herridge L, Agha T, Brooks D, Beauchamp MK, et al. Increasing the clinical utility of the BESTest, mini-BESTest, and brief-BESTest: normative values in Canadian adults who are healthy and aged 50 years or older. Phys Ther. 2014;94:334–342. doi: 10.2522/ptj.20130104.
    1. Duncan RP, Earhart GM. Should One Measure Balance or Gait to Best Predict Falls among People with Parkinson Disease? Parkinsons Dis. 2012;2012:923493.
    1. Leddy AL, Crowner BE, Earhart GM. Utility of the Mini-BESTest, BESTest, and BESTest sections for balance assessments in individuals with Parkinson disease. J Neurol Phys Ther. 2011;35:90–97. doi: 10.1097/NPT.0b013e31821a620c.
    1. Roth DL, Bachtler SD, Fillingim RB. Acute emotional and cardiovascular effects of stressful mental work during aerobic exercise. Psychophysiology. 1990;27:694–701. doi: 10.1111/j.1469-8986.1990.tb03196.x.
    1. Steptoe A, Cox S. Acute effects of aerobic exercise on mood. Health Psychol. 1988;7:329–340. doi: 10.1037/0278-6133.7.4.329.
    1. Hoffman MD, Hoffman DR. Exercisers achieve greater acute exercise-induced mood enhancement than nonexercisers. Arch Phys Med Rehabil. 2008;89:358–363. doi: 10.1016/j.apmr.2007.09.026.
    1. Pierce EF, Pate DW. Mood alterations in older adults following acute exercise. Percept Mot Skills. 1994;79:191–194. doi: 10.2466/pms.1994.79.1.191.
    1. Jaeger BK, Mourant RR. Comparison of Simulator Sickness Using Static and Dynamic Walking Simulators. Proc Hum Factors Ergon Soc Annu Meet. 2001;45:1896–1900. doi: 10.1177/154193120104502709.
    1. de Lau LM, Breteler MM. Epidemiology of Parkinson’s disease. Lancet Neurol. 2006;5:525–535. doi: 10.1016/S1474-4422(06)70471-9.
    1. Morris ME, Huxham F, McGinley J, Dodd K, Iansek R. The biomechanics and motor control of gait in Parkinson disease. Clin Biomech. 2001;16:459–470. doi: 10.1016/S0268-0033(01)00035-3.
    1. Cowie D, Limousin P, Peters A, Day BL. Insights into the neural control of locomotion from walking through doorways in Parkinson’s disease. Neuropsychologia. 2010;48:2750–2757. doi: 10.1016/j.neuropsychologia.2010.05.022.

Source: PubMed

3
Abonneren