The feasibility and positive effects of a customised videogame rehabilitation programme for freezing of gait and falls in Parkinson's disease patients: a pilot study

Dijana Nuic, Maria Vinti, Carine Karachi, Pierre Foulon, Angèle Van Hamme, Marie-Laure Welter, Dijana Nuic, Maria Vinti, Carine Karachi, Pierre Foulon, Angèle Van Hamme, Marie-Laure Welter

Abstract

Background: Freezing of gait and falls represent a major burden in patients with advanced forms of Parkinson's disease (PD). These axial motor signs are not fully alleviated by drug treatment or deep-brain stimulation. Recently, virtual reality has emerged as a rehabilitation option for these patients. In this pilot study, we aim to determine the feasibility and acceptability of rehabilitation with a customised videogame to treat gait and balance disorders in PD patients, and assess its effects on these disabling motor signs.

Methods: We developed a customised videogame displayed on a screen using the Kinect system. To play, the patient had to perform large amplitude and fast movements of all four limbs, pelvis and trunk, in response to visual and auditory cueing, to displace an avatar to collect coins and avoid obstacles to gain points. We tested ten patients with advanced forms of PD (median disease duration = 16.5 years) suffering from freezing of gait and/or falls (Hoehn&Yahr score ≥ 3) resistant to antiparkinsonian treatment and deep brain stimulation. Patients performed 18 training sessions during a 6-9 week period. We measured the feasibility and acceptability of our rehabilitation programme and its effects on parkinsonian disability, gait and balance disorders (with clinical scales and kinematics recordings), positive and negative affects, and quality of life, after the 9th and 18th training sessions and 3 months later.

Results: All patients completed the 18 training sessions with high feasibility, acceptability and satisfaction scores. After training, the freezing-of-gait questionnaire, gait-and-balance scale and axial score significantly decreased by 39, 38 and 41%, respectively, and the activity-balance confidence scale increased by 35%. Kinematic gait parameters also significantly improved with increased step length and gait velocity and decreased double-stance time. Three months after the final session, no significant change persisted except decreased axial score and increased step length and velocity.

Conclusions: This study suggests that rehabilitation with a customised videogame to treat gait and balance disorders is feasible, well accepted, and effective in parkinsonian patients. These data serve as preliminary evidence for further larger and controlled studies to propose this customised videogame rehabilitation programme at home.

Trial registration: ClinicalTrials.gov NCT02469350 .

Keywords: Falls; Freezing of gait; Parkinson’s disease; Rehabilitation; Videogame.

Conflict of interest statement

Authors’ information

DN is physiotherapist and PhD student; MV is physiotherapist; AVH is research engineer, specialized in kinematics data; CK is neurosurgeon, specialized in deep brain stimulation for movement disorders; PF is responsible of clinical research programme in the Genious Group; MLW is neurologist and neurophysiologist, specialized in movement disorders and gait and balance disorders.

Ethics approval and consent to participate

This study is part of clinical trial C15–12 sponsored by Inserm (ID RCB: 2015-A00277–42). It was granted approval by local Ethics Committee (Comité de protection des personnes-Ile de France V on June 2, 2015), authorised by the French authorities (ANSM, 150358B-31), and registered in a public trials registry (Trial Registration: Competing interests

Dijana Nuic, Maria Vinti, Angele Van Hamme and Carine Karachi report no conflict of interest.

Marie-Laure Welter received personal fees from Medtronic for scientific board and medical training.

Pierre Foulon is employed by Genious Systems which has no property rights on the data.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
The ‘Toap Run’ videogame training. The images show screen shots of one patient during videogame training with ‘Toap Run’ in the three different scenarios. From Top to Bottom: ‘The Garden’, ‘The Mine’, and ‘The River’. The movements are schematically represented to the side of the images, from top to bottom: arm extension, lateral shift, trunk lateral displacement with knee flexion, knee flexion/extension, trunk rotation with arm movements, and anteroposterior trunk movement
Fig. 2
Fig. 2
Kinematic parameter recordings of gait initiation. Kinematic parameters of gait initiation in an individual patient. From top to bottom, curves represent the smoothed mean of ten trials and show the vertical centre of mass velocity (CoM-Vz), mediolateral (CoP x) and anteroposterior (CoP y) displacements and anteroposterior centre of foot pressure (CoP) velocity (CoP-Vy). APAs: anticipatory postural adjustments, DS: double-stance, CoP: centre of foot pressure, CoM: centre of mass, FC: foot contact of the swing leg, FO1: foot-off of the swing leg, FO2: foot-off of the stance leg, L: step length, t0: time of the first biomechanical event, V1: negative peak of the CoM vertical velocity, V2: CoM vertical velocity at the time of foot contact, W: step width
Fig. 3
Fig. 3
Game duration, difficulty and performance in PD patients. The graphs represent the mean and standard deviation, from top to bottom, in game duration, difficulty (number of movements) and performance after the 1st (S1), 3rd (S3), 6th (S6), 9th (S9), 12th (S12), 15th (S15) and 18th (S18) training sessions. * p < 0.05 repeated measures ANOVAs
Fig. 4
Fig. 4
Acceptability and feasibility of the ‘Toap Run’ videogame training in PD patients. The graphs represent the mean and standard deviation, from left to right and top to bottom, in perceived interest, perceived competence, perceived difficulty, perceived fatigue, acceptability and positive affects after the 1st session (W1) and once a week from the 2nd to the 6th week (W2 to W6). * p < 0.05 repeated measures ANOVAs
Fig. 5
Fig. 5
Effects of the ‘Toap Run’ videogame training on gait and balance disorders, parkinsonian disability and quality of life in PD patients. The graphs represent the mean and standard deviation, from left to right and top to bottom, in the Freezing Of Gait Questionnaire (FOG-Q), Activities and Balance Confidence (ABC) scale, Gait And Balance scale part B (GABS-B), Axial score (UPDRS items 18 + 27 + 28 + 29 + 30), parkinsonian motor disability (UPDRS part III) and activities of daily living (ADL, UPDRS part II) scores. Results were obtained before the first (Pre), after the 9th (Post-9) and 18th (Post-18) training sessions, and 3 months later (Post-M3). * p < 0.05 as compared to the first (baseline) assessment
Fig. 6
Fig. 6
Effects of the ‘Toap Run’ videogame training on gait initiation kinematic parameters. Each graph represents the mean and standard deviation from left to right and top to bottom of the APAs phase and double-stance durations, and anteroposterior CoP displacements during APAs and step length. Results were obtained before (Pre), after the 9th (Post-9) and 18th (Post-18) sessions, and 3 months later (Post-M3). * p < 0.05 as compared to the first (Pre) assessment

References

    1. Lang AE, Lozano AM. Parkinson’s disease. Second of two parts. N Engl J Med. 1998;339(16):1130–1143. doi: 10.1056/NEJM199810153391607.
    1. Lang AE, Lozano AM. Parkinson’s disease. First of two parts. N Engl J Med. 1998;339(15):1044–1053. doi: 10.1056/NEJM199810083391506.
    1. Pillon B, Dubois B, Cusimano G, Bonnet AM, Lhermitte F, Agid Y. Does cognitive impairment in Parkinson’s disease result from non-dopaminergic lesions? J Neurol Neurosurg Psychiatry. 1989;52(2):201–206. doi: 10.1136/jnnp.52.2.201.
    1. Bloem BR, Hausdorff JM, Visser JE, Giladi N. Falls and freezing of gait in Parkinson’s disease: a review of two interconnected, episodic phenomena. Mov Disord. 2004;19(8):871–884. doi: 10.1002/mds.20115.
    1. Fasano A, Aquino CC, Krauss JK, Honey CR, Bloem BR. Axial disability and deep brain stimulation in patients with Parkinson disease. Nat Rev Neurol. 2015;11(2):98–110. doi: 10.1038/nrneurol.2014.252.
    1. Kempster PA, Williams DR, Selikhova M, Holton J, Revesz T, Lees AJ. Patterns of levodopa response in Parkinson’s disease: a clinico-pathological study. Brain. 2007;130(Pt 8):2123–2128. doi: 10.1093/brain/awm142.
    1. Tomlinson CL, Patel S, Meek C, Herd CP, Clarke CE, Stowe R, et al. Physiotherapy intervention in Parkinson's disease: systematic review and meta-analysis. BMJ. 2012;345:e5004. doi: 10.1136/bmj.e5004.
    1. Klamroth S, Steib S, Devan S, Pfeifer K. Effects of exercise therapy on postural instability in Parkinson disease: a meta-analysis. J Neurol Phys Ther. 2016;40(1):3–14. doi: 10.1097/NPT.0000000000000117.
    1. Mak MK, Wong-Yu IS, Shen X, Chung CL. Long-term effects of exercise and physical therapy in people with Parkinson disease. Nat Rev Neurol. 2017;13(11):689–703. doi: 10.1038/nrneurol.2017.128.
    1. Ellis T, Boudreau JK, Deangelis TR, Brown LE, Cavanaugh JT, Earhart GM, et al. Barriers to exercise in people with Parkinson disease. Phys Ther. 2013;93(5):628–636. doi: 10.2522/ptj.20120279.
    1. Mirelman A, Maidan I, Deutsch JE. Virtual reality and motor imagery: promising tools for assessment and therapy in Parkinson’s disease. Mov Disord. 2013;28(11):1597–1608. doi: 10.1002/mds.25670.
    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((2):234–240. doi: 10.1093/gerona/glq201.
    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;388(10050):1170–1182. doi: 10.1016/S0140-6736(16)31325-3.
    1. Gallagher R, Damodaran H, Werner WG, Powell W, Deutsch JE. Auditory and visual cueing modulate cycling speed of older adults and persons with Parkinson's disease in a virtual cycling (V-Cycle) system. J Neuroeng Rehabil. 2016;13(1):77. doi: 10.1186/s12984-016-0184-z.
    1. Dockx K, Bekkers EM, Van den Bergh V, Ginis P, Rochester L, Hausdorff JM, et al. Virtual reality for rehabilitation in Parkinson’s disease. Cochrane Database Syst Rev. 2016;12:CD010760.
    1. Ekker MS, Janssen S, Nonnekes J, Bloem BR, de Vries NM. Neurorehabilitation for Parkinson's disease: future perspectives for behavioural adaptation. Parkinsonism Relat Disord. 2016;22(Suppl 1):S73–S77. doi: 10.1016/j.parkreldis.2015.08.031.
    1. Barry G, Galna B, Rochester L. The role of exergaming in Parkinson's disease rehabilitation: a systematic review of the evidence. J Neuroeng Rehabil. 2014;11:33. doi: 10.1186/1743-0003-11-33.
    1. Esculier JF, Vaudrin J, Beriault P, Gagnon K, Tremblay LE. Home-based balance training programme using Wii Fit with balance board for Parkinsons's disease: a pilot study. J Rehabil Med. 2012;44(2):144–150. doi: 10.2340/16501977-0922.
    1. Mhatre PV, Vilares I, Stibb SM, Albert MV, Pickering L, Marciniak CM, et al. Wii Fit balance board playing improves balance and gait in Parkinson disease. PM R. 2013;5(9):769–777. doi: 10.1016/j.pmrj.2013.05.019.
    1. Negrini S, Bissolotti L, Ferraris A, Noro F, Bishop MD, Villafane JH. Nintendo Wii fit for balance rehabilitation in patients with Parkinson's disease: a comparative study. J Bodyw Mov Ther. 2017;21(1):117–123. doi: 10.1016/j.jbmt.2016.06.001.
    1. Pompeu JE, Mendes FA, Silva KG, Lobo AM, Oliveira Tde P, Zomignani AP, et al. Effect of Nintendo Wii-based motor and cognitive training on activities of daily living in patients with Parkinson’s disease: a randomised clinical trial. Physiotherapy. 2012;98(3):196–204. doi: 10.1016/j.physio.2012.06.004.
    1. Herz NB, Mehta SH, Sethi KD, Jackson P, Hall P, Morgan JC. Nintendo Wii rehabilitation (“Wii-hab”) provides benefits in Parkinson’s disease. Parkinsonism Relat Disord. 2013;19(11):1039–1042. doi: 10.1016/j.parkreldis.2013.07.014.
    1. dos Santos Mendes FA, Pompeu JE, Modenesi Lobo A, Guedes da Silva K, Oliveira Tde P, Peterson Zomignani A, et al. Motor learning, retention and transfer after virtual-reality-based training in Parkinson’s disease--effect of motor and cognitive demands of games: a longitudinal, controlled clinical study. Physiotherapy. 2012;98(3):217–223. doi: 10.1016/j.physio.2012.06.001.
    1. Summa S, Basteris A, Betti E, Sanguineti V. Adaptive training with full-body movements to reduce bradykinesia in persons with Parkinson's disease: a pilot study. J Neuroeng Rehabil. 2015;12:16. doi: 10.1186/s12984-015-0009-5.
    1. Farley BG, Koshland GF. Training BIG to move faster: the application of the speed-amplitude relation as a rehabilitation strategy for people with Parkinson’s disease. Exp Brain Res. 2005;167(3):462–467. doi: 10.1007/s00221-005-0179-7.
    1. Keus S, Munneke M, Graziano M, Paltamaa J, Pelosin E, Domingos J, et al. European Physiotherapy Guideline for Parkinson’s Disease. the Netherlands: KNGF/Parkinson Net; 2014.
    1. Hoehn MM, Yahr MD. Parkinsonism: onset, progression and mortality. Neurology. 1967;17(5):427–442. doi: 10.1212/WNL.17.5.427.
    1. Crenna P, Frigo C. A motor programme for the initiation of forward-oriented movements in humans. J Physiol. 1991;437:635–653. doi: 10.1113/jphysiol.1991.sp018616.
    1. Chastan N, Do MC, Bonneville F, Torny F, Bloch F, Westby GW, et al. Gait and balance disorders in Parkinson's disease: impaired active braking of the fall of Centre of gravity. Mov Disord. 2009;24(2):188–195. doi: 10.1002/mds.22269.
    1. Ben-Sadoun G, Sacco G, Manera V, Bourgeois J, Konig A, Foulon P, et al. Physical and cognitive stimulation using an Exergame in subjects with normal aging, mild and moderate cognitive impairment. J Alzheimers Dis. 2016;53(4):1299–1314. doi: 10.3233/JAD-160268.
    1. Gledhill JA, Rodary C, Mahe C, Laizet C. French validation of the revised Piper Fatigue Scale. Rech Soins Infirm. 2002;68:50–65.
    1. Pelissolo A, Rolland JP, Perez-Diaz F, Jouvent R, Allilaire JF. Dimensional approach of emotion in psychiatry: validation of the positive and negative emotionality scale (EPN-31) Encéphale. 2007;33(3 Pt 1):256–263. doi: 10.1016/S0013-7006(07)92037-0.
    1. Thomas M, Jankovic J, Suteerawattananon M, Wankadia S, Caroline KS, Vuong KD, et al. Clinical gait and balance scale (GABS): validation and utilization. J Neurol Sci. 2004;217(1):89–99. doi: 10.1016/j.jns.2003.09.005.
    1. Giladi N, Shabtai H, Simon ES, Biran S, Tal J, Korczyn AD. Construction of freezing of gait questionnaire for patients with parkinsonism. Parkinsonism Relat Disord. 2000;6(3):165–170. doi: 10.1016/S1353-8020(99)00062-0.
    1. Powell LE, Myers AM. The Activities-specific Balance Confidence (ABC) scale. J Gerontol A Biol Sci Med Sci. 1995;50A(1):M28–M34. doi: 10.1093/gerona/50A.1.M28.
    1. Martinez-Martin P, Frades Payo B. Quality of life in Parkinson’s disease: validation study of the PDQ-39 Spanish version. The Grupo Centro for study of movement disorders. J Neurol. 1998;245(Suppl 1):S34–S38. doi: 10.1007/PL00007737.
    1. Winter DA. Human balance and posture control during standing and walking. Gait Posture. 1995;3:193–214. doi: 10.1016/0966-6362(96)82849-9.
    1. Burleigh-Jacobs A, Horak FB, Nutt JG, Obeso JA. Step initiation in Parkinson’s disease: influence of levodopa and external sensory triggers. Mov Disord. 1997;12(2):206–215. doi: 10.1002/mds.870120211.
    1. Sparrow D, DeAngelis TR, Hendron K, Thomas CA, Saint-Hilaire M, Ellis T. Highly challenging balance program reduces fall rate in Parkinson disease. J Neurol Phys Ther. 2016;40(1):24–30. doi: 10.1097/NPT.0000000000000111.
    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;1:CD007830.
    1. Esculier JF, Vaudrin J, Tremblay LE. Corticomotor excitability in Parkinson’s disease during observation, imagery and imitation of action: effects of rehabilitation using wii fit and comparison to healthy controls. J Parkinsons Dis. 2014;4(1):67–75.
    1. Hess JA, Woollacott M, Shivitz N. Ankle force and rate of force production increase following high intensity strength training in frail older adults. Aging Clin Exp Res. 2006;18(2):107–115. doi: 10.1007/BF03327425.
    1. Rochester L, Baker K, Hetherington V, Jones D, Willems AM, Kwakkel G, et al. Evidence for motor learning in Parkinson’s disease: acquisition, automaticity and retention of cued gait performance after training with external rhythmical cues. Brain Res. 2010;1319:103–111. doi: 10.1016/j.brainres.2010.01.001.
    1. Azulay JP, Mesure S, Amblard B, Blin O, Sangla I, Pouget J. Visual control of locomotion in Parkinson’s disease. Brain. 1999;122(Pt 1):111–120. doi: 10.1093/brain/122.1.111.
    1. Mokienko OA, Chervyakov AV, Kulikova SN, Bobrov PD, Chernikova LA, Frolov AA, et al. Increased motor cortex excitability during motor imagery in brain-computer interface trained subjects. Front Comput Neurosci. 2013;7:168. doi: 10.3389/fncom.2013.00168.
    1. Sehm B, Taubert M, Conde V, Weise D, Classen J, Dukart J, et al. Structural brain plasticity in Parkinson’s disease induced by balance training. Neurobiol Aging. 2014;35(1):232–239. doi: 10.1016/j.neurobiolaging.2013.06.021.
    1. Koepp MJ, Gunn RN, Lawrence AD, Cunningham VJ, Dagher A, Jones T, et al. Evidence for striatal dopamine release during a video game. Nature. 1998;393(6682):266–268. doi: 10.1038/30498.
    1. Tomlinson CL, Patel S, Meek C, Clarke CE, Stowe R, Shah L, et al. Physiotherapy versus placebo or no intervention in Parkinson's disease. Cochrane Database Syst Rev. 2012;7:CD002817.

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