Cueing Paradigms to Improve Gait and Posture in Parkinson's Disease: A Narrative Review

Niveditha Muthukrishnan, James J Abbas, Holly A Shill, Narayanan Krishnamurthi, Niveditha Muthukrishnan, James J Abbas, Holly A Shill, Narayanan Krishnamurthi

Abstract

Progressive gait dysfunction is one of the primary motor symptoms in people with Parkinson's disease (PD). It is generally expressed as reduced step length and gait speed and as increased variability in step time and step length. People with PD also exhibit stooped posture which disrupts gait and impedes social interaction. The gait and posture impairments are usually resistant to the pharmacological treatment, worsen as the disease progresses, increase the likelihood of falls, and result in higher rates of hospitalization and mortality. These impairments may be caused by perceptual deficiencies (poor spatial awareness and loss of temporal rhythmicity) due to the disruptions in processing intrinsic information related to movement initiation and execution which can result in misperceptions of the actual effort required to perform a desired movement and maintain a stable posture. Consequently, people with PD often depend on external cues during execution of motor tasks. Numerous studies involving open-loop cues have shown improvements in gait and freezing of gait (FoG) in people with PD. However, the benefits of cueing may be limited, since cues are provided in a consistent/rhythmic manner irrespective of how well a person follows them. This limitation can be addressed by providing feedback in real-time to the user about performance (closed-loop cueing) which may help to improve movement patterns. Some studies that used closed-loop cueing observed improvements in gait and posture in PD, but the treadmill-based setup in a laboratory would not be accessible outside of a research setting, and the skills learned may not readily and completely transfer to overground locomotion in the community. Technologies suitable for cueing outside of laboratory environments could facilitate movement practice during daily activities at home or in the community and could strongly reinforce movement patterns and improve clinical outcomes. This narrative review presents an overview of cueing paradigms that have been utilized to improve gait and posture in people with PD and recommends development of closed-loop wearable systems that can be used at home or in the community to improve gait and posture in PD.

Keywords: Parkinson’s disease; cueing; gait; posture; rehabilitation; wearable sensors.

Conflict of interest statement

The authors have no conflict of interest/financial disclosures to report.

Figures

Figure 1
Figure 1
(A) Sensory-motor areas for movement execution in the basal ganglia and the impaired motor pathways in Parkinson’s disease (PD) with the prevalence of the indirect pathway over the direct pathway and the affected SN’s input to the circuit. SN—Substantia nigra, GPi—globus pallidus internus, GPe—globus pallidus externus, Put—putamen, Th—thalamus, CN—caudate nucleus, STN—sub-thalamic nucleus. This results in increased neuronal firing activity in the output nuclei of the basal ganglia that leads to excessive inhibition of thalamo-cortical and brainstem motor systems which, in turn, interferes with movement onset and execution [28,29]. (B) Representation of brain areas activated during external cueing reported from findings of image analysis studies conducted on people with PD during cueing experiments [17,30,31,32].

References

    1. Rogers M.W. Disorders of posture, balance, and gait in Parkinson’s disease. Clin. Geriatr. Med. 1996;12:825–845. doi: 10.1016/S0749-0690(18)30203-9.
    1. Kalia L.V., Lang A.E. Parkinson disease in 2015: Evolving basic, pathological and clinical concepts in PD. Nat. Rev. Neurol. 2016;12:65–66. doi: 10.1038/nrneurol.2015.249.
    1. Miller-Patterson C., Buesa R., McLaughlin N., Jones R., Akbar U., Friedman J.H. Motor asymmetry over time in Parkinson’s disease. J. Neurol. Sci. 2018;393:14–17. doi: 10.1016/j.jns.2018.08.001.
    1. Takakusaki K., Tomita N., Yano M. Substrates for normal gait and pathophysiology of gait disturbances with respect to the basal ganglia dysfunction. J. Neurol. 2008;255(Suppl. 4):19–29. doi: 10.1007/s00415-008-4004-7.
    1. Plotnik M., Hausdorff J.M. The role of gait rhythmicity and bilateral coordination of stepping in the pathophysiology of freezing of gait in Parkinson’s disease. Mov. Disord. 2008;23(Suppl. 2):S444–S450. doi: 10.1002/mds.21984.
    1. Boonstra T.A., van der Kooij H., Munneke M., Bloem B.R. Gait disorders and balance disturbances in Parkinson’s disease: Clinical update and pathophysiology. Curr. Opin. Neurol. 2008;21:461–471. doi: 10.1097/WCO.0b013e328305bdaf.
    1. Hobert M.A., Nussbaum S., Heger T., Berg D., Maetzler W., Heinzel S. Progressive Gait Deficits in Parkinson’s Disease: A Wearable-Based Biannual 5-Year Prospective Study. Front. Aging Neurosci. 2019;11:22. doi: 10.3389/fnagi.2019.00022.
    1. Rochester L., Baker K., Nieuwboer A., Burn D. Targeting dopa-sensitive and dopa-resistant gait dysfunction in Parkinson’s disease: Selective responses to internal and external cues. Mov. Disord. 2011;26:430–435. doi: 10.1002/mds.23450.
    1. Rocchi L., Chiari L., Horak F.B. Effects of deep brain stimulation and levodopa on postural sway in Parkinson’s disease. J. Neurol. Neurosurg. Psychiatry. 2002;73:267–274. doi: 10.1136/jnnp.73.3.267.
    1. Beuter A., Hernandez R., Rigal R., Modolo J., Blanchet P.J. Postural sway and effect of levodopa in early Parkinson’s disease. Can. J. Neurol. Sci. 2008;35:65–68. doi: 10.1017/S0317167100007575.
    1. King L.A., Horak F.B. Lateral stepping for postural correction in Parkinson’s disease. Arch. Phys. Med. Rehabil. 2008;89:492–499. doi: 10.1016/j.apmr.2007.11.017.
    1. King L.A., St George R.J., Carlson-Kuhta P., Nutt J.G., Horak F.B. Preparation for compensatory forward stepping in Parkinson’s disease. Arch. Phys. Med. Rehabil. 2010;91:1332–1338. doi: 10.1016/j.apmr.2010.05.013.
    1. Potter-Nerger M., Volkmann J. Deep brain stimulation for gait and postural symptoms in Parkinson’s disease. Mov. Disord. Off. J. Mov. Disord. Soc. 2013;28:1609–1615. doi: 10.1002/mds.25677.
    1. Wang J.W., Zhang Y.Q., Zhang X.H., Wang Y.P., Li J.P., Li Y.J. Deep Brain Stimulation of Pedunculopontine Nucleus for Postural Instability and Gait Disorder After Parkinson Disease: A Meta-Analysis of Individual Patient Data. World Neurosurg. 2017;102:72–78. doi: 10.1016/j.wneu.2017.02.110.
    1. Baizabal-Carvallo J.F., Alonso-Juarez M. Low-frequency deep brain stimulation for movement disorders. Parkinsonism Relat. Disord. 2016;31:14–22. doi: 10.1016/j.parkreldis.2016.07.018.
    1. Xie T., Bloom L., Padmanaban M., Bertacchi B., Kang W., MacCracken E., Dachman A., Vigil J., Satzer D., Zadikoff C., et al. Long-term effect of low frequency stimulation of STN on dysphagia, freezing of gait and other motor symptoms in PD. J. Neurol. Neurosurg. Psychiatry. 2018;89:989–994. doi: 10.1136/jnnp-2018-318060.
    1. Debaere F., Wenderoth N., Sunaert S., Van Hecke P., Swinnen S.P. Internal vs external generation of movements: Differential neural pathways involved in bimanual coordination performed in the presence or absence of augmented visual feedback. NeuroImage. 2003;19:764–776. doi: 10.1016/S1053-8119(03)00148-4.
    1. Cunnington R., Iansek R., Bradshaw J.L., Phillips J.G. Movement-related potentials in Parkinson’s disease. Presence and predictability of temporal and spatial cues. Pt 4Brain. 1995;118:935–950. doi: 10.1093/brain/118.4.935.
    1. Georgiou N., Iansek R., Bradshaw J.L., Phillips J.G., Mattingley J.B., Bradshaw J.A. An evaluation of the role of internal cues in the pathogenesis of parkinsonian hypokinesia. Pt 6Brain. 1993;116:1575–1587. doi: 10.1093/brain/116.6.1575.
    1. Ferrarin M., Rizzone M., Lopiano L., Recalcati M., Pedotti A. Effects of subthalamic nucleus stimulation and L-dopa in trunk kinematics of patients with Parkinson’s disease. Gait Posture. 2004;19:164–171. doi: 10.1016/S0966-6362(03)00058-4.
    1. Redgrave P., Rodriguez M., Smith Y., Rodriguez-Oroz M.C., Lehericy S., Bergman H., Agid Y., DeLong M.R., Obeso J.A. Goal-directed and habitual control in the basal ganglia: Implications for Parkinson’s disease. Nat. Rev. Neurosci. 2010;11:760–772. doi: 10.1038/nrn2915.
    1. Benninger F., Khlebtovsky A., Roditi Y., Keret O., Steiner I., Melamed E., Djaldetti R. Beneficial effect of levodopa therapy on stooped posture in Parkinson’s disease. Gait Posture. 2015;42:263–268. doi: 10.1016/j.gaitpost.2015.05.015.
    1. Weiss D., Schoellmann A., Fox M.D., Bohnen N.I., Factor S.A., Nieuwboer A., Hallett M., Lewis S.J.G. Freezing of gait: Understanding the complexity of an enigmatic phenomenon. Brain. 2019 doi: 10.1093/brain/awz314.
    1. Abbruzzese G., Berardelli A. Sensorimotor integration in movement disorders. Mov. Disord. 2003;18:231–240. doi: 10.1002/mds.10327.
    1. Zia S., Cody F., O’Boyle D. Joint position sense is impaired by Parkinson’s disease. Ann. Neurol. 2000;47:218–228. doi: 10.1002/1531-8249(200002)47:2<218::AID-ANA12>;2-#.
    1. Schubert M., Prokop T., Brocke F., Berger W. Visual kinesthesia and locomotion in Parkinson’s disease. Mov. Disord. Off. J. Mov. Disord. Soc. 2005;20:141–150. doi: 10.1002/mds.20281.
    1. Baroni A., Benvenuti F., Fantini L., Pantaleo T., Urbani F. Human ballistic arm abduction movements: Effects of L-dopa treatment in Parkinson’s disease. Neurology. 1984;34:868–876. doi: 10.1212/WNL.34.7.868.
    1. Obeso J.A., Rodriguez-Oroz M.C., Benitez-Temino B., Blesa F.J., Guridi J., Marin C., Rodriguez M. Functional organization of the basal ganglia: Therapeutic implications for Parkinson’s disease. Mov. Disord. 2008;23(Suppl. 3):S548–S559. doi: 10.1002/mds.22062.
    1. Magrinelli F., Picelli A., Tocco P., Federico A., Roncari L., Smania N., Zanette G., Tamburin S. Pathophysiology of Motor Dysfunction in Parkinson’s Disease as the Rationale for Drug Treatment and Rehabilitation. Parkinsons Dis. 2016;2016:9832839. doi: 10.1155/2016/9832839.
    1. Sweeney D., Quinlan L.R., Browne P., Richardson M., Meskell P., ÓLaighin G. A Technological Review of Wearable Cueing Devices Addressing Freezing of Gait in Parkinson’s Disease. Sensors. 2019;19:1277. doi: 10.3390/s19061277.
    1. Nieuwboer A. Cueing for freezing of gait in patients with Parkinson’s disease: A rehabilitation perspective. Mov. Disord. 2008;23(Suppl. 2):S475–S481. doi: 10.1002/mds.21978.
    1. Nieuwboer A., Kwakkel G., Rochester L., Jones D., van Wegen E., Willems A.M., Chavret F., Hetherington V., Baker K., Lim I. Cueing training in the home improves gait-related mobility in Parkinson’s disease: The RESCUE trial. J. Neurol. Neurosurg. Psychiatry. 2007;78:134–140. doi: 10.1136/jnnp.200X.097923.
    1. Amirnovin R., Williams Z.M., Cosgrove G.R., Eskandar E.N. Visually guided movements suppress subthalamic oscillations in Parkinson’s disease patients. J. Neurosci. 2004;24:11302–11306. doi: 10.1523/JNEUROSCI.3242-04.2004.
    1. Sarma S.V., Cheng M.L., Eden U., Williams Z., Brown E.N., Eskandar E. The effects of cues on neurons in the basal ganglia in Parkinson’s disease. Front. Integr. Neurosci. 2012;6:40. doi: 10.3389/fnint.2012.00040.
    1. Glickstein M., Stein J. Paradoxical movement in Parkinson’s disease. Trends Neurosci. 1991;14:480–482. doi: 10.1016/0166-2236(91)90055-Y.
    1. Ashoori A., Eagleman D.M., Jankovic J. Effects of Auditory Rhythm and Music on Gait Disturbances in Parkinson’s Disease. Front. Neurol. 2015;6:234. doi: 10.3389/fneur.2015.00234.
    1. Ginis P., Nackaerts E., Nieuwboer A., Heremans E. Cueing for people with Parkinson’s disease with freezing of gait: A narrative review of the state-of-the-art and novel perspectives. Ann. Phys. Rehabil. Med. 2018;61:407–413. doi: 10.1016/j.rehab.2017.08.002.
    1. Griffin H.J., Greenlaw R., Limousin P., Bhatia K., Quinn N.P., Jahanshahi M. The effect of real and virtual visual cues on walking in Parkinson’s disease. J. Neurol. 2011;258:991–1000. doi: 10.1007/s00415-010-5866-z.
    1. Mancini M., Smulders K., Harker G., Stuart S., Nutt J.G. Assessment of the ability of open-and closed-loop cueing to improve turning and freezing in people with Parkinson’s disease. Sci. Rep. 2018;8:12773. doi: 10.1038/s41598-018-31156-4.
    1. Suteerawattananon M., Morris G.S., Etnyre B.R., Jankovic J., Protas E.J. Effects of visual and auditory cues on gait in individuals with Parkinson’s disease. J. Neurol. Sci. 2004;219:63–69. doi: 10.1016/j.jns.2003.12.007.
    1. Lu C., Amundsen Huffmaster S.L., Tuite P.J., Vachon J.M., MacKinnon C.D. Effect of Cue Timing and Modality on Gait Initiation in Parkinson Disease With Freezing of Gait. Arch. Phys. Med. Rehabil. 2017;98:1291–1299. doi: 10.1016/j.apmr.2017.01.009.
    1. Thaut M.H., McIntosh G.C., Rice R.R., Miller R.A., Rathbun J., Brault J.M. Rhythmic auditory stimulation in gait training for Parkinson’s disease patients. Mov. Disord. 1996;11:193–200. doi: 10.1002/mds.870110213.
    1. Murgia M., Pili R., Corona F., Sors F., Agostini T.A., Bernardis P., Casula C., Cossu G., Guicciardi M., Pau M. The Use of Footstep Sounds as Rhythmic Auditory Stimulation for Gait Rehabilitation in Parkinson’s Disease: A Randomized Controlled Trial. Front. Neurol. 2018;9:348. doi: 10.3389/fneur.2018.00348.
    1. Hausdorff J.M., Lowenthal J., Herman T., Gruendlinger L., Peretz C., Giladi N. Rhythmic auditory stimulation modulates gait variability in Parkinson’s disease. Eur. J. Neurosci. 2007;26:2369–2375. doi: 10.1111/j.1460-9568.2007.05810.x.
    1. McIntosh G.C., Brown S.H., Rice R.R., Thaut M.H. Rhythmic auditory-motor facilitation of gait patterns in patients with Parkinson’s disease. J. Neurol. Neurosurg. Psychiatry. 1997;62:22–26. doi: 10.1136/jnnp.62.1.22.
    1. Howe T.E., Lovgreen B., Cody F.W., Ashton V.J., Oldham J.A. Auditory cues can modify the gait of persons with early-stage Parkinson’s disease: A method for enhancing parkinsonian walking performance? Clin. Rehabil. 2003;17:363–367. doi: 10.1191/0269215503cr621oa.
    1. Behrman A.L., Teitelbaum P., Cauraugh J.H. Verbal instructional sets to normalise the temporal and spatial gait variables in Parkinson’s disease. J. Neurol. Neurosurg. Psychiatry. 1998;65:580–582. doi: 10.1136/jnnp.65.4.580.
    1. Bagley S., Kelly B., Tunnicliffe N., Turnbull G.I., Walker J.M. The effect of visual cues on the gait of independently mobile Parkinson’s patients. Phyiotherapy. 1991;77:415–420. doi: 10.1016/S0031-9406(10)62035-4.
    1. Lewis G.N., Byblow W.D., Walt S.E. Stride length regulation in Parkinson’s disease: The use of extrinsic, visual cues. Pt 10Brain. 2000;123:2077–2090. doi: 10.1093/brain/123.10.2077.
    1. Sidaway B., Anderson J., Danielson G., Martin L., Smith G. Effects of long-term gait training using visual cues in an individual with Parkinson disease. Phys. Ther. 2006;86:186–194.
    1. Azulay J.P., Mesure S., Amblard B., Blin O., Sangla I., Pouget J. Visual control of locomotion in Parkinson’s disease. Pt 1Brain. 1999;122:111–120. doi: 10.1093/brain/122.1.111.
    1. Luessi F., Mueller L.K., Breimhorst M., Vogt T. Influence of visual cues on gait in Parkinson’s disease during treadmill walking at multiple velocities. J. Neurol. Sci. 2012;314:78–82. doi: 10.1016/j.jns.2011.10.027.
    1. Xu J., Bao T., Lee U.H., Kinnaird C., Carender W., Huang Y., Sienko K.H., Shull P.B. Configurable, wearable sensing and vibrotactile feedback system for real-time postural balance and gait training: Proof-of-concept. J. Neuroeng. Rehabil. 2017;14:102. doi: 10.1186/s12984-017-0313-3.
    1. Gopalai A.A., Senanayake S.M., Kiong L.C., Gouwanda D. Real-time stability measurement system for postural control. J. Bodyw. Mov. Ther. 2011;15:453–464. doi: 10.1016/j.jbmt.2010.10.005.
    1. Van Wegen E., de Goede C., Lim I., Rietberg M., Nieuwboer A., Willems A., Jones D., Rochester L., Hetherington V., Berendse H., et al. The effect of rhythmic somatosensory cueing on gait in patients with Parkinson’s disease. J. Neurol. Sci. 2006;248:210–214. doi: 10.1016/j.jns.2006.05.034.
    1. De Oliveira Souza C., Callil Voos M., Fen Chien H., Ferreira Barbosa A., Brant Rodrigues R., Colucci Fonoff F., Caromano F.A., de Abreu L.C., Reis Barbosa E., Talamoni Fonoff E. Combined auditory and visual cueing provided by eyeglasses influence gait performance in Parkinson Disease patients submitted to deep brain stimulation: A pilot study. Int. Arch. Med. 2015 doi: 10.3823/1731.
    1. Lohnes C.A., Earhart G.M. The impact of attentional, auditory, and combined cues on walking during single and cognitive dual tasks in Parkinson disease. Gait Posture. 2011;33:478–483. doi: 10.1016/j.gaitpost.2010.12.029.
    1. Cubo E., Leurgans S., Goetz C.G. Short-term and practice effects of metronome pacing in Parkinson’s disease patients with gait freezing while in the ‘on’ state: Randomized single blind evaluation. Parkinsonism Relat. Disord. 2004;10:507–510. doi: 10.1016/j.parkreldis.2004.05.001.
    1. Del Olmo M.F., Cudeiro J. Temporal variability of gait in Parkinson disease: Effects of a rehabilitation programme based on rhythmic sound cues. Parkinsonism Relat. Disord. 2005;11:25–33. doi: 10.1016/j.parkreldis.2004.09.002.
    1. Van den Heuvel M.R., Kwakkel G., Beek P.J., Berendse H.W., Daffertshofer A., van Wegen E.E. Effects of augmented visual feedback during balance training in Parkinson’s disease: A pilot randomized clinical trial. Parkinsonism Relat. Disord. 2014;20:1352–1358. doi: 10.1016/j.parkreldis.2014.09.022.
    1. Morris M.E., Iansek R., Matyas T.A., Summers J.J. Ability to modulate walking cadence remains intact in Parkinson’s disease. J. Neurol. Neurosurg. Psychiatry. 1994;57:1532–1534. doi: 10.1136/jnnp.57.12.1532.
    1. Shen X., Mak M.K. Balance and Gait Training with Augmented Feedback Improves Balance Confidence in People With Parkinson’s Disease: A Randomized Controlled Trial. Neurorehabil. Neural Repair. 2014;28:524–535. doi: 10.1177/1545968313517752.
    1. Lim I., van Wegen E., de Goede C., Deutekom M., Nieuwboer A., Willems A., Jones D., Rochester L., Kwakkel G. Effects of external rhythmical cueing on gait in patients with Parkinson’s disease: A systematic review. Clin. Rehabil. 2005;19:695–713. doi: 10.1191/0269215505cr906oa.
    1. Nieuwboer A., Baker K., Willems A.M., Jones D., Spildooren J., Lim I., Kwakkel G., Van Wegen E., Rochester L. The short-term effects of different cueing modalities on turn speed in people with Parkinson’s disease. Neurorehabil. Neural Repair. 2009;23:831–836. doi: 10.1177/1545968309337136.
    1. Ford M.P., Malone L.A., Nyikos I., Yelisetty R., Bickel C.S. Gait training with progressive external auditory cueing in persons with Parkinson’s disease. Arch. Phys. Med. Rehabil. 2010;91:1255–1261. doi: 10.1016/j.apmr.2010.04.012.
    1. Marchese R., Diverio M., Zucchi F., Lentino C., Abbruzzese G. The role of sensory cues in the rehabilitation of parkinsonian patients: A comparison of two physical therapy protocols. Mov. Disord. 2000;15:879–883. doi: 10.1002/1531-8257(200009)15:5<879::AID-MDS1018>;2-9.
    1. Frazzitta G., Bertotti G., Ucellini D., Maestri R. Parkinson’s Disease Rehabilitation-a pilot study with 1 year follow-up. Mov. Disord. 2010;25:1762–1763.
    1. Frazzitta G., Maestri R., Uccellini D., Bertotti G., Abelli P. Rehabilitation treatment of gait in patients with Parkinson’s disease with freezing: A comparison between two physical therapy protocols using visual and auditory cues with or without treadmill training. Mov. Disord. 2009;24:1139–1143. doi: 10.1002/mds.22491.
    1. Jellish J., Abbas J.J., Ingalls T., Mahant P., Samanta J., Ospina M., Krishnamurthi N. A System for Real-Time Feedback to Improve Gait and Posture in Parkinson’s Disease. IEEE J. Biomed. Health Inform. 2015;19:1809–1819. doi: 10.1109/JBHI.2015.2472560.
    1. Schlick C., Ernst A., Botzel K., Plate A., Pelykh O., Ilmberger J. Visual cues combined with treadmill training to improve gait performance in Parkinson’s disease: A pilot randomized controlled trial. Clin. Rehabil. 2016;30:463–471. doi: 10.1177/0269215515588836.
    1. Lee N.Y., Lee D.K., Song H.S. Effect of virtual reality dance exercise on the balance, activities of daily living, and depressive disorder status of Parkinson’s disease patients. J. Phys. Ther. Sci. 2015;27:145–147. doi: 10.1589/jpts.27.145.
    1. Liao Y.Y., Yang Y.R., Cheng S.J., Wu Y.R., Fuh J.L., Wang R.Y. Virtual Reality-Based Training to Improve Obstacle-Crossing Performance and Dynamic Balance in Patients With Parkinson’s Disease. Neurorehabil. Neural Repair. 2015;29:658–667. doi: 10.1177/1545968314562111.
    1. Pedreira G., Prazeres A., Cruz D., Gomes I., Monteiro L., Melos A. Virtual games and quality of life in PD-a randomized controlled trial. Adv. Parkinson’s Dis. 2013;2:97–101. doi: 10.4236/apd.2013.24018.
    1. Pompeu J.E., Mendes F.A., Silva K.G., Lobo A.M., Oliveira Tde P., Zomignani A.P., Piemonte M.E. 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;98:196–204. doi: 10.1016/j.physio.2012.06.004.
    1. Yang W.C., Wang H.K., Wu R.M., Lo C.S., Lin K.H. Home-based virtual reality balance training and conventional balance training in Parkinson’s disease: A randomized controlled trial. J. Formos. Med. Assoc. 2016;115:734–743. doi: 10.1016/j.jfma.2015.07.012.
    1. Yen C.Y., Lin K.H., Hu M.H., Wu R.M., Lu T.W., Lin C.H. Effects of virtual reality-augmented balance training on sensory organization and attentional demand for postural control in people with Parkinson disease: A randomized controlled trial. Phys. Ther. 2011;91:862–874. doi: 10.2522/ptj.20100050.
    1. Dockx K., Bekkers E.M., Van den Bergh V., Ginis P., Rochester L., Hausdorff J.M., Mirelman A., Nieuwboer A. Virtual reality for rehabilitation in Parkinson’s disease. Cochrane Database Syst. Rev. 2016;12:CD010760. doi: 10.1002/14651858.CD010760.pub2.
    1. Zijlstra W., Rutgers A.W., Van Weerden T.W. Voluntary and involuntary adaptation of gait in Parkinson’s disease. Gait Posture. 1998;7:53–63. doi: 10.1016/S0966-6362(97)00037-4.
    1. Willems A.M., Nieuwboer A., Chavret F., Desloovere K., Dom R., Rochester L., Jones D., Kwakkel G., Van Wegen E. The use of rhythmic auditory cues to influence gait in patients with Parkinson’s disease, the differential effect for freezers and non-freezers, an explorative study. Disabil. Rehabil. 2006;28:721–728. doi: 10.1080/09638280500386569.
    1. McCoy R.W., Kohl R.M., Elliott S.M., Joyce A.S. The impact of auditory cues on gait control of individuals with Parkinson’s disease. J. Hum. Mov. Stud. 2002;42:229–236.
    1. Rochester L., Baker K., Hetherington V., Jones D., Willems A.M., Kwakkel G., Van Wegen E., Lim I., Nieuwboer A. 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. Spaulding S.J., Barber B., Colby M., Cormack B., Mick T., Jenkins M.E. Cueing and gait improvement among people with Parkinson’s disease: A meta-analysis. Arch. Phys. Med. Rehabil. 2013;94:562–570. doi: 10.1016/j.apmr.2012.10.026.
    1. Wu T., Hallett M. Neural correlates of dual task performance in patients with Parkinson’s disease. J. Neurol. Neurosurg. Psychiatry. 2008;79:760–766. doi: 10.1136/jnnp.2007.126599.
    1. Badarny S., Aharon-Peretz J., Susel Z., Habib G., Baram Y. Virtual reality feedback cues for improvement of gait in patients with Parkinson’s disease. Tremor Other Hyperkinetic Mov. 2014;4:225. doi: 10.7916/D8V69GM4.
    1. Machado J.P.F. Smartphone Based Closed-Loop Auditory Cueing System. [(accessed on 4 October 2019)];2014 Available online: .
    1. Ginis P., Nieuwboer A., Dorfman M., Ferrari A., Gazit E., Canning C.G., Rocchi L., Chiari L., Hausdorff J.M., Mirelman A. Feasibility and effects of home-based smartphone-delivered automated feedback training for gait in people with Parkinson’s disease: A pilot randomized controlled trial. Parkinsonism Relat. Disord. 2016;22:28–34. doi: 10.1016/j.parkreldis.2015.11.004.
    1. Chomiak T., Sidhu A.S., Watts A., Su L., Graham B., Wu J., Classen S., Falter B., Hu B. Development and Validation of Ambulosono: A Wearable Sensor for Bio-Feedback Rehabilitation Training. Sensors. 2019;19:686. doi: 10.3390/s19030686.
    1. Bartels B.M., Moreno A., Quezada M.J., Sivertson H., Abbas J., Krishnamurthi N. Real-Time Feedback Derived from Wearable Sensors to Improve Gait in Parkinson’s Disease. Technol. Innov. 2018;20:37–46. doi: 10.21300/20.1-2.2018.37.
    1. Thompson E., Agada P., Wright W.G., Reimann H., Jeka J. Spatiotemporal gait changes with use of an arm swing cueing device in people with Parkinson’s disease. Gait Posture. 2017;58:46–51. doi: 10.1016/j.gaitpost.2017.07.001.
    1. Baskaran D. Real-Time Feedback Training to Improve Gait and Posture in Parkinson’s Disease. Arizona State University; Tempe, AZ, USA: 2017.
    1. Krishnamurthi N., Baskaran D., Parikh S., Venugopal V., Muthukrishnan N., Driver-Dunckley E., Mahant P., Ospina M.C., Abbas J.J. Real-Time Feedback during Treadmill Training for Individuals with Parkinson’s Disease. Society for Neuroscience; Chicago, IL, USA: 2019. p. 1.
    1. Morris M.E., Iansek R., Matyas T.A., Summers J.J. Stride length regulation in Parkinson’s disease. Normalization strategies and underlying mechanisms. Pt 2Brain. 1996;119:551–568. doi: 10.1093/brain/119.2.551.
    1. Schlick C., Struppler A., Boetzel K., Plate A., Ilmberger J. Dynamic visual cueing in combination with treadmill training for gait rehabilitation in Parkinson disease. Am. J. Phys. Med. Rehabil. 2012;91:75–79. doi: 10.1097/PHM.0b013e3182389fe2.
    1. Mirelman A., Rochester L., Maidan I., Del Din S., Alcock L., Nieuwhof F., Rikkert M.O., Bloem B.R., Pelosin E., Avanzino L., 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;388:1170–1182. doi: 10.1016/S0140-6736(16)31325-3.
    1. Carpinella I., Cattaneo D., Bonora G., Bowman T., Martina L., Montesano A., Ferrarin M. Wearable Sensor-Based Biofeedback Training for Balance and Gait in Parkinson Disease: A Pilot Randomized Controlled Trial. Arch. Phys. Med. Rehabil. 2017;98:622–630. doi: 10.1016/j.apmr.2016.11.003.
    1. Espay A.J., Baram Y., Dwivedi A.K., Shukla R., Gartner M., Gaines L., Duker A.P., Revilla F.J. At-home training with closed-loop augmented-reality cueing device for improving gait in patients with Parkinson disease. J. Rehabil. Res. Dev. 2010;47:573. doi: 10.1682/JRRD.2009.10.0165.
    1. Karatsidis A., Richards R.E., Konrath J.M., van den Noort J.C., Schepers H.M., Bellusci G., Harlaar J., Veltink P.H. Validation of wearable visual feedback for retraining foot progression angle using inertial sensors and an augmented reality headset. J. Neuroeng. Rehabil. 2018;15:78. doi: 10.1186/s12984-018-0419-2.
    1. Young W.R., Shreve L., Quinn E.J., Craig C., Bronte-Stewart H. Auditory cueing in Parkinson’s patients with freezing of gait. What matters most: Action-relevance or cue-continuity? Neuropsychologia. 2016;87:54–62. doi: 10.1016/j.neuropsychologia.2016.04.034.
    1. Pereira M.P., Gobbi L.T., Almeida Q.J. Freezing of gait in Parkinson’s disease: Evidence of sensory rather than attentional mechanisms through muscle vibration. Parkinsonism Relat. Disord. 2016;29:78–82. doi: 10.1016/j.parkreldis.2016.05.021.
    1. Rocha P.A., Porfirio G.M., Ferraz H.B., Trevisani V.F. Effects of external cues on gait parameters of Parkinson’s disease patients: A systematic review. Clin. Neurol. Neurosurg. 2014;124:127–134. doi: 10.1016/j.clineuro.2014.06.026.
    1. Bhatt T., Yang F., Mak M.K., Hui-Chan C.W., Pai Y.C. Effect of externally cued training on dynamic stability control during the sit-to-stand task in people with Parkinson disease. Phys. Ther. 2013;93:492–503. doi: 10.2522/ptj.20100423.
    1. Mak M.K., Hui-Chan C.W. Audiovisual cues can enhance sit-to-stand in patients with Parkinson’s disease. Mov. Disord. 2004;19:1012–1019. doi: 10.1002/mds.20196.
    1. Schlenstedt C., Mancini M., Horak F., Peterson D. Anticipatory Postural Adjustment during Self-Initiated, Cued, and Compensatory Stepping in Healthy Older Adults and Patients With Parkinson Disease. Arch. Phys. Med. Rehabil. 2017;98:1316–1324. doi: 10.1016/j.apmr.2017.01.023.
    1. Lopez W.O., Higuera C.A., Fonoff E.T., Souza Cde O., Albicker U., Martinez J.A. Listenmee and Listenmee smartphone application: Synchronizing walking to rhythmic auditory cues to improve gait in Parkinson’s disease. Hum. Mov. Sci. 2014;37:147–156. doi: 10.1016/j.humov.2014.08.001.
    1. Muthukrishnan N., Turaga P., Abbas J.J., Ingalls T., Krishnamurthi N. Gait and Balance Monitoring Using Wearable Technology for Real-Time Feedback in Parkinson’s Disease. Society for Neuroscience; Chicago, IL, USA: 2019. p. 1.

Source: PubMed

3
Abonnieren