Assessment of the ability of open- and closed-loop cueing to improve turning and freezing in people with Parkinson's disease

Martina Mancini, Katrijn Smulders, Graham Harker, Samuel Stuart, John G Nutt, Martina Mancini, Katrijn Smulders, Graham Harker, Samuel Stuart, John G Nutt

Abstract

Turning impairments are common in Parkinson's disease (PD) and can elicit freezing of gait (FoG). Extensive examination of open-loop cueing interventions has demonstrated that they can ameliorate gait deficits in PD; less is known about efficacy to improve turning. Here, we investigate the immediate effectiveness of open- and closed-loop cueing in improving turning characteristics in people with PD. Twenty-five subjects with and 18 subjects without FoG participated in the study. Subjects turned in place for one minute under single- and dual-task for 3 randomized conditions: (i) Baseline; (ii) Turning to the beat of a metronome (open-loop); and (iii) Turning with phase-dependent tactile biofeedback (closed-loop). Objective measures of freezing, such as % time spent freezing and FoG-ratio, significantly improved when turning with both open-loop and closed-loop cueing compared to baseline. Dual-tasking did not worsen FoG in freezers, but significantly slowed down turns in both groups. Both cueing modalities significantly improved turning smoothness in both groups, but reduced turning velocity and number of turns compared to baseline. Both open and closed-loop cueing markedly improved turning in people with PD. These preliminary observations warrant further exploration of vibrotactile closed-loop cueing to improve mobility in everyday life.

Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
(A) Representative power spectral densities of the AP acceleration of the shins for baseline, open-loop, and closed-loop conditions together with the relative FoG ratio for that example. Right panel, freezing severity across the 3 conditions, measured by the (B) % time spent freezing (only in freezers) and (C) the FoG ratio (freezers and non freezers).
Figure 2
Figure 2
Association between the baseline FoG ratio at baseline and the delta change in the FoG ratio with the use of close- or open-loop cueing. In addition, association between the delta changes, close-loop cueing versus open-loop cueing has been reported in both freezers and non freezers.
Figure 3
Figure 3
Representative data in a subject with FoG from trunk and shins sensors while turning during baseline, open-loop cueing, and closed-loop cueing. Grey shaded areas show turn duration while pink areas show data during freezing of gait episodes.

References

    1. Stack E, Ashburn A. Dysfunctional turning in Parkinson’s disease. Disability and rehabilitation. 2008;30(16):1222–9. doi: 10.1080/09638280701829938.
    1. Stack EL, Ashburn AM, Jupp KE. Strategies used by people with Parkinson’s disease who report difficulty turning. Parkinsonism & related disorders. 2006;12(2):87–92. doi: 10.1016/j.parkreldis.2005.08.008.
    1. Morris ME, Huxham FE, McGinley J, Iansek R. Gait disorders and gait rehabilitation in Parkinson’s disease. Adv Neurol. 2001;87:347–61.
    1. Huxham F, Baker R, Morris ME, Iansek R. Head and trunk rotation during walking turns in Parkinson’s disease. Movement disorders: official journal of the Movement Disorder Society. 2008;23(10):1391–7. doi: 10.1002/mds.21943.
    1. Visser JE, et al. Quantification of trunk rotations during turning and walking in Parkinson’s disease. Clinical neurophysiology: official journal of the International Federation of Clinical Neurophysiology. 2007;118(7):1602–6. doi: 10.1016/j.clinph.2007.03.010.
    1. Hong M, Perlmutter JS, Earhart GM. A kinematic and electromyographic analysis of turning in people with Parkinson disease. Neurorehabilitation and neural repair. 2009;23(2):166–76. doi: 10.1177/1545968308320639.
    1. Huxham F, Baker R, Morris ME, Iansek R. Footstep adjustments used to turn during walking in Parkinson’s disease. Movement disorders: official journal of the Movement Disorder Society. 2008;23(6):817–23. doi: 10.1002/mds.21932.
    1. Mak MK, Patla A, Hui-Chan C. Sudden turn during walking is impaired in people with Parkinson’s disease. Experimental brain research. 2008;190(1):43–51. doi: 10.1007/s00221-008-1446-1.
    1. Crenna P, et al. The association between impaired turning and normal straight walking in Parkinson’s disease. Gait & posture. 2007;26(2):172–8. doi: 10.1016/j.gaitpost.2007.04.010.
    1. Ashburn A, et al. Sequence and onset of whole-body coordination when turning in response to a visual trigger: comparing people with Parkinson’s disease and healthy adults. Gait Posture. 2014;39(1):278–83. doi: 10.1016/j.gaitpost.2013.07.128.
    1. Mancini, M. et al. The Clinical Significance Of Freezing While Turning in Parkinson’s Disease. Neuroscience; In press: (2016).
    1. Spildooren J, et al. Freezing of gait in Parkinson’s disease: the impact of dual-tasking and turning. Movement disorders: official journal of the Movement Disorder Society. 2010;25(15):2563–70. doi: 10.1002/mds.23327.
    1. Snijders AH, Haaxma CA, Hagen YJ, Munneke M, Bloem BR. Freezer or non-freezer: clinical assessment of freezing of gait. Parkinsonism & related disorders. 2012;18(2):149–54. doi: 10.1016/j.parkreldis.2011.09.006.
    1. Zach H, et al. Identifying freezing of gait in Parkinson’s disease during freezing provoking tasks using waist-mounted accelerometry. Parkinsonism & related disorders. 2015;21(11):1362–6. doi: 10.1016/j.parkreldis.2015.09.051.
    1. Giladi N, et al. Freezing of gait in patients with advanced Parkinson’s disease. J Neural Transm. 2001;108(1):53–61. doi: 10.1007/s007020170096.
    1. Nutt JG, et al. Freezing of gait: moving forward on a mysterious clinical phenomenon. The Lancet Neurology. 2011;10(8):734–44. doi: 10.1016/S1474-4422(11)70143-0.
    1. Bohnen NI, Albin RL, Muller ML, Chou K. Advances in Therapeutic Options for Gait and Balance in Parkinson’s Disease. US neurology. 2011;7(2):100–8. doi: 10.17925/USN.2011.07.02.100.
    1. Morris ME, Iansek R, Galna B. Gait festination and freezing in Parkinson’s disease: pathogenesis and rehabilitation. Mov Disord; 2008;23(Suppl 2):S451–60. doi: 10.1002/mds.21974.
    1. Nieuwboer A, et al. Cueing training in the home improves gait-related mobility in Parkinson’s disease: the RESCUE trial. Journal of neurology, neurosurgery, and psychiatry. 2007;78(2):134–40. doi: 10.1136/jnnp.200X.097923.
    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 (2017).
    1. McCandless PJ, et al. Effect of three cueing devices for people with Parkinson’s disease with gait initiation difficulties. Gait Posture. 2016;44:7–11. doi: 10.1016/j.gaitpost.2015.11.006.
    1. Zhao Y, et al. Feasibility of external rhythmic cueing with the Google Glass for improving gait in people with Parkinson’s disease. Journal of neurology. 2016;263(6):1156–65. doi: 10.1007/s00415-016-8115-2.
    1. Spildooren J, et al. Influence of Cueing and an Attentional Strategy on Freezing of Gait in Parkinson Disease During Turning. Journal of neurologic physical therapy: JNPT. 2017;41(2):129–35. doi: 10.1097/NPT.0000000000000178.
    1. Spildooren J, et al. Turning and unilateral cueing in Parkinson’s disease patients with and without freezing of gait. Neuroscience. 2012;207:298–306. doi: 10.1016/j.neuroscience.2012.01.024.
    1. Barthel C, et al. The laser shoes: A new ambulatory device to alleviate freezing of gait in Parkinson disease. Neurology; 2018;90(2):e164–e71. doi: 10.1212/WNL.0000000000004795.
    1. Ferraye MU, Fraix V, Pollak P, Bloem BR, Debu B. The laser-shoe: A new form of continuous ambulatory cueing for patients with Parkinson’s disease. Parkinsonism & related disorders. 2016;29:127–8. doi: 10.1016/j.parkreldis.2016.05.004.
    1. Ginis P, et al. 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 & related disorders. 2016;22:28–34. doi: 10.1016/j.parkreldis.2015.11.004.
    1. Harrington, W. et al. Alleviating Freezing of Gait using phase-dependent tactile biofeedback. Conference proceedings: Annual International Conference of the IEEE Engineering in Medicine and Biology Society IEEE Engineering in Medicine and Biology Society Annual Conference; 2016, 5841–4 (2016).
    1. Ginis P, et al. External input for gait in people with Parkinson’s disease with and without freezing of gait: One size does not fit all. Journal of neurology. 2017;264(7):1488–96. doi: 10.1007/s00415-017-8552-6.
    1. Espay AJ, et al. At-home training with closed-loop augmented-reality cueing device for improving gait in patients with Parkinson disease. Journal of rehabilitation research and development. 2010;47(6):573–81. doi: 10.1682/JRRD.2009.10.0165.
    1. Helmich RC, de Lange FP, Bloem BR, Toni I. Cerebral compensation during motor imagery in Parkinson’s disease. Neuropsychologia. 2007;45(10):2201–15. doi: 10.1016/j.neuropsychologia.2007.02.024.
    1. Wright, W. G. et al. Axial kinesthesia is impaired in Parkinson’s disease: effects of levodopa. Exp Neurol;225(1) 202–9.
    1. Wright WG, Gurfinkel V, King L, Horak F. Parkinson’s disease shows perceptuomotor asymmetry unrelated to motor symptoms. Neurosci Lett. 2007;417(1):10–5. doi: 10.1016/j.neulet.2007.02.016.
    1. Almeida QJ, Lebold CA. Freezing of gait in Parkinson’s disease: a perceptual cause for a motor impairment? J Neurol Neurosurg Psychiatry. 2010;81(5):513–8. doi: 10.1136/jnnp.2008.160580.
    1. Snijders AH, Toni I, Ruzicka E, Bloem BR. Bicycling breaks the ice for freezers of gait. Movement disorders: official journal of the Movement Disorder Society. 2011;26(3):367–71. doi: 10.1002/mds.23530.
    1. Snijders AH, van Kesteren M, Bloem BR. Cycling is less affected than walking in freezers of gait. Journal of neurology, neurosurgery, and psychiatry. 2012;83(5):575–6. doi: 10.1136/jnnp-2011-300375.
    1. Novak P, Novak V. Effect of step-synchronized vibration stimulation of soles on gait in Parkinson’s disease: a pilot study. Journal of neuroengineering and rehabilitation. 2006;3:9. doi: 10.1186/1743-0003-3-9.
    1. Jacobs JV, Nutt JG, Carlson-Kuhta P, Stephens M, Horak FB. Knee trembling during freezing of gait represents multiple anticipatory postural adjustments. Exp Neurol. 2009;215(2):334–41. doi: 10.1016/j.expneurol.2008.10.019.
    1. De Nunzio AM, Grasso M, Nardone A, Godi M, Schieppati M. Alternate rhythmic vibratory stimulation of trunk muscles affects walking cadence and velocity in Parkinson’s disease. Clinical neurophysiology: official journal of the International Federation of Clinical Neurophysiology. 2010;121(2):240–7. doi: 10.1016/j.clinph.2009.10.018.
    1. Nieuwboer A. Cueing for freezing of gait in patients with Parkinson’s disease: a rehabilitation perspective. Mov Disord; 2008;23(Suppl 2):S475–81. doi: 10.1002/mds.21978.
    1. Morris TR, et al. A comparison of clinical and objective measures of freezing of gait in Parkinson’s disease. Parkinsonism & related disorders. 2012;18(5):572–7. doi: 10.1016/j.parkreldis.2012.03.001.
    1. Mancini, M., Weiss, A., Herman, T. & Hausdorff, J. M. Turn Around Freezing: Community-Living Turning Behavior in People with Parkinson’s Disease. Frontiers in Neurology; 9(18) (2018).
    1. Nantel J, de Solages C, Bronte-Stewart H. Repetitive stepping in place identifies and measures freezing episodes in subjects with Parkinson’s disease. Gait Posture. 2011;34(3):329–33. doi: 10.1016/j.gaitpost.2011.05.020.
    1. Curtze C, Nutt JG, Carlson-Kuhta P, Mancini M, Horak FB. Levodopa Is a Double-Edged Sword for Balance and Gait in People With Parkinson’s Disease. Movement disorders: official journal of the Movement Disorder Society. 2015;30(10):1361–70. doi: 10.1002/mds.26269.
    1. Mellone S, Mancini M, King LA, Horak FB, Chiari L. The quality of turning in Parkinson’s disease: a compensatory strategy to prevent postural instability? Journal of neuroengineering and rehabilitation. 2016;13:39. doi: 10.1186/s12984-016-0147-4.
    1. Munoz-Hellin E, Cano-de-la-Cuerda R, Miangolarra-Page JC. Visual cues as a therapeutic tool in Parkinson’s disease. A systematic review. Revista espanola de geriatria y gerontologia. 2013;48(4):190–7. doi: 10.1016/j.regg.2013.03.002.
    1. Morris ME, Iansek R, Matyas TA, Summers JJ. Stride length regulation in Parkinson’s disease. Normalization strategies and underlying mechanisms. Brain. 1996;119(Pt 2):551–68. doi: 10.1093/brain/119.2.551.
    1. Stuart S, Lord S, Hill E, Rochester L. Gait in Parkinson’s disease: a visuo-cognitive challenge. Neuroscience & Biobehavioral Reviews. 2016;62:76–88. doi: 10.1016/j.neubiorev.2016.01.002.
    1. Vitorio R, et al. Visual cues and gait improvement in Parkinson’s disease: which piece of information is really important? Neuroscience. 2014;277:273–80. doi: 10.1016/j.neuroscience.2014.07.024.
    1. Maidan I, et al. Changes in oxygenated hemoglobin link freezing of gait to frontal activation in patients with Parkinson disease: an fNIRS study of transient motor-cognitive failures. Journal of neurology. 2015;262(4):899–908. doi: 10.1007/s00415-015-7650-6.
    1. Lewis SJ, Barker RA. A pathophysiological model of freezing of gait in Parkinson’s disease. Parkinsonism & related disorders. 2009;15(5):333–8. doi: 10.1016/j.parkreldis.2008.08.006.
    1. Wu T, Hallett M, Chan P. Motor automaticity in Parkinson’s disease. Neurobiol Dis. 2015;82:226–34. doi: 10.1016/j.nbd.2015.06.014.
    1. Gilat M, et al. Dopamine depletion impairs gait automaticity by altering cortico-striatal and cerebellar processing in Parkinson’s disease. NeuroImage. 2017;152:207–20. doi: 10.1016/j.neuroimage.2017.02.073.
    1. Nieuwboer A, et al. Reliability of the new freezing of gait questionnaire: agreement between patients with Parkinson’s disease and their carers. Gait Posture. 2009;30(4):459–63. doi: 10.1016/j.gaitpost.2009.07.108.
    1. Goetz CG, et al. Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Movement disorders: official journal of the Movement Disorder Society. 2008;23(15):2129–70. doi: 10.1002/mds.22340.
    1. Stebbins GT, et al. How to identify tremor dominant and postural instability/gait difficulty groups with the movement disorder society unified Parkinson’s disease rating scale: comparison with the unified Parkinson’s disease rating scale. Movement disorders: official journal of the Movement Disorder Society. 2013;28(5):668–70. doi: 10.1002/mds.25383.
    1. Nasreddine ZS, et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. Journal of the American Geriatrics Society. 2005;53(4):695–9. doi: 10.1111/j.1532-5415.2005.53221.x.
    1. Buchman AS, Wilson RS, Leurgans S, Bennett DA. Vibratory thresholds and mobility in older persons. Muscle Nerve. 2009;39(6):754–60. doi: 10.1002/mus.21263.

Source: PubMed

Patrocinadores e Colaboradores

Condições médicas

Intervenções de drogas

3
Se inscrever