Effect of On-Demand Cueing on Freezing of Gait in Parkinson’s Patients
Gait disturbance, particularly freezing of gait (FOG), is a phenomenon that is common in Parkinson’s patients and significantly contributes to a loss of function and independence. Walking performance and number of freezing episodes have been known to respond favorably to sensory cues of different modalities. However, a topic that has so far barely been touched is how to resolve freezing episodes via sensory cues once they have appeared. In this study, we analyze the effect of five different sensory cues on the duration of freezing episodes: (1) vibratory alert, (2) auditory alert, (3) vibratory rhythm, (4) auditory rhythm, (5) visual cue in form of parallel lines projected to the floor. The motivation for this study is to investigate the possibility of the design of a gait assistive device for Parkinson’s patients. Test subjects were 7 Parkinson’s patients regularly suffering from FOG. The patients had to repeatedly walk a pre-defined course and cues were triggered always 2 s after freezing onset. The effect was analyzed via experimental measurements and patient interviews. The measurements showed that all 5 sensory cues led to a decrease of the average duration of freezing: baseline (7.9s), vibratory alert (7.1s), auditory alert (6.7s), auditory rhythm (6.4s), vibratory rhythm (6.3s), and visual cue (5.3s). Nevertheless, interestingly, patients subjectively evaluated the audio alert and vibratory signals to have a significantly better effect for reducing their freezing duration than the visual cue.
[1] S. Bagley, B. Kelly, N. Tunnicliffe, G. I. Turnbull, and J. M. Walker.
The effect of visual cues on the gait of independently mobile parkinson’s
disease patients. Physiotherapy, 77:415–420, 1991.
[2] M. E. Morris, R. Iansek, T. A. Matyas, and J. J. Summers. Stride length
regulation in parkinson’s disease. Normalization strategies and
underlying mechanisms. Brain, 119 (Pt 2):551–568, Apr 1996.
[3] J. P. Azulay, C. Van Den Brand, D. Mestre, O. Blin, I. Sangla, J. Pouget,
and G. Serratrice. Automatic motion analysis of gait in patients with
parkinson disease: effects of levodopa and visual stimulations. Rev
Neurol (Paris), 152(2):128–134, Feb 1996.
[4] J. P. Azulay, S. Mesure, B. Amblard, O. Blin, I. Sangla, and J. Pouget.
Visual control of locomotion in parkinson’s disease. Brain, 122 (Pt
1):111–120, Jan 1999.
[5] G. N. Lewis, W. D. Byblow, and S. E. Walt. Stride length regulation in
parkinson’s disease: the use of extrinsic, visual cues. Brain, 123 (Pt
10):2077–2090, Oct 2000.
[6] W. Enzensberger, P. A. Fischer. Metronome in parkinson’s disease.
Lancet, 347, 1996.
[7] G.C McIntosh, S.H. Brown, R.R. Rice, and M.H. Thaut. Rhythmic
auditory-motor facilitation of gait patterns in patients with parkinson’s
disease. J. Neurol. Neurosurg. Psychiatry, 62:22–26, 1997.
[8] N. Ito, A. Hayshi, W. Lin, N. Ohkoshi, M. Watanabe, and S. Shoji.
Integrated human brain science: theory, method, application (music),
chapter Music therapy in parkinson’s disease: Improvement of
Parkinsonian gait and depression with rhythmic auditory stimulation,
pages 435–443. Elsevier, 2000.
[9] P. Arias and J. Cudeiro. Effect of Rhythmic Auditory Stimulation on
Gait in Parkinsonian Patients with and without Freezing of Gait, PLoS
ONE 5(3): e9675. doi:10.1371/journal.pone.0009675, 2010.
[10] M. S. Bryant. An evaluation of self-administration of auditory cueing to
improve gait in people with Parkinson's disease, Disabil Rehabil Assist
Technol. 4(5): 357–363, 2009.
[11] E. van Wegen, C. de Goede, I. Lim, M. Rietberg, A. Nieuwboer, A.
Willems, D. Jones, L. Rochester, V. Hetherington, and H. Berendse. The
effect of rhythmic somatosensory cueing on gait in patients with
parkinson’s disease. Journal of the Neurological Sciences, 248:210–214,
2006.
[12] M. A. Dietz, C. G. Goetz, and G. T. Stebbins. Evaluation of a modified
inverted walking stick as a treatment for parkinsonian freezing episodes.
Mov Disord, 5(3):243–247, 1990.
[13] K. Kompoliti, C. G. Goetz, S. Leurgans, M. Morrissey, and I. M. Siegel,
“On“ freezing in Parkinson's disease: Resistance to visual cue walking
devices, Movement Disorders, Volume 15 Issue 2, Pages 309–312,
2001.
[14] E. Cubo, S. Leurgans, and C. G. Goetz. 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
and Related Disorders, 10(8), 507-510, 2004
[15] A. Burleigh-Jacobs, F. B. Horak, J. G. Nutt, and J. A. Obeso. Step
initiation in parkinson’s disease: influence of levodopa and external
sensory triggers. Mov Disord, 12(2):206–215, Mar 1997.
[16] L. E Dibble, D. E Nicholson, B. Shultz, B. A. MacWilliams, R. L.
Marcus, and C. Moncur. Sensory cueing effects on maximal speed gait
initiation in persons with parkinson’s disease and healthy elders. Gait
Posture, 19(3):215–225, Jun 2004.
[17] Y. Jiang and K. E. Norman. Effects of visual and auditory cues on gait
initiation in people with parkinson’s disease. Clin Rehabil, 20(1):36–45,
Jan 2006.
[18] A. Nieuwboer, K. Baker, A.-M. Willems, D. Jones, J. Spildooren, I. Lim,
G. Kwakkel, E. Van Wegen, and L. Rochester. The short-term effects of
different cueing modalities on turn speed in people with parkinson’s
disease. Neurorehabil Neural Repair, 23(8):831–836, Oct 2009.
[19] A.-M. Willems, A. Nieuwboer, F. Chavret, K. Desloovere, R. Dom, L.
Rochester, G. Kwakkel, E. van Wegen, and D. Jones. Turning in
parkinson’s disease patients and controls: The effect of auditory cues.
Movement Disorders, 21:1871–1878, 2007.
[20] R. Velik, U. Hoffmann, H. Zabaleta, and J. F. Martí-Massó. Effect of
sensory cues applied at the onset of freezing episodes in parkinson’s
disease patients, International Journal of Medical and Biological
Sciences, Volume 6, pp. 57–62, 2012.
[21] R. Velik, U. Hoffmann, H. Zabaleta, J. F. Martí Massó, and T. Keller.
The effect of visual cues on the number and duration of freezing
episodes in parkinson’s patients, EMBS, 2012.
[22] N. Giladi, H. Shabtai, E. S. Simon, S. Biran, J. Tal, and A. D. Korczyn,
Construction of freezing of gait questionnaire for patients with
Parkinsonism, Parkinsonism and Related Disorders 6 (2000) 165–170.
[23] K. Kompoliti, C. G. Goetz, S. Leurgans, M. Morrissey, and I. M. Siegel.
‘‘On’’ freezing in parkinson’s disease: resistance to visual cue walking
devices. Mov. Disord 15: 309–312, 2000.
[1] S. Bagley, B. Kelly, N. Tunnicliffe, G. I. Turnbull, and J. M. Walker.
The effect of visual cues on the gait of independently mobile parkinson’s
disease patients. Physiotherapy, 77:415–420, 1991.
[2] M. E. Morris, R. Iansek, T. A. Matyas, and J. J. Summers. Stride length
regulation in parkinson’s disease. Normalization strategies and
underlying mechanisms. Brain, 119 (Pt 2):551–568, Apr 1996.
[3] J. P. Azulay, C. Van Den Brand, D. Mestre, O. Blin, I. Sangla, J. Pouget,
and G. Serratrice. Automatic motion analysis of gait in patients with
parkinson disease: effects of levodopa and visual stimulations. Rev
Neurol (Paris), 152(2):128–134, Feb 1996.
[4] J. P. Azulay, S. Mesure, B. Amblard, O. Blin, I. Sangla, and J. Pouget.
Visual control of locomotion in parkinson’s disease. Brain, 122 (Pt
1):111–120, Jan 1999.
[5] G. N. Lewis, W. D. Byblow, and S. E. Walt. Stride length regulation in
parkinson’s disease: the use of extrinsic, visual cues. Brain, 123 (Pt
10):2077–2090, Oct 2000.
[6] W. Enzensberger, P. A. Fischer. Metronome in parkinson’s disease.
Lancet, 347, 1996.
[7] G.C McIntosh, S.H. Brown, R.R. Rice, and M.H. Thaut. Rhythmic
auditory-motor facilitation of gait patterns in patients with parkinson’s
disease. J. Neurol. Neurosurg. Psychiatry, 62:22–26, 1997.
[8] N. Ito, A. Hayshi, W. Lin, N. Ohkoshi, M. Watanabe, and S. Shoji.
Integrated human brain science: theory, method, application (music),
chapter Music therapy in parkinson’s disease: Improvement of
Parkinsonian gait and depression with rhythmic auditory stimulation,
pages 435–443. Elsevier, 2000.
[9] P. Arias and J. Cudeiro. Effect of Rhythmic Auditory Stimulation on
Gait in Parkinsonian Patients with and without Freezing of Gait, PLoS
ONE 5(3): e9675. doi:10.1371/journal.pone.0009675, 2010.
[10] M. S. Bryant. An evaluation of self-administration of auditory cueing to
improve gait in people with Parkinson's disease, Disabil Rehabil Assist
Technol. 4(5): 357–363, 2009.
[11] E. van Wegen, C. de Goede, I. Lim, M. Rietberg, A. Nieuwboer, A.
Willems, D. Jones, L. Rochester, V. Hetherington, and H. Berendse. The
effect of rhythmic somatosensory cueing on gait in patients with
parkinson’s disease. Journal of the Neurological Sciences, 248:210–214,
2006.
[12] M. A. Dietz, C. G. Goetz, and G. T. Stebbins. Evaluation of a modified
inverted walking stick as a treatment for parkinsonian freezing episodes.
Mov Disord, 5(3):243–247, 1990.
[13] K. Kompoliti, C. G. Goetz, S. Leurgans, M. Morrissey, and I. M. Siegel,
“On“ freezing in Parkinson's disease: Resistance to visual cue walking
devices, Movement Disorders, Volume 15 Issue 2, Pages 309–312,
2001.
[14] E. Cubo, S. Leurgans, and C. G. Goetz. 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
and Related Disorders, 10(8), 507-510, 2004
[15] A. Burleigh-Jacobs, F. B. Horak, J. G. Nutt, and J. A. Obeso. Step
initiation in parkinson’s disease: influence of levodopa and external
sensory triggers. Mov Disord, 12(2):206–215, Mar 1997.
[16] L. E Dibble, D. E Nicholson, B. Shultz, B. A. MacWilliams, R. L.
Marcus, and C. Moncur. Sensory cueing effects on maximal speed gait
initiation in persons with parkinson’s disease and healthy elders. Gait
Posture, 19(3):215–225, Jun 2004.
[17] Y. Jiang and K. E. Norman. Effects of visual and auditory cues on gait
initiation in people with parkinson’s disease. Clin Rehabil, 20(1):36–45,
Jan 2006.
[18] A. Nieuwboer, K. Baker, A.-M. Willems, D. Jones, J. Spildooren, I. Lim,
G. Kwakkel, E. Van Wegen, and L. Rochester. The short-term effects of
different cueing modalities on turn speed in people with parkinson’s
disease. Neurorehabil Neural Repair, 23(8):831–836, Oct 2009.
[19] A.-M. Willems, A. Nieuwboer, F. Chavret, K. Desloovere, R. Dom, L.
Rochester, G. Kwakkel, E. van Wegen, and D. Jones. Turning in
parkinson’s disease patients and controls: The effect of auditory cues.
Movement Disorders, 21:1871–1878, 2007.
[20] R. Velik, U. Hoffmann, H. Zabaleta, and J. F. Martí-Massó. Effect of
sensory cues applied at the onset of freezing episodes in parkinson’s
disease patients, International Journal of Medical and Biological
Sciences, Volume 6, pp. 57–62, 2012.
[21] R. Velik, U. Hoffmann, H. Zabaleta, J. F. Martí Massó, and T. Keller.
The effect of visual cues on the number and duration of freezing
episodes in parkinson’s patients, EMBS, 2012.
[22] N. Giladi, H. Shabtai, E. S. Simon, S. Biran, J. Tal, and A. D. Korczyn,
Construction of freezing of gait questionnaire for patients with
Parkinsonism, Parkinsonism and Related Disorders 6 (2000) 165–170.
[23] K. Kompoliti, C. G. Goetz, S. Leurgans, M. Morrissey, and I. M. Siegel.
‘‘On’’ freezing in parkinson’s disease: resistance to visual cue walking
devices. Mov. Disord 15: 309–312, 2000.
@article{"International Journal of Medical, Medicine and Health Sciences:65104", author = "Rosemarie Velik", title = "Effect of On-Demand Cueing on Freezing of Gait in Parkinson’s Patients", abstract = "Gait disturbance, particularly freezing of gait (FOG), is a phenomenon that is common in Parkinson’s patients and significantly contributes to a loss of function and independence. Walking performance and number of freezing episodes have been known to respond favorably to sensory cues of different modalities. However, a topic that has so far barely been touched is how to resolve freezing episodes via sensory cues once they have appeared. In this study, we analyze the effect of five different sensory cues on the duration of freezing episodes: (1) vibratory alert, (2) auditory alert, (3) vibratory rhythm, (4) auditory rhythm, (5) visual cue in form of parallel lines projected to the floor. The motivation for this study is to investigate the possibility of the design of a gait assistive device for Parkinson’s patients. Test subjects were 7 Parkinson’s patients regularly suffering from FOG. The patients had to repeatedly walk a pre-defined course and cues were triggered always 2 s after freezing onset. The effect was analyzed via experimental measurements and patient interviews. The measurements showed that all 5 sensory cues led to a decrease of the average duration of freezing: baseline (7.9s), vibratory alert (7.1s), auditory alert (6.7s), auditory rhythm (6.4s), vibratory rhythm (6.3s), and visual cue (5.3s). Nevertheless, interestingly, patients subjectively evaluated the audio alert and vibratory signals to have a significantly better effect for reducing their freezing duration than the visual cue.
", keywords = "Auditory cueing, freezing of gait, gait assistance, Parkinson’s disease, vibratory cueing, visual cueing", volume = "6", number = "6", pages = "280-6", }
