Skip to main content
Top
Published in: Journal of Neurology 2/2014

01-02-2014 | Original Communication

Gait and upper limb variability in Parkinson’s disease patients with and without freezing of gait

Authors: Michael T. Barbe, Martin Amarell, Anke H. Snijders, Esther Florin, Eva-Lotte Quatuor, Eckhard Schönau, Gereon R. Fink, Bastiaan R. Bloem, Lars Timmermann

Published in: Journal of Neurology | Issue 2/2014

Login to get access

Abstract

Patients with Parkinson’s disease (PD) and freezing of gait (FOG) (freezers) demonstrate high gait variability. The objective of this study was to determine whether freezers display a higher variability of upper limb movements and elucidate if these changes correlate with gait. We were the first group to compare directly objectively measured gait and upper limb movement variability of freezers between freezing episodes. Patients with objectively verified FOG (n = 11) and PD patients without FOG (non-freezers) (n = 11) in a non-randomized medication condition (OFF/ON) were analyzed. Uncued antiphasic finger tapping and forearm diadochokinetic movements were analyzed via three-dimensional ultrasound kinematic measurements. Gait variability of straight gait was assessed using ground reaction forces. Freezers had shorter stride length (p = 0.004) and higher stride length variability (p = 0.005) in the medication OFF condition. Movement variability was not different during finger tapping or diadochokinesia between the groups. There was a trend towards more freezing of the upper limb during finger tapping for the freezers (p = 0.07). Variability in stride length generation and stride timing was not associated with variability of upper limb movement in freezers. Our findings demonstrate that: (1) freezers have a higher spatial gait variability between freezing episodes; (2) freezing-like episodes of the upper limb occur in PD patients, and tend to be more pronounced among freezers than non-freezers for finger tapping; (3) spatial and temporal upper extremity variability is equally affected in freezers and non-freezers in an uncued task. Upper limb freezing is not correlated to lower limb freezing, implicating a different pathophysiology.
Literature
1.
go back to reference Almeida QJ, Wishart LR, Lee TD (2002) Bimanual coordination deficits with Parkinson’s disease: the influence of movement speed and external cueing. Mov Disord 17:30–37CrossRefPubMed Almeida QJ, Wishart LR, Lee TD (2002) Bimanual coordination deficits with Parkinson’s disease: the influence of movement speed and external cueing. Mov Disord 17:30–37CrossRefPubMed
2.
go back to reference Barbe MT, Liebhart L, Runge M, Deyng J, Florin E, Wojtecki L, Schnitzler A, Allert N, Sturm V, Fink GR, Maarouf M, Timmermann L (2011) Deep brain stimulation of the ventral intermediate nucleus in patients with essential tremor: stimulation below intercommissural line is more efficient but equally effective as stimulation above. Exp Neurol 230:131–137CrossRefPubMed Barbe MT, Liebhart L, Runge M, Deyng J, Florin E, Wojtecki L, Schnitzler A, Allert N, Sturm V, Fink GR, Maarouf M, Timmermann L (2011) Deep brain stimulation of the ventral intermediate nucleus in patients with essential tremor: stimulation below intercommissural line is more efficient but equally effective as stimulation above. Exp Neurol 230:131–137CrossRefPubMed
3.
go back to reference Barrett MJ, Wylie SA, Harrison MB, Wooten GF (2010) Handedness and motor symptom asymmetry in Parkinson’s disease. J Neurol Neurosurg Psychiatry 82:1122–1124PubMedCentralCrossRefPubMed Barrett MJ, Wylie SA, Harrison MB, Wooten GF (2010) Handedness and motor symptom asymmetry in Parkinson’s disease. J Neurol Neurosurg Psychiatry 82:1122–1124PubMedCentralCrossRefPubMed
4.
go back to reference Beatty WW, Staton RD, Weir WS, Monson N, Whitaker HA (1989) Cognitive disturbances in Parkinson’s disease. J Geriatr Psychiatry Neurol 2:22–33CrossRefPubMed Beatty WW, Staton RD, Weir WS, Monson N, Whitaker HA (1989) Cognitive disturbances in Parkinson’s disease. J Geriatr Psychiatry Neurol 2:22–33CrossRefPubMed
5.
go back to reference Chee R, Murphy A, Danoudis M, Georgiou-Karistianis N, Iansek R (2009) Gait freezing in Parkinson’s disease and the stride length sequence effect interaction. Brain 132:2151–2160CrossRefPubMed Chee R, Murphy A, Danoudis M, Georgiou-Karistianis N, Iansek R (2009) Gait freezing in Parkinson’s disease and the stride length sequence effect interaction. Brain 132:2151–2160CrossRefPubMed
6.
go back to reference Espay AJ, Fasano A, van Nuenen BF, Payne MM, Snijders AH, Bloem BR (2012) “On” state freezing of gait in Parkinson disease: a paradoxical levodopa-induced complication. Neurology 78:454–457PubMedCentralCrossRefPubMed Espay AJ, Fasano A, van Nuenen BF, Payne MM, Snijders AH, Bloem BR (2012) “On” state freezing of gait in Parkinson disease: a paradoxical levodopa-induced complication. Neurology 78:454–457PubMedCentralCrossRefPubMed
7.
go back to reference Fahn S, Elton RL (1987) Unified Parkinson’s disease rating scale. In: Fahn S, Marsden CD, Calne D, Goldstein M (eds) Recent developments in Parkinson’s disease. Florham Park, MacMillan Health Care Information, pp 153–163 Fahn S, Elton RL (1987) Unified Parkinson’s disease rating scale. In: Fahn S, Marsden CD, Calne D, Goldstein M (eds) Recent developments in Parkinson’s disease. Florham Park, MacMillan Health Care Information, pp 153–163
8.
go back to reference Fietzek UM, Zwosta J, Schroeteler FE, Ziegler K, Ceballos-Baumann AO (2013) Levodopa changes the severity of freezing in Parkinson’s disease. Parkinsonism Relat Disord 19:894–896CrossRefPubMed Fietzek UM, Zwosta J, Schroeteler FE, Ziegler K, Ceballos-Baumann AO (2013) Levodopa changes the severity of freezing in Parkinson’s disease. Parkinsonism Relat Disord 19:894–896CrossRefPubMed
9.
go back to reference Giladi N, McDermott MP, Fahn S, Przedborski S, Jankovic J, Stern M, Tanner C (2001) Freezing of gait in PD: prospective assessment in the DATATOP cohort. Neurology 56:1712–1721CrossRefPubMed Giladi N, McDermott MP, Fahn S, Przedborski S, Jankovic J, Stern M, Tanner C (2001) Freezing of gait in PD: prospective assessment in the DATATOP cohort. Neurology 56:1712–1721CrossRefPubMed
10.
go back to reference Giladi N, Shabtai H, Simon ES, Biran S, Tal J, Korczyn AD (2000) Construction of freezing of gait questionnaire for patients with Parkinsonism. Parkinsonism Relat Disord 6:165–170CrossRefPubMed Giladi N, Shabtai H, Simon ES, Biran S, Tal J, Korczyn AD (2000) Construction of freezing of gait questionnaire for patients with Parkinsonism. Parkinsonism Relat Disord 6:165–170CrossRefPubMed
11.
go back to reference Giladi N, Tal J, Azulay T, Rascol O, Brooks DJ, Melamed E, Oertel W, Poewe WH, Stocchi F, Tolosa E (2009) Validation of the freezing of gait questionnaire in patients with Parkinson’s disease. Mov Disord 24:655–661CrossRefPubMed Giladi N, Tal J, Azulay T, Rascol O, Brooks DJ, Melamed E, Oertel W, Poewe WH, Stocchi F, Tolosa E (2009) Validation of the freezing of gait questionnaire in patients with Parkinson’s disease. Mov Disord 24:655–661CrossRefPubMed
12.
go back to reference Hausdorff JM, Schaafsma JD, Balash Y, Bartels AL, Gurevich T, Giladi N (2003) Impaired regulation of stride variability in Parkinson’s disease subjects with freezing of gait. Exp Brain Res 149:187–194PubMed Hausdorff JM, Schaafsma JD, Balash Y, Bartels AL, Gurevich T, Giladi N (2003) Impaired regulation of stride variability in Parkinson’s disease subjects with freezing of gait. Exp Brain Res 149:187–194PubMed
13.
go back to reference Heremans E, Nieuwboer A, Vercruysse S (2013) Freezing of gait in Parkinson’s disease: where are we now? Curr Neurol Neurosci Rep 13:350CrossRefPubMed Heremans E, Nieuwboer A, Vercruysse S (2013) Freezing of gait in Parkinson’s disease: where are we now? Curr Neurol Neurosci Rep 13:350CrossRefPubMed
14.
go back to reference Hermsdorfer J, Marquardt C, Wack S, Mai N (1999) Comparative analysis of diadochokinetic movements. J Electromyogr Kinesiol 9:283–295CrossRefPubMed Hermsdorfer J, Marquardt C, Wack S, Mai N (1999) Comparative analysis of diadochokinetic movements. J Electromyogr Kinesiol 9:283–295CrossRefPubMed
15.
go back to reference Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55:181–184PubMedCentralCrossRefPubMed Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55:181–184PubMedCentralCrossRefPubMed
16.
go back to reference Iansek R, Huxham F, McGinley J (2006) The sequence effect and gait festination in Parkinson disease: contributors to freezing of gait? Mov Disord 21:1419–1424CrossRefPubMed Iansek R, Huxham F, McGinley J (2006) The sequence effect and gait festination in Parkinson disease: contributors to freezing of gait? Mov Disord 21:1419–1424CrossRefPubMed
17.
go back to reference Kandori A, Yokoe M, Sakoda S, Abe K, Miyashita T, Oe H, Naritomi H, Ogata K, Tsukada K (2004) Quantitative magnetic detection of finger movements in patients with Parkinson’s disease. Neurosci Res 49:253–260CrossRefPubMed Kandori A, Yokoe M, Sakoda S, Abe K, Miyashita T, Oe H, Naritomi H, Ogata K, Tsukada K (2004) Quantitative magnetic detection of finger movements in patients with Parkinson’s disease. Neurosci Res 49:253–260CrossRefPubMed
18.
go back to reference Knobl P, Kielstra L, Almeida Q (2011) The relationship between motor planning and freezing of gait in Parkinson’s disease. J Neurol Neurosurg Psychiatry 83:98–101CrossRefPubMed Knobl P, Kielstra L, Almeida Q (2011) The relationship between motor planning and freezing of gait in Parkinson’s disease. J Neurol Neurosurg Psychiatry 83:98–101CrossRefPubMed
19.
go back to reference Lamberti P, Armenise S, Castaldo V, de Mari M, Iliceto G, Tronci P, Serlenga L (1997) Freezing gait in Parkinson’s disease. Eur Neurol 38:297–301CrossRefPubMed Lamberti P, Armenise S, Castaldo V, de Mari M, Iliceto G, Tronci P, Serlenga L (1997) Freezing gait in Parkinson’s disease. Eur Neurol 38:297–301CrossRefPubMed
20.
go back to reference Macht M, Kaussner Y, Moller JC, Stiasny-Kolster K, Eggert KM, Kruger HP, Ellgring H (2007) Predictors of freezing in Parkinson’s disease: a survey of 6,620 patients. Mov Disord 22:953–956CrossRefPubMed Macht M, Kaussner Y, Moller JC, Stiasny-Kolster K, Eggert KM, Kruger HP, Ellgring H (2007) Predictors of freezing in Parkinson’s disease: a survey of 6,620 patients. Mov Disord 22:953–956CrossRefPubMed
21.
go back to reference Moreau C, Ozsancak C, Blatt JL, Derambure P, Destee A, Defebvre L (2007) Oral festination in Parkinson’s disease: biomechanical analysis and correlation with festination and freezing of gait. Mov Disord 22:1503–1506CrossRefPubMed Moreau C, Ozsancak C, Blatt JL, Derambure P, Destee A, Defebvre L (2007) Oral festination in Parkinson’s disease: biomechanical analysis and correlation with festination and freezing of gait. Mov Disord 22:1503–1506CrossRefPubMed
22.
go back to reference Nanhoe-Mahabier W, Snijders AH, Delval A, Weerdesteyn V, Duysens J, Overeem S, Bloem BR (2013) Split-belt locomotion in Parkinson’s disease with and without freezing of gait. Neuroscience 236:110–116CrossRefPubMed Nanhoe-Mahabier W, Snijders AH, Delval A, Weerdesteyn V, Duysens J, Overeem S, Bloem BR (2013) Split-belt locomotion in Parkinson’s disease with and without freezing of gait. Neuroscience 236:110–116CrossRefPubMed
23.
go back to reference Nanhoe-Mahabier W, Snijders AH, Delval A, Weerdesteyn V, Duysens J, Overeem S, Bloem BR (2011) Walking patterns in Parkinson’s disease with and without freezing of gait. Neuroscience 182:217–224CrossRefPubMed Nanhoe-Mahabier W, Snijders AH, Delval A, Weerdesteyn V, Duysens J, Overeem S, Bloem BR (2011) Walking patterns in Parkinson’s disease with and without freezing of gait. Neuroscience 182:217–224CrossRefPubMed
24.
go back to reference Nieuwboer A, Dom R, De Weerdt W, Desloovere K, Fieuws S, Broens-Kaucsik E (2001) Abnormalities of the spatiotemporal characteristics of gait at the onset of freezing in Parkinson’s disease. Mov Disord 16:1066–1075CrossRefPubMed Nieuwboer A, Dom R, De Weerdt W, Desloovere K, Fieuws S, Broens-Kaucsik E (2001) Abnormalities of the spatiotemporal characteristics of gait at the onset of freezing in Parkinson’s disease. Mov Disord 16:1066–1075CrossRefPubMed
25.
go back to reference Nieuwboer A, Vercruysse S, Feys P, Levin O, Spildooren J, Swinnen S (2009) Upper limb movement interruptions are correlated to freezing of gait in Parkinson’s disease. Eur J Neurosci 29:1422–1430CrossRefPubMed Nieuwboer A, Vercruysse S, Feys P, Levin O, Spildooren J, Swinnen S (2009) Upper limb movement interruptions are correlated to freezing of gait in Parkinson’s disease. Eur J Neurosci 29:1422–1430CrossRefPubMed
26.
go back to reference Nutt JG, Bloem BR, Giladi N, Hallett M, Horak FB, Nieuwboer A (2011) Freezing of gait: moving forward on a mysterious clinical phenomenon. Lancet Neurol 10:734–744CrossRefPubMed Nutt JG, Bloem BR, Giladi N, Hallett M, Horak FB, Nieuwboer A (2011) Freezing of gait: moving forward on a mysterious clinical phenomenon. Lancet Neurol 10:734–744CrossRefPubMed
27.
go back to reference Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113CrossRefPubMed Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113CrossRefPubMed
28.
go back to reference Plotnik M, Giladi N, Balash Y, Peretz C, Hausdorff JM (2005) Is freezing of gait in Parkinson’s disease related to asymmetric motor function? Ann Neurol 57:656–663CrossRefPubMed Plotnik M, Giladi N, Balash Y, Peretz C, Hausdorff JM (2005) Is freezing of gait in Parkinson’s disease related to asymmetric motor function? Ann Neurol 57:656–663CrossRefPubMed
29.
go back to reference Plotnik M, Giladi N, Hausdorff JM (2008) Bilateral coordination of walking and freezing of gait in Parkinson’s disease. Eur J Neurosci 27:1999–2006CrossRefPubMed Plotnik M, Giladi N, Hausdorff JM (2008) Bilateral coordination of walking and freezing of gait in Parkinson’s disease. Eur J Neurosci 27:1999–2006CrossRefPubMed
30.
go back to reference Schaafsma JD, Balash Y, Gurevich T, Bartels AL, Hausdorff JM, Giladi N (2003) Characterization of freezing of gait subtypes and the response of each to levodopa in Parkinson’s disease. Eur J Neurol 10:391–398CrossRefPubMed Schaafsma JD, Balash Y, Gurevich T, Bartels AL, Hausdorff JM, Giladi N (2003) Characterization of freezing of gait subtypes and the response of each to levodopa in Parkinson’s disease. Eur J Neurol 10:391–398CrossRefPubMed
31.
go back to reference Shine JM, Matar E, Bolitho SJ, Dilda V, Morris TR, Naismith SL, Moore ST, Lewis SJ (2013) Modeling freezing of gait in Parkinson’s disease with a virtual reality paradigm. Gait Posture 38:104–108CrossRefPubMed Shine JM, Matar E, Bolitho SJ, Dilda V, Morris TR, Naismith SL, Moore ST, Lewis SJ (2013) Modeling freezing of gait in Parkinson’s disease with a virtual reality paradigm. Gait Posture 38:104–108CrossRefPubMed
32.
go back to reference Shine JM, Matar E, Ward PB, Frank MJ, Moustafa AA, Pearson M, Naismith SL, Lewis SJ (2013) Freezing of gait in Parkinson’s disease is associated with functional decoupling between the cognitive control network and the basal ganglia. Brain Shine JM, Matar E, Ward PB, Frank MJ, Moustafa AA, Pearson M, Naismith SL, Lewis SJ (2013) Freezing of gait in Parkinson’s disease is associated with functional decoupling between the cognitive control network and the basal ganglia. Brain
33.
go back to reference Snijders AH, Haaxma CA, Hagen YJ, Munneke M, Bloem BR (2012) Freezer or non-freezer: clinical assessment of freezing of gait. Parkinsonism Relat Disord 18:149–154CrossRefPubMed Snijders AH, Haaxma CA, Hagen YJ, Munneke M, Bloem BR (2012) Freezer or non-freezer: clinical assessment of freezing of gait. Parkinsonism Relat Disord 18:149–154CrossRefPubMed
34.
go back to reference Timmermann L, Braun M, Groiss S, Wojtecki L, Ostrowski S, Krause H, Pollok B, Sudmeyer M, Ploner M, Gross J, Maarouf M, Voges J, Sturm V, Schnitzler A (2008) Differential effects of levodopa and subthalamic nucleus deep brain stimulation on bradykinesia in Parkinson’s disease. Mov Disord 23:218–227CrossRefPubMed Timmermann L, Braun M, Groiss S, Wojtecki L, Ostrowski S, Krause H, Pollok B, Sudmeyer M, Ploner M, Gross J, Maarouf M, Voges J, Sturm V, Schnitzler A (2008) Differential effects of levodopa and subthalamic nucleus deep brain stimulation on bradykinesia in Parkinson’s disease. Mov Disord 23:218–227CrossRefPubMed
35.
go back to reference Uitti RJ, Baba Y, Whaley NR, Wszolek ZK, Putzke JD (2005) Parkinson disease: handedness predicts asymmetry. Neurology 64:1925–1930CrossRefPubMed Uitti RJ, Baba Y, Whaley NR, Wszolek ZK, Putzke JD (2005) Parkinson disease: handedness predicts asymmetry. Neurology 64:1925–1930CrossRefPubMed
36.
go back to reference Veilleux LN, Robert M, Ballaz L, Lemay M, Rauch F (2011) Gait analysis using a force-measuring gangway: intrasession repeatability in healthy adults. J Musculoskelet Neuronal Interact 11:27–33PubMed Veilleux LN, Robert M, Ballaz L, Lemay M, Rauch F (2011) Gait analysis using a force-measuring gangway: intrasession repeatability in healthy adults. J Musculoskelet Neuronal Interact 11:27–33PubMed
37.
go back to reference Vercruysse S, Spildooren J, Heremans E, Vandenbossche J, Levin O, Wenderoth N, Swinnen SP, Janssens L, Vandenberghe W, Nieuwboer A (2012) Freezing in Parkinson’s disease: a spatiotemporal motor disorder beyond gait. Mov Disord 27:254–263CrossRefPubMed Vercruysse S, Spildooren J, Heremans E, Vandenbossche J, Levin O, Wenderoth N, Swinnen SP, Janssens L, Vandenberghe W, Nieuwboer A (2012) Freezing in Parkinson’s disease: a spatiotemporal motor disorder beyond gait. Mov Disord 27:254–263CrossRefPubMed
38.
go back to reference Vercruysse S, Spildooren J, Heremans E, Vandenbossche J, Wenderoth N, Swinnen SP, Vandenberghe W, Nieuwboer A (2012) Abnormalities and cue dependence of rhythmical upper-limb movements in Parkinson patients with freezing of gait. Neurorehabil Neural Repair 26:636–645CrossRefPubMed Vercruysse S, Spildooren J, Heremans E, Vandenbossche J, Wenderoth N, Swinnen SP, Vandenberghe W, Nieuwboer A (2012) Abnormalities and cue dependence of rhythmical upper-limb movements in Parkinson patients with freezing of gait. Neurorehabil Neural Repair 26:636–645CrossRefPubMed
39.
go back to reference Vercruysse S, Spildooren J, Heremans E, Wenderoth N, Swinnen SP, Vandenberghe W, Nieuwboer A (2013) The neural correlates of upper limb motor blocks in Parkinson’s disease and their relation to freezing of gait. Cereb Cortex Vercruysse S, Spildooren J, Heremans E, Wenderoth N, Swinnen SP, Vandenberghe W, Nieuwboer A (2013) The neural correlates of upper limb motor blocks in Parkinson’s disease and their relation to freezing of gait. Cereb Cortex
40.
go back to reference Ziv I, Avraham M, Dabby R, Zoldan J, Djaldetti R, Melamed E (1999) Early-occurrence of manual motor blocks in Parkinson’s disease: a quantitative assessment. Acta Neurol Scand 99:106–111CrossRefPubMed Ziv I, Avraham M, Dabby R, Zoldan J, Djaldetti R, Melamed E (1999) Early-occurrence of manual motor blocks in Parkinson’s disease: a quantitative assessment. Acta Neurol Scand 99:106–111CrossRefPubMed
Metadata
Title
Gait and upper limb variability in Parkinson’s disease patients with and without freezing of gait
Authors
Michael T. Barbe
Martin Amarell
Anke H. Snijders
Esther Florin
Eva-Lotte Quatuor
Eckhard Schönau
Gereon R. Fink
Bastiaan R. Bloem
Lars Timmermann
Publication date
01-02-2014
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 2/2014
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-013-7199-1

Other articles of this Issue 2/2014

Journal of Neurology 2/2014 Go to the issue