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Published in: Journal of Neurology 12/2014

01-12-2014 | Original Communication

Gait and balance in Parkinson’s disease subtypes: objective measures and classification considerations

Authors: Talia Herman, Aner Weiss, Marina Brozgol, Nir Giladi, Jeffrey M. Hausdorff

Published in: Journal of Neurology | Issue 12/2014

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Abstract

Parkinson’s disease (PD) is often divided into tremor dominant (TD) and postural instability gait difficulty (PIGD) subtypes. However, objective measures of gait (e.g., stride length, variability) and balance have not been well studied in these subtypes. To better understand these motor subtypes, we objectively quantified gait and balance and their behavioral correlates. 110 patients with PD underwent a clinical evaluation and were stratified into PIGD and TD subtypes. Participants walked under single and dual task conditions while wearing a single body-fixed sensor, both “OFF” and “ON” medications and at home for 3 days. We also examined performance-based tests of mobility, balance, and fall risk. Stricter criteria were also applied, dividing the subjects into predominant representative subgroups: p-PIGD and p-TD. Both the PIGD (n = 62) and TD (n = 42) groups and the p-PIGD (n = 31) and p-TD (n = 32) subgroups were similar with respect to basic disease characteristics (e.g., disease duration, p > 0.69). Surprisingly gait speed, stride length, and variability did not differ between the PIGD and TD groups (p > 0.05). In contrast, the p-PIGD group had reduced gait speed (under single and dual task conditions), shorter strides, increased stride variability, and decreased stride regularity (regularity: p-PIGD 0.66 ± 0.10; p-TD 0.74 ± 0.08; p = 0.003). The p-PIGD group also scored worse on performance-based tests, compared to the p-TD. Clinical assessments of the disturbances seen in patients with the PIGD subtype are not consistent with objective measures; overlapping between the groups is seen in many objective features of gait and balance. These findings suggest that the proposed alternate classification scheme may be useful.
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Literature
1.
go back to reference Jankovic J (2008) Parkinson’s disease: clinical features and diagnosis. J Neurol Neurosurg Psychiatry 79:368–376CrossRefPubMed Jankovic J (2008) Parkinson’s disease: clinical features and diagnosis. J Neurol Neurosurg Psychiatry 79:368–376CrossRefPubMed
2.
go back to reference Jankovic J, McDermott M, Carter J, Gauthier S, Goetz C, Golbe L, Huber S, Koller W, Olanow C, Shoulson I (1990) Variable expression of Parkinson’s disease: a base-line analysis of the DATATOP cohort. The Parkinson Study Group. Neurology 40:1529–1534CrossRefPubMed Jankovic J, McDermott M, Carter J, Gauthier S, Goetz C, Golbe L, Huber S, Koller W, Olanow C, Shoulson I (1990) Variable expression of Parkinson’s disease: a base-line analysis of the DATATOP cohort. The Parkinson Study Group. Neurology 40:1529–1534CrossRefPubMed
3.
go back to reference van Rooden SM, Colas F, Martinez-Martin P, Visser M, Verbaan D, Marinus J, Chaudhuri RK, Kok JN, van Hilten JJ (2011) Clinical subtypes of Parkinson’s disease. Mov Disord 26:51–58CrossRefPubMed van Rooden SM, Colas F, Martinez-Martin P, Visser M, Verbaan D, Marinus J, Chaudhuri RK, Kok JN, van Hilten JJ (2011) Clinical subtypes of Parkinson’s disease. Mov Disord 26:51–58CrossRefPubMed
4.
go back to reference Rajput AH, Voll A, Rajput ML, Robinson CA, Rajput A (2009) Course in Parkinson disease subtypes: a 39-year clinicopathologic study. Neurology 73:206–212CrossRefPubMed Rajput AH, Voll A, Rajput ML, Robinson CA, Rajput A (2009) Course in Parkinson disease subtypes: a 39-year clinicopathologic study. Neurology 73:206–212CrossRefPubMed
5.
go back to reference Fahn S, Elton R, Members of the UPDRS Development Committee (1987) Unified Parkinson’s disease rating scale. In: Fahn S, Marsden CD, Calne D, Goldstein M (eds) Recent developments in Parkinson’s disease. Macmillan Health Care Information, Florham Park, pp 153–163 Fahn S, Elton R, Members of the UPDRS Development Committee (1987) Unified Parkinson’s disease rating scale. In: Fahn S, Marsden CD, Calne D, Goldstein M (eds) Recent developments in Parkinson’s disease. Macmillan Health Care Information, Florham Park, pp 153–163
6.
go back to reference Herman T, Rosenberg-Katz K, Jacob Y, Auriel E, Gurevich T, Giladi N, Hausdorff JM (2013) White matter hyperintensities in Parkinson’s disease: do they explain the disparity between the postural instability gait difficulty and tremor dominant subtypes? PLoS ONE 8:e55193PubMedCentralCrossRefPubMed Herman T, Rosenberg-Katz K, Jacob Y, Auriel E, Gurevich T, Giladi N, Hausdorff JM (2013) White matter hyperintensities in Parkinson’s disease: do they explain the disparity between the postural instability gait difficulty and tremor dominant subtypes? PLoS ONE 8:e55193PubMedCentralCrossRefPubMed
7.
go back to reference Herman T, Weiss A, Brozgol M, Giladi N, Hausdorff JM (2014) Identifying axial and cognitive correlates in patients with Parkinson’s disease motor subtype using the instrumented Timed Up and Go. Exp Brain Res 232:713–721CrossRefPubMed Herman T, Weiss A, Brozgol M, Giladi N, Hausdorff JM (2014) Identifying axial and cognitive correlates in patients with Parkinson’s disease motor subtype using the instrumented Timed Up and Go. Exp Brain Res 232:713–721CrossRefPubMed
8.
go back to reference Rosenberg-Katz K, Herman T, Jacob Y, Giladi N, Hendler T, Hausdorff JM (2013) Gray matter atrophy distinguishes between Parkinson disease motor subtypes. Neurology 80:1467–1484CrossRef Rosenberg-Katz K, Herman T, Jacob Y, Giladi N, Hendler T, Hausdorff JM (2013) Gray matter atrophy distinguishes between Parkinson disease motor subtypes. Neurology 80:1467–1484CrossRef
9.
go back to reference Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198CrossRefPubMed Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198CrossRefPubMed
10.
go back to reference Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P, Poewe W, Sampaio C, Stern MB, Dodel R, Dubois B, Holloway R, Jankovic J, Kulisevsky J, Lang AE, Lees A, Leurgans S, LeWitt PA, Nyenhuis D, Olanow CW, Rascol O, Schrag A, Teresi JA, van Hilten JJ, LaPelle N (2008) Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord 23:2129–2170CrossRefPubMed Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P, Poewe W, Sampaio C, Stern MB, Dodel R, Dubois B, Holloway R, Jankovic J, Kulisevsky J, Lang AE, Lees A, Leurgans S, LeWitt PA, Nyenhuis D, Olanow CW, Rascol O, Schrag A, Teresi JA, van Hilten JJ, LaPelle N (2008) Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord 23:2129–2170CrossRefPubMed
11.
go back to reference Tomlinson CL, Stowe R, Patel S, Rick C, Gray R, Clarke CE (2010) Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord 25:2649–2653CrossRefPubMed Tomlinson CL, Stowe R, Patel S, Rick C, Gray R, Clarke CE (2010) Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord 25:2649–2653CrossRefPubMed
12.
go back to reference Plotnik M, Giladi N, Hausdorff JM (2007) A new measure for quantifying the bilateral coordination of human gait: effects of aging and Parkinson’s disease. Exp Brain Res 181:561–570CrossRefPubMed Plotnik M, Giladi N, Hausdorff JM (2007) A new measure for quantifying the bilateral coordination of human gait: effects of aging and Parkinson’s disease. Exp Brain Res 181:561–570CrossRefPubMed
13.
go back to reference Nieuwboer A, Rochester L, Herman T, Vandenberghe W, Emil GE, Thomaes T, Giladi N (2009) Reliability of the new freezing of gait questionnaire: agreement between patients with Parkinson’s disease and their carers. Gait Posture 30:459–463CrossRefPubMed Nieuwboer A, Rochester L, Herman T, Vandenberghe W, Emil GE, Thomaes T, Giladi N (2009) Reliability of the new freezing of gait questionnaire: agreement between patients with Parkinson’s disease and their carers. Gait Posture 30:459–463CrossRefPubMed
14.
go back to reference Weiss A, Sharifi S, Plotnik M, van Vugt JP, Giladi N, Hausdorff JM (2011) Toward automated, at-home assessment of mobility among patients with Parkinson disease, using a body-worn accelerometer. Neurorehabil Neural Repair 25:810–818CrossRefPubMed Weiss A, Sharifi S, Plotnik M, van Vugt JP, Giladi N, Hausdorff JM (2011) Toward automated, at-home assessment of mobility among patients with Parkinson disease, using a body-worn accelerometer. Neurorehabil Neural Repair 25:810–818CrossRefPubMed
15.
go back to reference Mirelman A, Gurevich T, Giladi N, Bar-Shira A, Orr-Urtreger A, Hausdorff JM (2011) Gait alterations in healthy carriers of the LRRK2 G2019S mutation. Ann Neurol 69:193–197CrossRefPubMed Mirelman A, Gurevich T, Giladi N, Bar-Shira A, Orr-Urtreger A, Hausdorff JM (2011) Gait alterations in healthy carriers of the LRRK2 G2019S mutation. Ann Neurol 69:193–197CrossRefPubMed
16.
go back to reference Mirelman A, Heman T, Yasinovsky K, Thaler A, Gurevich T, Marder K, Bressman S, Bar-Shira A, Orr-Urtreger A, Giladi N, Hausdorff JM (2013) Fall risk and gait in Parkinson’s disease: the role of the LRRK2 G2019S mutation. Mov Disord 28:1683–1690CrossRefPubMed Mirelman A, Heman T, Yasinovsky K, Thaler A, Gurevich T, Marder K, Bressman S, Bar-Shira A, Orr-Urtreger A, Giladi N, Hausdorff JM (2013) Fall risk and gait in Parkinson’s disease: the role of the LRRK2 G2019S mutation. Mov Disord 28:1683–1690CrossRefPubMed
17.
go back to reference Weiss A, Brozgol M, Dorfman M, Herman T, Shema S, Giladi N, Hausdorff JM (2013) Does the evaluation of gait quality during daily life provide insight into fall risk? A novel approach using 3-day accelerometer recordings. Neurorehabil Neural Repair 27:742–752CrossRefPubMed Weiss A, Brozgol M, Dorfman M, Herman T, Shema S, Giladi N, Hausdorff JM (2013) Does the evaluation of gait quality during daily life provide insight into fall risk? A novel approach using 3-day accelerometer recordings. Neurorehabil Neural Repair 27:742–752CrossRefPubMed
18.
go back to reference Weiss A, Herman T, Giladi N, Hausdorff JM (2014) Objective assessment of fall risk in Parkinson’s disease using a body-fixed sensor worn for 3 days. PLoS ONE 9:e96675PubMedCentralCrossRefPubMed Weiss A, Herman T, Giladi N, Hausdorff JM (2014) Objective assessment of fall risk in Parkinson’s disease using a body-fixed sensor worn for 3 days. PLoS ONE 9:e96675PubMedCentralCrossRefPubMed
19.
go back to reference Podsiadlo D, Richardson S (1991) The timed “Up & Go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc 39:142–148CrossRefPubMed Podsiadlo D, Richardson S (1991) The timed “Up & Go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc 39:142–148CrossRefPubMed
20.
go back to reference Berg K, Wood-Dauphinee S, Williams JI (1995) The Balance Scale: reliability assessment with elderly residents and patients with an acute stroke. Scand J Rehabil Med 27:27–36PubMed Berg K, Wood-Dauphinee S, Williams JI (1995) The Balance Scale: reliability assessment with elderly residents and patients with an acute stroke. Scand J Rehabil Med 27:27–36PubMed
21.
go back to reference Shumway-Cook A, Woollacott M (1995) Motor control: theory and applications. Wilkins & Wilkins, Baltimore Shumway-Cook A, Woollacott M (1995) Motor control: theory and applications. Wilkins & Wilkins, Baltimore
22.
go back to reference Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodol) 57:289–300 Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodol) 57:289–300
23.
24.
go back to reference Schaafsma JD, Giladi N, Balash Y, Bartels AL, Gurevich T, Hausdorff JM (2003) Gait dynamics in Parkinson’s disease: relationship to Parkinsonian features, falls and response to levodopa. J Neurol Sci 212:47–53CrossRefPubMed Schaafsma JD, Giladi N, Balash Y, Bartels AL, Gurevich T, Hausdorff JM (2003) Gait dynamics in Parkinson’s disease: relationship to Parkinsonian features, falls and response to levodopa. J Neurol Sci 212:47–53CrossRefPubMed
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 Herman T, Rosenberg-Katz K, Jacob Y, Giladi N, Hausdorff JM (2014) Gray matter atrophy and freezing of gait in Parkinson’s disease: is the evidence black-on-white? Mov Disord 29:134–139CrossRefPubMed Herman T, Rosenberg-Katz K, Jacob Y, Giladi N, Hausdorff JM (2014) Gray matter atrophy and freezing of gait in Parkinson’s disease: is the evidence black-on-white? Mov Disord 29:134–139CrossRefPubMed
28.
go back to reference Eggers C, Pedrosa DJ, Kahraman D, Maier F, Lewis CJ, Fink GR, Schmidt M, Timmermann L (2012) Parkinson subtypes progress differently in clinical course and imaging pattern. PLoS ONE 7:e46813PubMedCentralCrossRefPubMed Eggers C, Pedrosa DJ, Kahraman D, Maier F, Lewis CJ, Fink GR, Schmidt M, Timmermann L (2012) Parkinson subtypes progress differently in clinical course and imaging pattern. PLoS ONE 7:e46813PubMedCentralCrossRefPubMed
29.
go back to reference Erro R, Vitale C, Amboni M, Picillo M, Moccia M, Longo K, Santangelo G, De RA, Allocca R, Giordano F, Orefice G, De MG, Santoro L, Pellecchia MT, Barone P (2013) The heterogeneity of early Parkinson’s disease: a cluster analysis on newly diagnosed untreated patients. PLoS ONE 8:e70244PubMedCentralCrossRefPubMed Erro R, Vitale C, Amboni M, Picillo M, Moccia M, Longo K, Santangelo G, De RA, Allocca R, Giordano F, Orefice G, De MG, Santoro L, Pellecchia MT, Barone P (2013) The heterogeneity of early Parkinson’s disease: a cluster analysis on newly diagnosed untreated patients. PLoS ONE 8:e70244PubMedCentralCrossRefPubMed
30.
go back to reference Graham JM, Sagar HJ (1999) A data-driven approach to the study of heterogeneity in idiopathic Parkinson’s disease: identification of three distinct subtypes. Mov Disord 14:10–20CrossRefPubMed Graham JM, Sagar HJ (1999) A data-driven approach to the study of heterogeneity in idiopathic Parkinson’s disease: identification of three distinct subtypes. Mov Disord 14:10–20CrossRefPubMed
31.
go back to reference Liu P, Feng T, Wang YJ, Zhang X, Chen B (2011) Clinical heterogeneity in patients with early-stage Parkinson’s disease: a cluster analysis. J Zhejiang Univ Sci B 12:694–703PubMedCentralCrossRefPubMed Liu P, Feng T, Wang YJ, Zhang X, Chen B (2011) Clinical heterogeneity in patients with early-stage Parkinson’s disease: a cluster analysis. J Zhejiang Univ Sci B 12:694–703PubMedCentralCrossRefPubMed
32.
go back to reference Smulders K, van Nimwegen M, Munneke M, Bloem BR, Kessels RP, Esselink RA (2013) Involvement of specific executive functions in mobility in Parkinson’s disease. Parkinsonism Relat Disord 19:126–128CrossRefPubMed Smulders K, van Nimwegen M, Munneke M, Bloem BR, Kessels RP, Esselink RA (2013) Involvement of specific executive functions in mobility in Parkinson’s disease. Parkinsonism Relat Disord 19:126–128CrossRefPubMed
33.
go back to reference Marras C, Lang A (2013) Parkinson’s disease subtypes: lost in translation? J Neurol Neurosurg Psychiatry 84:409–415CrossRefPubMed Marras C, Lang A (2013) Parkinson’s disease subtypes: lost in translation? J Neurol Neurosurg Psychiatry 84:409–415CrossRefPubMed
34.
go back to reference Selikhova M, Williams DR, Kempster PA, Holton JL, Revesz T, Lees AJ (2009) A clinico-pathological study of subtypes in Parkinson’s disease. Brain 132:2947–2957CrossRefPubMed Selikhova M, Williams DR, Kempster PA, Holton JL, Revesz T, Lees AJ (2009) A clinico-pathological study of subtypes in Parkinson’s disease. Brain 132:2947–2957CrossRefPubMed
35.
go back to reference Stebbins GT, Goetz CG, Burn DJ, Jankovic J, Khoo TK, Tilley BC (2013) 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. Mov Disord 28:668–670CrossRefPubMed Stebbins GT, Goetz CG, Burn DJ, Jankovic J, Khoo TK, Tilley BC (2013) 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. Mov Disord 28:668–670CrossRefPubMed
36.
go back to reference Alves G, Pedersen KF, Bloem BR, Blennow K, Zetterberg H, Borm GF, Dalaker TO, Beyer MK, Aarsland D, Andreasson U, Lange J, Tysnes OB, Zivadinov R, Larsen JP (2013) Cerebrospinal fluid amyloid-beta and phenotypic heterogeneity in de novo Parkinson’s disease. J Neurol Neurosurg Psychiatry 84:537–543CrossRefPubMed Alves G, Pedersen KF, Bloem BR, Blennow K, Zetterberg H, Borm GF, Dalaker TO, Beyer MK, Aarsland D, Andreasson U, Lange J, Tysnes OB, Zivadinov R, Larsen JP (2013) Cerebrospinal fluid amyloid-beta and phenotypic heterogeneity in de novo Parkinson’s disease. J Neurol Neurosurg Psychiatry 84:537–543CrossRefPubMed
Metadata
Title
Gait and balance in Parkinson’s disease subtypes: objective measures and classification considerations
Authors
Talia Herman
Aner Weiss
Marina Brozgol
Nir Giladi
Jeffrey M. Hausdorff
Publication date
01-12-2014
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 12/2014
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-014-7513-6

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