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New evidence for gait abnormalities among Parkinson’s disease patients who suffer from freezing of gait: insights using a body-fixed sensor worn for 3 days

  • Neurology and Preclinical Neurological Studies - Original Article
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Abstract

Previous studies conducted in laboratory settings suggest that the gait pattern in between freezing of gait (FOG) episodes is abnormal among patients with Parkinson’s disease (PD) who suffer from FOG (i.e., “freezers”), compared to those who do not (i.e., “non-freezers”). We evaluated whether long-term recordings also reveal gait alterations in freezers and if these features were related to freezing severity and its impact on daily function. 72 patients with PD wore a 3-D accelerometer for 3 days. Acceleration-derived gait features included quantity (e.g., the amount of walking) and quality measures (e.g., gait variability). The New FOG-Questionnaire evaluated the subject’s perceptions of FOG severity and its impact. Age, gender, and disease duration were similar (p > 0.19) in the 28 freezers and 44 non-freezers. Walking quantity was similar in the two groups, while freezers walked with higher gait variability (i.e., larger anterior–posterior power spectral density width; p = 0.003) and lower gait consistency (i.e., lower vertical stride regularity; p = 0.007). Group differences were observed when comparing the typical (i.e., median), best, and worst performance among the multiple walking bouts measured. Vertical and medio-lateral gait consistency were associated with the impact of FOG on daily living (r < −0.39, p < 0.044). The present findings demonstrate that freezers have altered gait variability and consistency during spontaneous community ambulation, even during optimal performance, and that these measures are associated with the impact of FOG on daily function. Long-term recordings may provide new insights into PD and augment the monitoring of FOG and its response to therapy.

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References

  • Almeida QJ, Lebold CA (2010) Freezing of gait in Parkinson’s disease: a perceptual cause for a motor impairment? J Neurol Neurosurg Psychiatry 81:513–518

    Article  CAS  PubMed  Google Scholar 

  • Barbe MT, Amarell M, Snijders AH, Florin E, Quatuor EL, Schonau E, Fink GR, Bloem BR, Timmermann L (2014) Gait and upper limb variability in Parkinson’s disease patients with and without freezing of gait. J Neurol 261:330–342

    Article  PubMed  Google Scholar 

  • Benjamini YHY (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 57:125–133

    Google Scholar 

  • Berg KO, Wood-Dauphinee SL, Williams JI, Maki B (1992) Measuring balance in the elderly: validation of an instrument. Can J Public Health 83(Suppl 2):S7–S11

    PubMed  Google Scholar 

  • Bhatt H, Pieruccini-Faria F, Almeida QJ (2013) Dynamics of turning sharpness influences freezing of gait in Parkinson’s disease. Parkinsonism Relat Disord 19:181–185

    Article  PubMed  Google Scholar 

  • Brach JS, Berthold R, Craik R, VanSwearingen JM, Newman AB (2001) Gait variability in community-dwelling older adults. J Am Geriatr Soc 49:1646–1650

    Article  CAS  PubMed  Google Scholar 

  • Brach JS, Berlin JE, VanSwearingen JM, Newman AB, Studenski SA (2005) Too much or too little step width variability is associated with a fall history in older persons who walk at or near normal gait speed. J Neuroeng Rehabil 2:21

    Article  PubMed Central  PubMed  Google Scholar 

  • Brach JS, Studenski S, Perera S, VanSwearingen JM, Newman AB (2008) Stance time and step width variability have unique contributing impairments in older persons. Gait Posture 27:431–439

    Article  PubMed Central  PubMed  Google Scholar 

  • Cohen RG, Horak FB, Nutt JG (2012) Peering through the FoG: visual manipulations shed light on freezing of gait. Mov Disord 27:470–472

    Article  PubMed Central  PubMed  Google Scholar 

  • Cohen RG, Klein KA, Nomura M, Fleming M, Mancini M, Giladi N, Nutt JG, Horak FB (2014) Inhibition, executive function, and freezing of gait. J Parkinson Dis 4:111–122

    Google Scholar 

  • Ehgoetz Martens KA, Pieruccini-Faria F, Almeida QJ (2013) Could sensory mechanisms be a core factor that underlies freezing of gait in Parkinson’s disease? PLoS ONE 8:e62602

    Article  PubMed Central  PubMed  Google Scholar 

  • Fling BW, Cohen RG, Mancini M, Nutt JG, Fair DA, Horak FB (2013) Asymmetric pedunculopontine network connectivity in parkinsonian patients with freezing of gait. Brain 136:2405–2418

    Article  PubMed Central  PubMed  Google Scholar 

  • Giladi N, Hausdorff JM (2006) The role of mental function in the pathogenesis of freezing of gait in Parkinson’s disease. J Neurol Sci 248:173–176

    Article  PubMed  Google Scholar 

  • Giladi N, Horak FB, Hausdorff JM (2013) Classification of gait disturbances: distinguishing between continuous and episodic changes. Mov Disord 28:1469–1473

    Article  PubMed  Google Scholar 

  • Gilat M, Shine JM, Bolitho SJ, Matar E, Kamsma YP, Naismith SL, Lewis SJ (2013) Variability of stepping during a virtual reality paradigm in Parkinson’s disease patients with and without freezing of gait. PLoS ONE 8:e66718

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Goetz CG, Fahn S, Martinez-Martin P, Poewe W, Sampaio C, Stebbins GT, Stern MB, Tilley BC, 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 (2007) Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): process, format, and clinimetric testing plan. Mov Disord 22:41–47

    Article  PubMed  Google Scholar 

  • 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 149:187–194

    CAS  PubMed  Google Scholar 

  • Heremans E, Nieuwboer A, Vercruysse S (2013) Freezing of gait in Parkinson’s disease: where are we now? Curr Neurol Neurosci Rep 13:350

    Article  PubMed  Google Scholar 

  • Herman T, Giladi N, Hausdorff JM (2013a) Neuroimaging as a window into gait disturbances and freezing of gait in patients with Parkinson’s disease. Curr Neurol Neurosci Rep 13:411

    Article  PubMed  Google Scholar 

  • Herman T, Rosenberg-Katz K, Jacob Y, Auriel E, Gurevich T, Giladi N, Hausdorff JM (2013b) White matter hyperintensities in Parkinson’s disease: do they explain the disparity between the postural instability gait difficulty and tremor dominant subtypes? PLoS ONE 8:55193

    Article  Google Scholar 

  • 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 29:134–139

    Article  PubMed  Google Scholar 

  • Hobert MA, Maetzler W, Aminian K, Chiari L (2014) Technical and clinical view on ambulatory assessment in Parkinson’s disease. Acta Neurol Scand

  • Knobl P, Kielstra L, Almeida Q (2012) The relationship between motor planning and freezing of gait in Parkinson’s disease. J Neurol Neurosurg Psychiatry 83:98–101

    Article  PubMed  Google Scholar 

  • Kostic VS, Agosta F, Pievani M, Stefanova E, Jecmenica-Lukic M, Scarale A, Spica V, Filippi M (2012) Pattern of brain tissue loss associated with freezing of gait in Parkinson disease. Neurology 78:409–416

    Article  CAS  PubMed  Google Scholar 

  • Moe-Nilssen R, Helbostad JL (2004) Estimation of gait cycle characteristics by trunk accelerometry. J Biomech 37:121–126

    Article  PubMed  Google Scholar 

  • Moe-Nilssen R, Helbostad JL (2005) Interstride trunk acceleration variability but not step width variability can differentiate between fit and frail older adults. Gait Posture 21:164–170

    Article  PubMed  Google Scholar 

  • Moe-Nilssen R, Aaslund MK, Hodt-Billington C, Helbostad JL (2010) Gait variability measures may represent different constructs. Gait Posture 32:98–101

    Article  PubMed  Google Scholar 

  • Moore O, Peretz C, Giladi N (2007) Freezing of gait affects quality of life of peoples with Parkinson’s disease beyond its relationships with mobility and gait. Mov Disord 22:2192–2195

    Article  PubMed  Google Scholar 

  • Morris TR, Cho C, Dilda V, Shine JM, Naismith SL, Lewis SJ, Moore ST (2012) A comparison of clinical and objective measures of freezing of gait in Parkinson’s disease. Parkinsonism Relat Disord 18:572–577

    Article  PubMed  Google Scholar 

  • Muralidharan V, Balasubramani PP, Chakravarthy VS, Lewis SJ, Moustafa AA (2014) A computational model of altered gait patterns in parkinson’s disease patients negotiating narrow doorways. Front Comput Neurosci 7:190

    Article  PubMed Central  PubMed  Google Scholar 

  • Nasreddine ZS, Phillips NA, Bedirian V, Charbonneau S, Whitehead V, Collin I, Cummings JL, Chertkow H (2005) The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 53:695–699

    Article  PubMed  Google Scholar 

  • Nieuwboer A, Giladi N (2013) Characterizing freezing of gait in Parkinson’s disease: models of an episodic phenomenon. Mov Disord 28:1509–1519

    Article  PubMed  Google Scholar 

  • 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 30:459–463

    Article  PubMed  Google Scholar 

  • 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 10:734–744

    Article  PubMed  Google Scholar 

  • Plotnik M, Giladi N, Hausdorff JM (2012) Is freezing of gait in Parkinson’s disease a result of multiple gait impairments? Implications for treatment. Parkinson’s Dis 2012:459321

    Google Scholar 

  • Podsiadlo D, Richardson S (1991) The timed “Up & Go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc 39:142–148

    CAS  PubMed  Google Scholar 

  • Powell LE, Myers AM (1995) The Activities-specific Balance Confidence (ABC) Scale. J Gerontol A Biol Sci Med Sci 50A:M28–M34

    Article  CAS  PubMed  Google Scholar 

  • Rispens SM, van Schooten KS, Pijnappels M, Daffertshofer A, Beek PJ, van Dieen JH (2014) Identification of fall risk predictors in daily life measurements: gait characteristics’ reliability and association with self-reported fall history. Neurorehabil Neural Repair

  • Schwickert L, Becker C, Lindemann U, Marechal C, Bourke A, Chiari L, Helbostad JL, Zijlstra W, Aminian K, Todd C, Bandinelli S, Klenk J (2013) Fall detection with body-worn sensors: a systematic review. Z Gerontol Geriatr 46:706–719

    Article  CAS  PubMed  Google Scholar 

  • Shany T, Redmond SJ, Marschollek M, Lovell NH (2012) Assessing fall risk using wearable sensors: a practical discussion. A review of the practicalities and challenges associated with the use of wearable sensors for quantification of fall risk in older people. Z Gerontol Geriatr 45:694–706

    Article  CAS  PubMed  Google Scholar 

  • Shumway-Cook A, Woollacott M (1995) Motor control theory and applications. Williams and Wilkins, Baltimore

    Google Scholar 

  • Snijders AH, Nijkrake MJ, Bakker M, Munneke M, Wind C, Bloem BR (2008) Clinimetrics of freezing of gait. Mov Disord 23(Suppl 2):S468–S474

    Article  PubMed  Google Scholar 

  • Snijders AH, Leunissen I, Bakker M, Overeem S, Helmich RC, Bloem BR, Toni I (2011) Gait-related cerebral alterations in patients with Parkinson’s disease with freezing of gait. Brain 134:59–72

    Article  PubMed  Google Scholar 

  • Snijders AH, Haaxma CA, Hagen YJ, Munneke M, Bloem BR (2012) Freezer or non-freezer: clinical assessment of freezing of gait. Parkinsonism Relat Disord 18:149–154

    Article  PubMed  Google Scholar 

  • Tessitore A, Amboni M, Cirillo G, Corbo D, Picillo M, Russo A, Vitale C, Santangelo G, Erro R, Cirillo M, Esposito F, Barone P, Tedeschi G (2012) Regional gray matter atrophy in patients with Parkinson disease and freezing of gait. AJNR Am J Neuroradiol 33:1804–1809

    Article  CAS  PubMed  Google Scholar 

  • Thevathasan W, Cole MH, Graepel CL, Hyam JA, Jenkinson N, Brittain JS, Coyne TJ, Silburn PA, Aziz TZ, Kerr G, Brown P (2012) A spatiotemporal analysis of gait freezing and the impact of pedunculopontine nucleus stimulation. Brain 135:1446–1454

    Article  PubMed Central  PubMed  Google Scholar 

  • Vervoort G, Nackaerts E, Mohammadi F, Heremans E, Verschueren S, Nieuwboer A, Vercruysse S (2013) Which aspects of postural control differentiate between patients with Parkinson’s disease with and without freezing of gait? Parkinson’s Dis 2013:971480

    Google Scholar 

  • 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 25:810–818

    Article  PubMed  Google Scholar 

  • 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 27:742–752

    Article  PubMed  Google Scholar 

  • 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:e96675

    Article  PubMed Central  PubMed  Google Scholar 

  • Yack HJ, Berger RC (1993) Dynamic stability in the elderly: identifying a possible measure. J Gerontol 48:M225–M230

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors wish to thank the participants and staff of the Laboratory for Gait and Neurodynamics at the Tel Aviv Sourasky Medical Center for their assistance and time, especially Marina Brozgol for her help in clinical evaluation.

This study was supported in part by the Michael J. Fox Foundation for Parkinson’s Research.

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Authors and Affiliations

  1. Laboratory for Gait and Neurodynamics, Movement Disorders Unit, Department of Neurology, Tel Aviv Sourasky Medical Center, 6 Weizman Street, 64239, Tel Aviv, Israel

    Aner Weiss, Talia Herman, Nir Giladi & Jeffrey M. Hausdorff

  2. Department of Neurology, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel

    Nir Giladi

  3. Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel

    Nir Giladi & Jeffrey M. Hausdorff

  4. Department of Physical Therapy, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel

    Jeffrey M. Hausdorff

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  1. Aner Weiss
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  2. Talia Herman
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  3. Nir Giladi
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  4. Jeffrey M. Hausdorff
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Correspondence to Jeffrey M. Hausdorff.

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Weiss, A., Herman, T., Giladi, N. et al. New evidence for gait abnormalities among Parkinson’s disease patients who suffer from freezing of gait: insights using a body-fixed sensor worn for 3 days. J Neural Transm 122, 403–410 (2015). https://doi.org/10.1007/s00702-014-1279-y

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  • DOI: https://doi.org/10.1007/s00702-014-1279-y

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