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Increased gait variability is associated with the history of falls in patients with cerebellar ataxia

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Abstract

Falls are common in patients with cerebellar ataxia (CA). Identification of gait variables associated with a higher risk of falls allows us to detect fallers and initiate protective procedures early. Gait variability, which is increased in CA patients, is a good predictor of falls in elderly subjects and patients with neurodegenerative diseases. The relationship between gait variability and fall risk in patients with different cerebellar disorders was systematically investigated. A total of 48 patients with different cerebellar ataxia entities [adult-onset cerebellar atrophy (SAOA) (n = 23), unknown entity (n = 7), vascular (n = 5), post-cerebellitis (n = 6), congenital (n = 2), Louis–Bar syndrome (n = 2), ethyltoxic (n = 2) posttraumatic (n = 1)] were examined using a GAITRite® sensor mat. Spatial and temporal variability parameters were used for ANOVA testing and logistic regression models with categorized fall events as dependent variables. Gait variability in the fore–aft direction showed significant differences between the fall groups (p < 0.05–0.01). Model effects were highest for walking with slow speed (correct prediction 0.50–0.72). The speed-dependent integral of gait variability markers showed a higher discriminatory power (correct prediction 0.74–0.94). Gait variability is linked to the fall risk of patients with CA, slow walking and temporal gait variability being most relevant. The use of speed-dependent integrals of gait variability improves the accuracy of fall prediction. To predict fall risks in cerebellar ataxia, gait variability measurements made during slow walking should be included in a gait analysis procedure. The effects of speed-adjusted physiotherapeutic interventions have to be further investigated.

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References

  1. Arfken CL, Lach HW, Birge SJ, Miller JP (1994) The prevalence and correlates of fear of falling in elderly persons living in the community. Am J Public Health 84:565–570

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  2. Bauby CE, Kuo AD (2000) Active control of lateral balance in human walking. J Biomech 33:1433–1440

    Article  CAS  PubMed  Google Scholar 

  3. Beauchet O, Allali G, Annweiler C, Bridenbaugh S, Assal F, Kressig RW, Herrmann FR (2009) Gait variability among healthy adults: low and high stride-to-stride variability are both a reflection of gait stability. Gerontology 55:702–706

    Article  PubMed  Google Scholar 

  4. Berg KO, Maki BE, Williams JI, Holliday PJ, Wood-Dauphinee SL (1992) Clinical and laboratory measures of postural balance in an elderly population. Arch Phys Med Rehabil 73:1073–1080

    CAS  PubMed  Google Scholar 

  5. Bloem BR, Hausdorff JM, Visser JE, Giladi N (2004) Falls and freezing of gait in Parkinson’s disease: a review of two interconnected, episodic phenomena. Mov Disord 19:871–884

    Article  PubMed  Google Scholar 

  6. Chiou WL (1978) Critical evaluation of the potential error in pharmacokinetic studies of using the linear trapezoidal rule method for the calculation of the area under the plasma level-time curve. J Pharmacokinet Biopharm 6:539–546

    Article  CAS  PubMed  Google Scholar 

  7. Coelho FG, Stella F, de Andrade LP, Barbieri FA, Santos-Galduroz RF, Gobbi S, Costa JL, Gobbi LT (2012) Gait and risk of falls associated with frontal cognitive functions at different stages of Alzheimer’s disease. Neuropsychol Dev Cogn B Aging Neuropsychol Cogn 19:644–656

    Article  PubMed  Google Scholar 

  8. Cumming RG, Kelsey JL, Nevitt MC (1990) Methodologic issues in the study of frequent and recurrent health problems. Falls in the elderly. Ann Epidemiol 1:49–56

    Article  CAS  PubMed  Google Scholar 

  9. Cummings SR, Nevitt MC (1994) Falls. N Engl J Med 331:872–873

    Article  CAS  PubMed  Google Scholar 

  10. Ebersbach G, Sojer M, Valldeoriola F, Wissel J, Muller J, Tolosa E, Poewe W (1999) Comparative analysis of gait in Parkinson’s disease, cerebellar ataxia and subcortical arteriosclerotic encephalopathy. Brain 122(Pt 7):1349–1355

    Article  PubMed  Google Scholar 

  11. Fonteyn EM, Schmitz-Hubsch T, Verstappen CC, Baliko L, Bloem BR, Boesch S, Bunn L, Charles P, Durr A, Filla A, Giunti P, Globas C, Klockgether T, Melegh B, Pandolfo M, De Rosa A, Schols L, Timmann D, Munneke M, Kremer BP, van de Warrenburg BP (2010) Falls in spinocerebellar ataxias: results of the EuroSCA fall study. Cerebellum 9:232–239

    Article  PubMed  Google Scholar 

  12. Fonteyn EM, Schmitz-Hubsch T, Verstappen CC, Baliko L, Bloem BR, Boesch S, Bunn L, Giunti P, Globas C, Klockgether T, Melegh B, Pandolfo M, Schols L, Timmann D, van de Warrenburg BP (2013) Prospective analysis of falls in dominant ataxias. Eur Neurol 69:53–57

    Article  CAS  PubMed  Google Scholar 

  13. Greenberg SA (2012) Analysis of measurement tools of fear of falling for high-risk, community-dwelling older adults. Clin Nurs Res 21:113–130

    Article  PubMed  Google Scholar 

  14. Hand DJ, Till RJ (2001) A simple generalisation of the area under the ROC curve for multiple class classification problems. Machine Learn 45:171–186

    Article  Google Scholar 

  15. Hausdorff JM (2009) Gait dynamics in Parkinson’s disease: common and distinct behavior among stride length, gait variability, and fractal-like scaling. Chaos 19:026113

    Article  PubMed Central  PubMed  Google Scholar 

  16. Hausdorff JM (2005) Gait variability: methods, modeling and meaning. J Neuroeng Rehabil 2:19

    Article  PubMed Central  PubMed  Google Scholar 

  17. Hausdorff JM, Cudkowicz ME, Firtion R, Wei JY, Goldberger AL (1998) Gait variability and basal ganglia disorders: stride-to-stride variations of gait cycle timing in Parkinson’s disease and Huntington’s disease. Mov Disord 13:428–437

    Article  CAS  PubMed  Google Scholar 

  18. Hausdorff JM, Edelberg HK, Cudkowicz ME, Singh MA, Wei JY (1997) The relationship between gait changes and falls. J Am Geriatr Soc 45:1406

    Article  CAS  PubMed  Google Scholar 

  19. Hausdorff JM, Edelberg HK, Mitchell SL, Goldberger AL, Wei JY (1997) Increased gait unsteadiness in community-dwelling elderly fallers. Arch Phys Med Rehabil 78:278–283

    Article  CAS  PubMed  Google Scholar 

  20. Hausdorff JM, Mitchell SL, Firtion R, Peng CK, Cudkowicz ME, Wei JY, Goldberger AL (1997) Altered fractal dynamics of gait: reduced stride-interval correlations with aging and Huntington’s disease. J Appl Physiol 82:262–269

    CAS  PubMed  Google Scholar 

  21. Hausdorff JM, Rios DA, Edelberg HK (2001) Gait variability and fall risk in community-living older adults: a 1-year prospective study. Arch Phys Med Rehabil 82:1050–1056

    Article  CAS  PubMed  Google Scholar 

  22. 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 

  23. Herman T, Giladi N, Gurevich T, Hausdorff JM (2005) Gait instability and fractal dynamics of older adults with a “cautious” gait: why do certain older adults walk fearfully? Gait Posture 21:178–185

    Article  CAS  PubMed  Google Scholar 

  24. Ilg W, Giese MA, Gizewski ER, Schoch B, Timmann D (2008) The influence of focal cerebellar lesions on the control and adaptation of gait. Brain 131:2913–2927

    Article  CAS  PubMed  Google Scholar 

  25. Ilg W, Golla H, Thier P, Giese MA (2007) Specific influences of cerebellar dysfunctions on gait. Brain 130:786–798

    Article  PubMed  Google Scholar 

  26. Jordan K, Challis JH, Newell KM (2007) Speed influences on the scaling behavior of gait cycle fluctuations during treadmill running. Hum Mov Sci 26:87–102

    Article  PubMed  Google Scholar 

  27. Kropelin TF, Neyens JC, Halfens RJ, Kempen GI, Hamers JP (2013) Fall determinants in older long-term care residents with dementia: a systematic review. Int Psychogeriatr 25:549–563

    Article  PubMed  Google Scholar 

  28. Lamoth CJ, van Deudekom FJ, van Campen JP, Appels BA, de Vries OJ, Pijnappels M (2011) Gait stability and variability measures show effects of impaired cognition and dual tasking in frail people. J Neuroeng Rehabil 8:2

    Article  PubMed Central  PubMed  Google Scholar 

  29. Mackenzie L, Byles J, D’Este C (2006) Validation of self-reported fall events in intervention studies. Clin Rehabil 20:331–339

    Article  PubMed  Google Scholar 

  30. Nelson AJ, Zwick D, Brody S, Doran C, Pulver L, Rooz G, Sadownick M, Nelson R, Rothman J (2002) The validity of the GaitRite and the functional ambulation performance scoring system in the analysis of Parkinson gait. NeuroRehabilitation 17:255–262

    PubMed  Google Scholar 

  31. O’Connor SM, Kuo AD (2009) Direction-dependent control of balance during walking and standing. J Neurophysiol 102:1411–1419

    Article  PubMed Central  PubMed  Google Scholar 

  32. Palliyath S, Hallett M, Thomas SL, Lebiedowska MK (1998) Gait in patients with cerebellar ataxia. Mov Disord 13:958–964

    Article  CAS  PubMed  Google Scholar 

  33. Powell LE, Myers AM (1995) The activities-specific balance confidence (ABC) scale. J Gerontol Ser A Biol Sci Med Sci 50:M28–M34

    Article  Google Scholar 

  34. Pruessner JC, Kirschbaum C, Meinlschmid G, Hellhammer DH (2003) Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology 28:916–931

    Article  CAS  PubMed  Google Scholar 

  35. Rumelin A, Fauth U, Meyer M, Halmagyi M (2002) Clearance of ascorbic acid in plasma in patients before major maxillofacial surgery compared with that in volunteers. Nutr Cancer 42:59–61

    Article  PubMed  Google Scholar 

  36. Schmitz-Hubsch T, du Montcel ST, Baliko L, Berciano J, Boesch S, Depondt C, Giunti P, Globas C, Infante J, Kang JS, Kremer B, Mariotti C, Melegh B, Pandolfo M, Rakowicz M, Ribai P, Rola R, Schols L, Szymanski S, van de Warrenburg BP, Durr A, Klockgether T, Fancellu R (2006) Scale for the assessment and rating of ataxia: development of a new clinical scale. Neurology 66:1717–1720

    Article  CAS  PubMed  Google Scholar 

  37. Schniepp R, Wuehr M, Ackl N, Danek A, Brandt T, Strupp M, Jahn K (2011) 4-Aminopyridine improves gait variability in cerebellar ataxia due to CACNA 1A mutation. J Neurol 258:1708–1711

    Article  PubMed  Google Scholar 

  38. Schniepp R, Wuehr M, Neuhaeusser M, Benecke AK, Adrion C, Brandt T, Strupp M, Jahn K (2012) 4-aminopyridine and cerebellar gait: a retrospective case series. J Neurol 259:2491–2493

    Article  PubMed  Google Scholar 

  39. Schniepp R, Wuehr M, Neuhaeusser M, Kamenova M, Dimitriadis K, Klopstock T, Strupp M, Brandt T, Jahn K (2012) Locomotion speed determines gait variability in cerebellar ataxia and vestibular failure. Mov Disord 27:125–131

    Article  PubMed  Google Scholar 

  40. Serrao M, Pierelli F, Ranavolo A, Draicchio F, Conte C, Don R, Di Fabio R, LeRose M, Padua L, Sandrini G, Casali C (2012) Gait pattern in inherited cerebellar ataxias. Cerebellum 11:194–211

    Article  PubMed  Google Scholar 

  41. Sheridan PL, Solomont J, Kowall N, Hausdorff JM (2003) Influence of executive function on locomotor function: divided attention increases gait variability in Alzheimer’s disease. J Am Geriatr Soc 51:1633–1637

    Article  PubMed  Google Scholar 

  42. Snaterse M, Ton R, Kuo AD, Donelan JM (2011) Distinct fast and slow processes contribute to the selection of preferred step frequency during human walking. J Appl Physiol 110:1682–1690

    Article  PubMed Central  PubMed  Google Scholar 

  43. Sterke CS, van Beeck EF, Looman CW, Kressig RW, van der Cammen TJ (2012) An electronic walkway can predict short-term fall risk in nursing home residents with dementia. Gait Posture 36:95–101

    Article  PubMed  Google Scholar 

  44. Stolze H, Klebe S, Petersen G, Raethjen J, Wenzelburger R, Witt K, Deuschl G (2002) Typical features of cerebellar ataxic gait. J Neurol Neurosurg Psychiatry 73:310–312

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  45. Tinetti ME, Speechley M (1989) Prevention of falls among the elderly. N Engl J Med 320:1055–1059

    Article  CAS  PubMed  Google Scholar 

  46. van de Warrenburg BP, Steijns JA, Munneke M, Kremer BP, Bloem BR (2005) Falls in degenerative cerebellar ataxias. Mov Disord 20:497–500

    Article  PubMed  Google Scholar 

  47. Wrisley DM, Marchetti GF, Kuharsky DK, Whitney SL (2004) Reliability, internal consistency, and validity of data obtained with the functional gait assessment. Phys Ther 84:906–918

    PubMed  Google Scholar 

  48. Wuehr M, Schniepp R, Ilmberger J, Brandt T, Jahn K (2013) Speed-dependent temporospatial gait variability and long-range correlations in cerebellar ataxia. Gait Posture 37:214–218

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors thank Judy Benson for copy-editing the article. The work was supported by the German Research Foundation (Deutsche Forschungsgemeinschaft, DFG JA 1087/1-1), the German Hertie Foundation and the Federal Ministry for Education and Science (BMBF, Nr. 80121000-49) of Germany.

Conflicts of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

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Authors and Affiliations

  1. Department of Neurology, University of Munich, Marchioninistrasse 15, 81377, Munich, Germany

    Roman Schniepp, Cornelia Schlick, Marianne Dieterich & Klaus Jahn

  2. German Center for Vertigo and Balance Disorders (DSGZ), University of Munich, Munich, Germany

    Roman Schniepp, Max Wuehr, Cornelia Schlick, Sabrina Huth, Cauchy Pradhan, Marianne Dieterich, Thomas Brandt & Klaus Jahn

  3. Institute for Clinical Neurosciences, University of Munich, Munich, Germany

    Thomas Brandt

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  1. Roman Schniepp
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Correspondence to Roman Schniepp.

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Schniepp, R., Wuehr, M., Schlick, C. et al. Increased gait variability is associated with the history of falls in patients with cerebellar ataxia. J Neurol 261, 213–223 (2014). https://doi.org/10.1007/s00415-013-7189-3

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  • DOI: https://doi.org/10.1007/s00415-013-7189-3

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