Skip to main content
SpringerLink
Log in

Local Stability of the Trunk in Patients with Degenerative Cerebellar Ataxia During Walking

  • Original Paper
  • Published:
The Cerebellum Aims and scope Submit manuscript

Abstract

This study aims to evaluate trunk local stability in a group of patients with degenerative primary cerebellar ataxia and to correlate it with spatio-temporal parameters, clinical variables, and history of falls. Sixteen patients affected by degenerative cerebellar ataxia and 16 gender- and age-matched healthy adults were studied by means of an inertial sensor to measure trunk kinematics and spatio-temporal parameters during over-ground walking. Trunk local dynamic stability was quantified by the maximum Lyapunov exponent with short data series of the acceleration data. According to this index, low values indicate more stable trunk dynamics, while high values denote less stable trunk dynamics. Disease severity was assessed by means of International Cooperative Ataxia Rating Scale (ICARS) according to which higher values correspond to more severe disease, while lower values correspond to less severe disease.

Patients displayed a higher short-term maximum Lyapunov exponent than controls in all three spatial planes, which was correlated with the age, onset of the disease, and history of falls. Furthermore, the maximum Lyapunov exponent was negatively correlated with ICARS balance, ICARS posture, and ICARS total scores.

These findings indicate that trunk local stability during gait is lower in patients with cerebellar degenerative ataxia than that in healthy controls and that this may increase the risk of falls. Local dynamic stability of the trunk seems to be an important aspect in patients with ataxia and could be a useful tool in the evaluation of rehabilitative and pharmacological treatment outcomes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Ilg W, Timmann D. Gait ataxia-specific cerebellar influences and their rehabilitation. Mov Disord. 2013;28:1566–75.

    Article  PubMed  Google Scholar 

  2. Wuehr M, Schniepp R, Ilmberger J, Brandt T, Jahn K. Speed-dependent temporospatial gait variability and long-range correlations in cerebellar ataxia. Gait Posture. 2013;37:214–18.

    Article  CAS  PubMed  Google Scholar 

  3. Schniepp R, Wuehr M, Schlick C, Huth S, Pradhan C, Dieterich M, et al. Increased gait variability is associated with the history of falls in patients with cerebellar ataxia. J Neurol. 2014;261:213–23.

    Article  PubMed  Google Scholar 

  4. Palliyath S, Hallett M, Thomas SL, Lebiedowska MK. Gait in patients with cerebellar ataxia. Mov Disord. 1998;13:958–64.

    Article  CAS  PubMed  Google Scholar 

  5. Stolze H, Klebe S, Petersen G, Raethjen J, Wenzelburger R, Witt K, et al. Typical features of cerebellar ataxic gait. J Neurol Neurosurg Psychiatry. 2002;73:310–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Morton SM, Bastian AJ. Cerebellar control of balance and locomotion. Neuroscientist. 2004;10:247–59.

    Article  PubMed  Google Scholar 

  7. Serrao M, Pierelli F, Ranavolo A, Draicchio F, Conte C, Don R, et al. Gait pattern in inherited cerebellar ataxias. Cerebellum. 2012;11:194–211.

    Article  PubMed  Google Scholar 

  8. Mitoma H, Hayashi R, Yanagisawa N, Tsukagoshi H. Characteristics of parkinsonian and ataxic gaits: a study using surface electromyograms, angular displacements and floor reaction forces. J Neurol Sci. 2000;174:22–39.

    Article  CAS  PubMed  Google Scholar 

  9. Earhart GM, Bastian AJ. Selection and coordination of human locomotor forms following cerebellar damage. J Neurophysiol. 2001;85:759–69.

    CAS  PubMed  Google Scholar 

  10. Martino G, Ivanenko YP, Serrao M, Ranavolo A, d’Avella A, Draicchio F, et al. Locomotor pattern in cerebellar ataxia. J Neurophysiol. 2014;112:2810–21.

    Article  CAS  PubMed  Google Scholar 

  11. Aizawa CY, Pedroso JL, Braga-Neto P, Callegari MR, Barsottini OG. Patients with autosomal dominant spinocerebellar ataxia have more risk of falls, important balance impairment, and decreased ability to function. Arq Neuropsiquiatr. 2013;71:508–11.

    Article  PubMed  Google Scholar 

  12. Mari S, Serrao M, Casali C, Conte C, Martino G, Ranavolo A, et al. Lower limb antagonist muscle co-activation and its relationship with gait parameters in cerebellar ataxia. Cerebellum. 2014;13:226–36.

    Article  CAS  PubMed  Google Scholar 

  13. Van de Warrenburg BP, Steijns JA, Munneke M, Kremer BP, Bloem BR. Falls in degenerative cerebellar ataxias. Mov Disord. 2005;20:497–500.

    Article  PubMed  Google Scholar 

  14. Nardone A, Schieppati M. The role of instrumental assessment of balance in clinical decision making. Eur J Phys Rehabil Med. 2010;46:221–37.

    CAS  PubMed  Google Scholar 

  15. Bruijn SM, Meijer OG, Beek PJ, van Dieen JH. Assessing the stability of human locomotion: a review of current measures. J R Soc Interface. 2013;10:20120999.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Dingwell JB, Cusumano JP. Nonlinear time series analysis of normal and pathological human walking. Chaos. 2000;10:848–63.

    Article  PubMed  Google Scholar 

  17. Hoogkamer W, Bruijn SM, Sunaert S, Swinnen SP, Van Calenbergh F, Duysens J. Toward new sensitive measures to evaluate gait stability in focal cerebellar lesion patients. Gait Posture. 2015;41:592–6.

    Article  PubMed  Google Scholar 

  18. Dingwell JB, Cusumano JP, Cavanagh PR, Sternad D. Local dynamic stability versus kinematic variability of continuous overground and treadmill walking. J Biomech Eng. 2001;123:27–32.

    Article  CAS  PubMed  Google Scholar 

  19. Dingwell JB, Marin LC. Kinematic variability and local dynamic stability of upper body motions when walking at different speeds. J Biomech. 2006;39:444–52.

    Article  PubMed  Google Scholar 

  20. Rosenstein MT, Collins JJ, De Luca CJ. A practical method for calculating largest Lyapunov exponents from small data set. Physica D Nonlinear Phenomena. 1993;65:117–34.

    Article  Google Scholar 

  21. Hof AL, Gazendam MG, Sinke WE. The condition for dynamic stability. J Biomech. 2005;38:1–8.

    Article  CAS  PubMed  Google Scholar 

  22. Hof AF, van Bockel RM, Schoppen T, Postema K. Control of lateral balance during walking experimental findings in normal subjects and above knee amputees. Gait Posture. 2007;25:250–8.

    Article  PubMed  Google Scholar 

  23. Esrafilian A, Karimi MT, Amiri P, Fatoye F. Performance of subjects with knee osteoarthritis during walking: differential parameters. Rheumatol Int. 2013;33:1753–61.

    Article  PubMed  Google Scholar 

  24. Holmes G. The cerebellum of man. Brain. 1939;62:1–30.

    Article  Google Scholar 

  25. Conte C, Pierelli F, Casali C, Ranavolo A, Draicchio F, Martino G, et al. Upper body kinematics in patients with cerebellar ataxia. Cerebellum. 2014;13:689–97.

    Article  PubMed  Google Scholar 

  26. Trouillas P, Takayanagi T, Hallett M, Currier RD, Subramony SH, Wessel K, et al. International Cooperative Ataxia Rating Scale for pharmacological assessment of the cerebellar syndrome. J Neurol Sci. 1997;145:205–11.

    Article  CAS  PubMed  Google Scholar 

  27. Reynard F, Terrier P. To what extent does not wearing shoes affect the local dynamic stability of walking?: effect size and intrasession repeatability. J Appl Biomech. 2014;30:305–9.

    Article  PubMed  Google Scholar 

  28. Van Schooten KS, Rispens SM, Elders PJM, van Dieen JH, Pijnapples M. Toward ambulatory balance assessment: estimating variability and stability from short bouts of gait. Gait Posture. 2014;39:696–99.

    Google Scholar 

  29. England SA, Granata KP. The influence of gait speed on local dynamic stability of walking. Gait Posture. 2007;25:172–78.

    Article  PubMed  Google Scholar 

  30. Van Schooten KS, Sloot LH, Bruijn SM, Kingma H, Meijer OG, Pijnapples M, et al. Sensitivity of trunk variability and stability measures to balance impairments induced by galvanic vestibular stimulation during gait. Gait Posture. 2014;33:656–60.

    Article  Google Scholar 

  31. Reynard F, Terrier P. Local dynamic stability of treadmill walking: intrasession and week-to-week repeatability. J Biomech. 2014;47:74–80.

    Article  PubMed  Google Scholar 

  32. Hak L, van Dieën JH, van der Wurff P, Prins MR, Mert A, Beek PJ, et al. Walking in an unstable environment: strategies used by transtibial amputees to prevent falling during gait. Arch Phys Med Rehabil. 2013;94(11):2186–93.

    Article  PubMed  Google Scholar 

  33. Reynard F, Vuadens P, Deriaz O, Terrier P. Could local dynamic stability serve as an early predictor of falls in patients with moderate neurological gait disorders? A reliability and comparison study in healthy individuals and in patients with paresis of the lower extremities. PLoS One. 2014;9:e100550.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Kao PC, Dingwell JB, Higginson JS, Binder-Macleod S. Dynamic instability during post-stroke hemiparetic walking. Gait Posture. 2014;40:457–63.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Hegger R, Kantz H, Schreiber T. Practical implementation of nonlinear time series methods: the TISEAN package. CHAOS. 1999;9:413.

    Article  PubMed  Google Scholar 

  36. Kennel MB, Brown R, Abarnel HDI. Determining embedding dimension for phase-space reconstruction using a geometrical construction. Phys Rev A. 1992;45:3403–11.

    Article  CAS  PubMed  Google Scholar 

  37. Fraser AM, Swinney HL. Independent coordinates for strange attractors from mutual information. Phys Rev A. 1986;33:1134–40.

    Article  CAS  Google Scholar 

  38. Lang TA, Altman DG. Basic statistical reporting for articles published in Biomedical Journals: the “Statistical Analyses and Methods in the Published Literature” or The SAMPL Guidelines”. 2013.Handbook, European Association of Science Editors

  39. Sullivan GM, Feinn R. Using effect size—or why the P value is not enough. Journal of Graduate Medical Education. 2012

  40. Liu J, Lockhart TE, Jones M, Martin T. Local dynamic stability assessment of motion impaired elderly using electronic textile pants. IEEE Trans Autom Sci Eng. 2008;5:696–702.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Lochart T, Liu J. Differentiating fall-prone and healthy adults using local dynamic stability. Ergonomics. 2008;51:1860–72.

    Article  Google Scholar 

  42. Bruijn SM, Van Impe A, Duysens J, Swinnen SP. White matter microstructural organization and gait stability in older adults. Front Aging Neurosci. 2014;6:104.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgment

GC is supported by the Italian Ministry of Health and Fondazione Roma financially.

Author information

Authors and Affiliations

  1. Department of Occupational and Environmental Medicine, Epidemiology and Hygiene, INAILE, Via Fontana Candida 1, 00040, Monte Porzio Catone, Italy

    Giorgia Chini, Alberto Ranavolo & Francesco Draicchio

  2. Movement Analysis LAB, Rehabilitation Centre Policlinico Italia, Piazza del Campidano 6, 00162, Rome, Italy

    Giorgia Chini & Mariano Serrao

  3. Department of Medical and Surgical Sciences and Biotechnologies, Sapienza University of Rome, Corso della Repubblica 79, Latina, 40100, Italy

    Carlo Casali, Luca Leonardi, Francesco Pierelli & Mariano Serrao

  4. Fondazione Don Gnocchi Foundation, Milan, Italy

    Carmela Conte & Luca Padua

  5. Centre of SpaceBio-Medicine, University of Rome Tor Vergata, Via Mont Pellier 1, 00133, Rome, Italy

    Giovanni Martino

  6. Department of Neurophysiology of Vision and Neurophthalmology, G.B. Bietti Foundation-IRCCS, Via Livenza 3, 00198, Rome, Italy

    Gianluca Coppola

  7. IRCCS Neuromed, Pozzilli, (IS), Italy

    Francesco Pierelli

Authors
  1. Giorgia Chini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alberto Ranavolo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Francesco Draicchio
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carlo Casali
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Carmela Conte
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Giovanni Martino
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Luca Leonardi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Luca Padua
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Gianluca Coppola
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Francesco Pierelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Mariano Serrao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mariano Serrao.

Ethics declarations

Conflict of Interest

The authors declare that they have no competing interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chini, G., Ranavolo, A., Draicchio, F. et al. Local Stability of the Trunk in Patients with Degenerative Cerebellar Ataxia During Walking. Cerebellum 16, 26–33 (2017). https://doi.org/10.1007/s12311-016-0760-6

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12311-016-0760-6

Keywords

Search

Navigation