Skip to main content
SpringerLink
Log in

Digital Motor Biomarkers of Cerebellar Ataxia Using an RGB-Depth Camera-Based Motion Analysis System

  • RESEARCH
  • Published:
The Cerebellum Aims and scope Submit manuscript

Abstract

This study aimed to identify quantitative biomarkers of motor function for cerebellar ataxia by evaluating gait and postural control using an RGB-depth camera-based motion analysis system. In 28 patients with degenerative cerebellar ataxia and 33 age- and sex-matched healthy controls, motor tasks (short-distance walk, closed feet stance, and stepping in place) were selected from a previously reported protocol, and scanned using Kinect V2 and customized software. The Clinical Assessment Scale for the Assessment and Rating of Ataxia (SARA) was also evaluated. Compared with the normal control group, the cerebellar ataxia group had slower gait speed and shorter step lengths, increased step width, and mediolateral trunk sway in the walk test (all P < 0.001). Lateral sway increased in the stance test in the ataxia group (P < 0.001). When stepping in place, the ataxia group showed higher arrhythmicity of stepping and increased stance time (P < 0.001). In the correlation analyses, the ataxia group showed a positive correlation between the total SARA score and arrhythmicity of stepping in place (r = 0.587, P = 0.001). SARA total score (r = 0.561, P = 0.002) and gait subscore (ρ = 0.556, P = 0.002) correlated with mediolateral truncal sway during walking. These results suggest that the RGB-depth camera-based motion analyses on mediolateral truncal sway during walking and arrhythmicity of stepping in place are useful digital motor biomarkers for the assessment of cerebellar ataxia, and could be utilized in future clinical trials.

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

Similar content being viewed by others

Data Availability

The data that support the findings of this study are available from the corresponding author, upon reasonable request.

References

  1. Bodranghien F, Bastian A, Casali C, Hallett M, Louis ED, Manto M, Marien P, Nowak DA, Schmahmann JD, Serrao M, Steiner KM, Strupp M, Tilikete C, Timmann D, van Dun K. Consensus paper: Revisiting the symptoms and signs of cerebellar syndrome. Cerebellum. 2016;15:369–91.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Cabaraux P, Agrawal SK, Cai H, Calabro RS, Casali C, Damm L, Doss S, Habas C, Horn AKE, Ilg W, Louis ED, Mitoma H, Monaco V, Petracca M, Ranavolo A, Rao AK, Ruggieri S, Schirinzi T, Serrao M, Summa S, Strupp M, Surgent O, Synofzik M, Tao S, Terasi H, Torres-Russotto D, Travers B, Roper JA, Manto M. Consensus paper: Ataxic gait. Cerebellum. 2023;22:394–430.

    Article  PubMed  Google Scholar 

  3. Maetzler W, Domingos J, Srulijes K, Ferreira JJ, Bloem BR. Quantitative wearable sensors for objective assessment of Parkinson’s disease. Mov Disord. 2013;28:1628–37.

    Article  PubMed  Google Scholar 

  4. Galna B, Barry G, Jackson D, Mhiripiri D, Olivier P, Rochester L. Accuracy of the Microsoft Kinect sensor for measuring movement in people with Parkinson’s disease. Gait Posture. 2014;39:1062–8.

    Article  PubMed  Google Scholar 

  5. Behrens JR, Mertens S, Kruger T, Grobelny A, Otte K, Mansow-Model S, Gusho E, Paul F, Brandt AU, Schmitz-Hübsch T. Validity of visual perceptive computing for static posturography in patients with multiple sclerosis. Mult Scler. 2016;22:1596–606.

    Article  PubMed  Google Scholar 

  6. Chini G, Ranavolo A, Draicchio F, Casali C, Conte C, Martino G, Leonardi L, Padua L, Coppola G, Pierelli F, Serrao M. Local stability of the trunk in patients with degenerative cerebellar ataxia during walking. Cerebellum. 2017;16:26–33.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  8. Hadjivassiliou M, Martindale J, Shanmugarajah P, Grunewald RA, Sarrigiannis PG, Beauchamp N, Garrard K, Warburton R, Sanders DS, Friend D, Duty S, Taylor J, Hoggard N. Causes of progressive cerebellar ataxia: prospective evaluation of 1500 patients. J Neurol Neurosurg Psychiatry. 2017;88:301–9.

    Article  CAS  PubMed  Google Scholar 

  9. Tsuji S, Onodera O, Goto J, Nishizawa M, Study Group on Ataxic D. Sporadic ataxias in Japan–a population-based epidemiological study. Cerebellum. 2008;7:189–97.

    Article  CAS  PubMed  Google Scholar 

  10. Sakai H, Yoshida K, Shimizu Y, Morita H, Ikeda S, Matsumoto N. Analysis of an insertion mutation in a cohort of 94 patients with spinocerebellar ataxia type 31 from Nagano, Japan. Neurogenetics. 2010;11:409–15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Buckley E, Mazza C, McNeill A. A systematic review of the gait characteristics associated with cerebellar ataxia. Gait Posture. 2018;60:154–63.

    Article  PubMed  Google Scholar 

  12. Schmitz-Hübsch 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. Scale for the assessment and rating of ataxia: development of a new clinical scale. Neurology. 2006;66:1717–20.

    Article  PubMed  Google Scholar 

  13. Yabe I, Matsushima M, Soma H, Basri R, Sasaki H. Usefulness of the scale for assessment and rating of ataxia (SARA). J Neurol Sci. 2008;266:164–6.

    Article  PubMed  Google Scholar 

  14. Ilg W, Seemann J, Giese M, Traschutz A, Schols L, Timmann D, Synofzik M. Real-life gait assessment in degenerative cerebellar ataxia toward ecologically valid biomarkers. Neurology. 2020;95:E1199–210.

    Article  CAS  PubMed  Google Scholar 

  15. Shah VV, Rodriguez-Labrada R, Horak FB, McNames J, Casey H, Hansson Floyd K, El-Gohary M, Schmahmann JD, Rosenthal LS, Perlman S, Velazquez-Perez L, Gomez CM. Gait variability in spinocerebellar ataxia assessed using wearable inertial sensors. Mov Disord. 2021;36:2922–31.

    Article  PubMed  Google Scholar 

  16. Otte K, Kayser B, Mansow-Model S, Verrel J, Paul F, Brandt AU, Schmitz-Hübsch T. Accuracy and reliability of the Kinect version 2 for clinical measurement of motor function. PLoS One. 2016;11:e0166532.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Muller B, Ilg W, Giese MA, Ludolph N. Validation of enhanced kinect sensor based motion capturing for gait assessment. PLoS One. 2017;12:e0175813.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Summa S, Tartarisco G, Favetta M, Buzachis A, Romano A, Bernava GM, Vasco G, Pioggia G, Petrarca M, Castelli E, Bertini E, Schirinzi T. Spatio-temporal parameters of ataxia gait dataset obtained with the Kinect. Data Brief. 2020;32:106307.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Otte K, Ellermeyer T, Suzuki M, Röhling HM, Kuroiwa R, Cooper G, Mansow-Model S, Mori M, Zimmermann H, Brandt AU, Paul F, Hirano S, Kuwabara S, Schmitz-Hübsch T. Cultural bias in motor function patterns: potential relevance for predictive, preventive, and personalized medicine. EPMA J. 2021;12:91–101.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Röhling HM, Otte K, Rekers S, Finke C, Rust R, Dorsch EM, Behnia B, Paul F, Schmitz-Hübsch T. RGB-depth camera-based assessment of motor capacity: normative data for six standardized motor tasks. Int J Environ Res Public Health. 2022;19:16989.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Behrens J, Pfuller C, Mansow-Model S, Otte K, Paul F, Brandt AU. Using perceptive computing in multiple sclerosis - the Short Maximum Speed Walk test. J Neuroeng Rehabil. 2014;11:89.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Grobelny A, Behrens JR, Mertens S, Otte K, Mansow-Model S, Kruger T, Gusho E, Bellmann-Strobl J, Paul F, Brandt AU, Schmitz-Hübsch T. Maximum walking speed in multiple sclerosis assessed with visual perceptive computing. PLoS One. 2017;12:e0189281.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Otte K, Ellermeyer T, Vater TS, Voigt M, Kroneberg D, Rasche L, Kruger T, Röhling HM, Kayser B, Mansow-Model S, Klostermann F, Brandt AU, Paul F, Lipp A, Schmitz-Hübsch T. Instrumental assessment of stepping in place captures clinically relevant motor symptoms of Parkinson’s disease. Sensors (Basel). 2020;20:5465.

  24. Abele M, Burk K, Schols L, Schwartz S, Besenthal I, Dichgans J, Zuhlke C, Riess O, Klockgether T. The aetiology of sporadic adult-onset ataxia. Brain. 2002;125:961–8.

    Article  CAS  PubMed  Google Scholar 

  25. Gilman S, Wenning GK, Low PA, Brooks DJ, Mathias CJ, Trojanowski JQ, Wood NW, Colosimo C, Durr A, Fowler CJ, Kaufmann H, Klockgether T, Lees A, Poewe W, Quinn N, Revesz T, Robertson D, Sandroni P, Seppi K, Vidailhet M. Second consensus statement on the diagnosis of multiple system atrophy. Neurology. 2008;71:670–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Plotnik M, Giladi N, Balash Y, Peretz C, Hausdorff JM. Is freezing of gait in Parkinson’s disease related to asymmetric motor function? Ann Neurol. 2005;57:656–63.

    Article  PubMed  Google Scholar 

  27. Schmitz-Hübsch T, Fimmers R, Rakowicz M, Rola R, Zdzienicka E, Fancellu R, Mariotti C, Linnemann C, Schols L, Timmann D, Filla A, Salvatore E, Infante J, Giunti P, Labrum R, Kremer B, van de Warrenburg BP, Baliko L, Melegh B, Depondt C, Schulz J, du Montcel ST, Klockgether T. Responsiveness of different rating instruments in spinocerebellar ataxia patients. Neurology. 2010;74:678–84.

    Article  PubMed  Google Scholar 

  28. Nantel J, McDonald JC, Tan S, Bronte-Stewart H. Deficits in visuospatial processing contribute to quantitative measures of freezing of gait in Parkinson’s disease. Neuroscience. 2012;221:151–6.

    Article  CAS  PubMed  Google Scholar 

  29. Dalton C, Sciadas R, Nantel J. Executive function is necessary for the regulation of the stepping activity when stepping in place in older adults. Aging Clin Exp Res. 2016;28:909–15.

    Article  PubMed  Google Scholar 

  30. Morton SM, Bastian AJ. Relative contributions of balance and voluntary leg-coordination deficits to cerebellar gait ataxia. J Neurophysiol. 2003;89:1844–56.

    Article  PubMed  Google Scholar 

  31. Morton SM, Bastian AJ. Mechanisms of cerebellar gait ataxia. Cerebellum. 2007;6:79–86.

    Article  PubMed  Google Scholar 

  32. Shirai S, Yabe I, Matsushima M, Ito YM, Yoneyama M, Sasaki H. Quantitative evaluation of gait ataxia by accelerometers. J Neurol Sci. 2015;358:253–8.

    Article  PubMed  Google Scholar 

  33. Schniepp R, Wuehr M, Neuhaeusser M, Kamenova M, Dimitriadis K, Klopstock T, Strupp M, Brandt T, Jahn K. Locomotion speed determines gait variability in cerebellar ataxia and vestibular failure. Mov Disord. 2012;27:125–31.

    Article  PubMed  Google Scholar 

  34. 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;37:214–8.

    Article  CAS  PubMed  Google Scholar 

  35. Castiglia SF, Trabassi D, Tatarelli A, Ranavolo A, Varrecchia T, Fiori L, Di Lenola D, Cioffi E, Raju M, Coppola G, Caliandro P, Casali C, Serrao M. Identification of gait unbalance and fallers among subjects with cerebellar ataxia by a set of trunk acceleration-derived indices of gait. Cerebellum. 2023;22:46–58.

    Article  PubMed  Google Scholar 

  36. Manto M, Marmolino D. Cerebellar ataxias. Curr Opin Neurol. 2009;22:419–29.

    Article  PubMed  Google Scholar 

  37. Lanzetta D, Cattaneo D, Pellegatta D, Cardini R. Trunk control in unstable sitting posture during functional activities in healthy subjects and patients with multiple sclerosis. Arch Phys Med Rehabil. 2004;85:279–83.

    Article  PubMed  Google Scholar 

  38. Kavanagh JJ, Morrison S, Barrett RS. Coordination of head and trunk accelerations during walking. Eur J Appl Physiol. 2005;94:468–75.

    Article  CAS  PubMed  Google Scholar 

  39. Van de Warrenburg BP, Bakker M, Kremer BP, Bloem BR, Allum JH. Trunk sway in patients with spinocerebellar ataxia. Mov Disord. 2005;20:1006–13.

    Article  PubMed  Google Scholar 

  40. Bunn LM, Marsden JF, Giunti P, Day BL. Stance instability in spinocerebellar ataxia type 6. Mov Disord. 2013;28:510–6.

    Article  PubMed  Google Scholar 

  41. Sullivan EV, Rose J, Pfefferbaum A. Physiological and focal cerebellar substrates of abnormal postural sway and tremor in alcoholic women. Biol Psychiatry. 2010;67:44–51.

    Article  PubMed  PubMed Central  Google Scholar 

  42. 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 

  43. Ebersbach G, Sojer M, Valldeoriola F, Wissel J, Muller J, Tolosa E, Poewe W. Comparative analysis of gait in Parkinson’s disease, cerebellar ataxia and subcortical arteriosclerotic encephalopathy. Brain. 1999;122(Pt 7):1349–55.

    Article  PubMed  Google Scholar 

  44. Ilg W, Golla H, Thier P, Giese MA. Specific influences of cerebellar dysfunctions on gait. Brain. 2007;130:786–98.

    Article  PubMed  Google Scholar 

  45. Ilg W, Giese MA, Gizewski ER, Schoch B, Timmann D. The influence of focal cerebellar lesions on the control and adaptation of gait. Brain. 2008;131:2913–27.

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  47. Barak Y, Wagenaar RC, Holt KG. Gait characteristics of elderly people with a history of falls: a dynamic approach. Phys Ther. 2006;86:1501–10.

    Article  PubMed  Google Scholar 

  48. Hollman JH, Kovash FM, Kubik JJ, Linbo RA. Age-related differences in spatiotemporal markers of gait stability during dual task walking. Gait Posture. 2007;26:113–9.

    Article  PubMed  Google Scholar 

  49. Hausdorff JM. Stride variability: beyond length and frequency. Gait Posture. 2004;20:304 (author reply 5).

    Article  CAS  PubMed  Google Scholar 

  50. 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 

  51. van Schooten KS, Sloot LH, Bruijn SM, Kingma H, Meijer OG, Pijnappels M, van Dieen JH. Sensitivity of trunk variability and stability measures to balance impairments induced by galvanic vestibular stimulation during gait. Gait Posture. 2011;33:656–60.

    Article  PubMed  Google Scholar 

  52. van Schooten KS, Rispens SM, Elders PJ, van Dieen JH, Pijnappels M. Toward ambulatory balance assessment: estimating variability and stability from short bouts of gait. Gait Posture. 2014;39:695–9.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank all the participants for their contributions to this study. We are also grateful to the staff members of the Division of Rehabilitation Medicine, Chiba University Hospital, for their technical support.

Author information

Authors and Affiliations

  1. Department of Neurology, Graduate School of Medicine, Chiba University, 1-8-1 Inohana, Chuo-Ku, Chiba-Shi, Chiba, 260-8670, Japan

    Masahide Suzuki, Shigeki Hirano, Michiko Izumi, Mitsuyoshi Tamura, Atsuhiko Sugiyama, Masahiro Mori & Satoshi Kuwabara

  2. Department of Functional Brain Imaging Research, Institute for Quantum Medical Science, National Institute for Quantum Science and Technology, Chiba, Japan

    Shigeki Hirano & Mitsuyoshi Tamura

  3. Experimental and Clinical Research Center, a cooperation of Max Delbrueck Center for Molecular Medicine and Charité - Universitätsmedizin Berlin, Berlin, Germany

    Karen Otte, Tanja Schmitz-Hübsch, Hanna M. Röhling, Alexander U. Brandt & Friedemann Paul

  4. Motognosis GmbH, Berlin, Germany

    Karen Otte & Hanna M. Röhling

  5. Neuroscience Clinical Research Center, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität Zu Berlin, Berlin, Germany

    Tanja Schmitz-Hübsch, Alexander U. Brandt & Friedemann Paul

  6. Division of Rehabilitation Medicine, Chiba University Hospital, Chiba, Japan

    Ryota Kuroiwa & Atsushi Murata

  7. Department of Neurology, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität Zu Berlin, Berlin, Germany

    Friedemann Paul

Authors
  1. Masahide Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shigeki Hirano
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Karen Otte
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tanja Schmitz-Hübsch
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michiko Izumi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mitsuyoshi Tamura
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ryota Kuroiwa
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Atsuhiko Sugiyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Masahiro Mori
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Hanna M. Röhling
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Alexander U. Brandt
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Atsushi Murata
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Friedemann Paul
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Satoshi Kuwabara
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MS: data acquisition, writing manuscript; SH; project administration, participant administration, data curation, writing manuscript; KO: Data acquisition and analysis, software, editing manuscript; TSH: study design, editing manuscript; MI, MT; data acquisition and curation; RK, AS: participant administration, editing manuscript; MM: project management, editing manuscript; HMR: data curation, software, reviewing manuscript; AUB, AM, FP, SK: supervision and reviewing manuscript.

Corresponding author

Correspondence to Shigeki Hirano.

Ethics declarations

Ethical Approval

This study was approved by the Ethics Committee of the Graduate School of Medicine, Chiba University (approval no. 3174). Written informed consent for participation and publication was obtained.

Competing Interests

KO and AUB are shareholders of Motognosis GmbH and are named inventors of patent applications describing perceptive visual computing for tracking motor dysfunction. HMR was employed at Motognosis GmbH. All the other authors have no conflicts of interest to declare relevant to the content of this article.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Suzuki, M., Hirano, S., Otte, K. et al. Digital Motor Biomarkers of Cerebellar Ataxia Using an RGB-Depth Camera-Based Motion Analysis System. Cerebellum (2023). https://doi.org/10.1007/s12311-023-01604-7

Download citation

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12311-023-01604-7

Keywords

Search

Navigation