SpringerLink
Log in

Assessment of gait and balance impairment in people with spinocerebellar ataxia using wearable sensors

  • Original Article
  • Published:
Neurological Sciences Aims and scope Submit manuscript

Abstract

Objective

To explore the use of wearable sensors for objective measurement of motor impairment in spinocerebellar ataxia (SCA) patients during clinical assessments of gait and balance.

Methods

In total, 14 patients with genetically confirmed SCA (mean age 61.6 ± 8.6 years) and 4 healthy controls (mean age 49.0 ± 16.4 years) were recruited through the Massachusetts General Hospital (MGH) Ataxia Center. Participants donned seven inertial sensors while performing two independent trials of gait and balance assessments from the Scale for the Assessment and Rating of Ataxia (SARA) and Brief Ataxia Rating Scale (BARS2). Univariate analysis was used to identify sensor-derived metrics from wearable sensors that discriminate motor function between the SCA and control groups. Multivariate linear regression models were used to estimate the subjective in-person SARA/BARS2 ratings. Spearman correlation coefficients were used to evaluate the performance of the model.

Results

Stride length variability, stride duration, cadence, stance phase, pelvis sway, and turn duration were different between SCA and controls (p < 0.05). Similarly, sway and sway velocity of the ankle, hip, and center of mass differentiated SCA and controls (p < 0.05). Using these features, linear regression models showed moderate-to-strong correlation with clinical scores from the in-person rater during SARA assessments of gait (r = 0.73, p = 0.003) and stance (r = 0.90, p < 0.001) and the BARS2 gait assessment (r = 0.74, p = 0.003).

Conclusion

This study demonstrates that sensor-derived metrics can potentially be used to estimate the level of motor impairment in patient with SCA quickly and objectively. Thus, digital biomarkers from wearable sensors have the potential to be an integral tool for SCA clinical trials and care.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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 study was an industry-sponsored study and collected data are not available to the public.

Code availability

The study was an industry-sponsored study and codes are not available to the public.

References

  1. Manto M, Gruol DL, Schmahmann JD, Koibuchi N, Rossi F (eds) (2013) Handbook of the cerebellum and cerebellar disorders. Springer Netherlands

    Google Scholar 

  2. Klockgether T, Mariotti C, Paulson HL (2019) Spinocerebellar ataxia. Nat Rev Dis Primers 5(1):24. https://doi.org/10.1038/s41572-019-0074-3

    Article  PubMed  Google Scholar 

  3. Van de Warrenburg B et al (2002) Spinocerebellar ataxias in the Netherlands: prevalence and age at onset variance analysis. Neurology 58(5):702–708

    Article  Google Scholar 

  4. López-Bastida J, Perestelo-Pérez L, Montón-álvarez F, Serrano-Aguilar P (2008) Social economic costs and health-related quality of life in patients with degenerative cerebellar ataxia in Spain. Mov Disord 23(2):212–217

    Article  Google Scholar 

  5. van de Warrenburg BP, Steijns JA, Munneke M, Kremer BP, Bloem BR (2005) Falls in degenerative cerebellar ataxias. Mov Disord 20(4):497–500

    Article  Google Scholar 

  6. Fonteyn EMR et al (2010) Falls in spinocerebellar ataxias: results of the EuroSCA Fall Study. Cerebellum 9(2):232–239. https://doi.org/10.1007/s12311-010-0155-z

    Article  PubMed  Google Scholar 

  7. Garali I et al (2018) A strategy for multimodal data integration: application to biomarkers identification in spinocerebellar ataxia. Brief Bioinform 19(6):1356–1369

    Article  Google Scholar 

  8. Luo L et al (2017) The initial symptom and motor progression in spinocerebellar ataxias. Cerebellum 16(3):615–622. https://doi.org/10.1007/s12311-016-0836-3

    Article  PubMed  PubMed Central  Google Scholar 

  9. Trouillas P et al (1997) International Cooperative Ataxia Rating Scale for pharmacological assessment of the cerebellar syndrome. J Neurol Sci 145(2):205–211

    Article  CAS  Google Scholar 

  10. Schmitz-Hübsch T et al (2006) Scale for the assessment and rating of ataxia: development of a new clinical scale. Neurology 66(11):1717–1720

    Article  Google Scholar 

  11. Schmahmann JD, Gardner R, MacMore J, Vangel MG (2009) Development of a brief ataxia rating scale (BARS) based on a modified form of the ICARS. Mov Disord 24(12):1820–1828

    Article  Google Scholar 

  12. Storey E, Tuck K, Hester R, Hughes A, Churchyard A (2004) Inter-rater reliability of the International Cooperative Ataxia Rating scale (ICARS). Mov Disord Off J Mov Disord Soc 19(2):190–192

    Article  Google Scholar 

  13. Wilson RB (2006) Experimental therapeutics for Friedreich ataxia. Elsevier, Burlington

    Google Scholar 

  14. Klucken J et al (2013) Unbiased and mobile gait analysis detects motor impairment in Parkinson’s disease. PloS one 8(2):e56956

    Article  CAS  Google Scholar 

  15. R. Jaroensri et al., “A Video-Based Method for Automatically Rating Ataxia,” in Proceedings of 2nd Machine Learning for Healthcare, Boston, MA, Aug. 2017, vol. 68, pp. 201–160.

  16. Grobe-Einsler M et al (2021) Development of SARAhome, a new video-based tool for the assessment of ataxia at home. Mov Disord. https://doi.org/10.1002/mds.28478

    Article  PubMed  Google Scholar 

  17. Phan D, Nguyen N, Pathirana PN, Horne M, Power L, Szmulewicz D (2020) A random forest approach for quantifying gait ataxia with truncal and peripheral measurements using multiple wearable sensors. IEEE Sens J 20(2):723–734. https://doi.org/10.1109/JSEN.2019.2943879

    Article  Google Scholar 

  18. Arcuria G et al (2020) Develo** a smartphone application, triaxial accelerometer-based, to quantify static and dynamic balance deficits in patients with cerebellar ataxias. J Neurol 267(3):625–639. https://doi.org/10.1007/s00415-019-09570-z

    Article  PubMed  Google Scholar 

  19. Pulliam CL, Burack MA, Heldman DA, Giuffrida JP, Mera TO (2014) Motion sensor dyskinesia assessment during activities of daily living. J Parkinsons Dis 4(4):609–615. https://doi.org/10.3233/JPD-140348

    Article  CAS  PubMed  Google Scholar 

  20. Aminian K, Najafi B, Büla C, Leyvraz P-F, Robert P (2002) Spatio-temporal parameters of gait measured by an ambulatory system using miniature gyroscopes. J Biomech 35(5):689–699

    Article  Google Scholar 

  21. Najafi B, Bharara M, Talal TK, Armstrong DG (2012) Advances in balance assessment and balance training for diabetes. Diabetes Manag 2(4):293–308

    Article  CAS  Google Scholar 

  22. Margolin BH, Light RJ (1974) An analysis of variance for categorical data, II: small sample comparisons with chi square and other competitors. J Am Stat Assoc 69(347):755–764

    Article  Google Scholar 

  23. Mann HB, Whitney DR (1947) On a test of whether one of two random variables is stochastically larger than the other. Ann Math Statist 18(1):50–60. https://doi.org/10.1214/aoms/1177730491

    Article  Google Scholar 

  24. Okeh U et al (2009) Statistical analysis of the application of Wilcoxon and Mann-Whitney U test in medical research studies. Biotechnol Mol Biol Rev 4(6):128–131

    Google Scholar 

  25. Akoglu H (2018) User’s guide to correlation coefficients. Turk J Emerg Med 18(3):91–93

    Article  Google Scholar 

  26. Koo TK, Li MY (2016) A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med 15(2):155–163

    Article  Google Scholar 

  27. Cohen J (2013) Statistical power analysis for the behavioral sciences. Academic press. Accessed 15 May 2021

    Book  Google Scholar 

  28. Tibshirani RJ, Efron B (1993) An introduction to the bootstrap. Monogr Statist Appl Probab 57:1–436

    Google Scholar 

  29. Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52(3/4):591–611. https://doi.org/10.2307/2333709

    Article  Google Scholar 

  30. Pearson K (1920) Notes on the history of correlation. Biometrika 13(1):25–45. https://doi.org/10.2307/2331722

    Article  Google Scholar 

  31. Van de Warrenburg BP, Bakker M, Kremer BP, Bloem BR, Allum JH (2005) Trunk sway in patients with spinocerebellar ataxia. Mov Disord Off J Mov Disord Soc 20(8):1006–1013

    Article  Google Scholar 

  32. Yabe I, Matsushima M, Soma H, Basri R, Sasaki H (2008) Usefulness of the Scale for Assessment and Rating of Ataxia (SARA). J Neurol Sci 266(1–2):164–166

    Article  Google Scholar 

  33. Matsushima A et al (2015) Clinical assessment of standing and gait in ataxic patients using a triaxial accelerometer. Cerebellum Ataxias 2(1):1–7

    Article  Google Scholar 

  34. E. Parikesit, T. L. R. Mengko, and H. Zakaria (2011) Wearable gait measurement system based on accelerometer and pressure sensor. In 2011 2nd International Conference on Instrumentation, Communications, Information Technology, and Biomedical Engineering, Bandung, Indonesia 395–398. https://doi.org/10.1109/ICICI-BME.2011.6108634.

  35. Prosperini L, Pozzilli C (2013) The clinical relevance of force platform measures in multiple sclerosis: a review. Mult Scler Int 2013:756564

  36. Zhou H et al (2018) Hemodialysis impact on motor function beyond aging and diabetes—objectively assessing gait and balance by wearable technology. Sensors 18(11):3939

  37. Stanley WJ et al (2020) Cost of cerebellar ataxia in Hong Kong: a retrospective cost-of-illness analysis. Front Neurol 11:711

  38. Brouillette AM, Öz G, Gomez CM (2015) Cerebrospinal fluid biomarkers in spinocerebellar ataxia: a pilot study. Dis Markers 2015:413098

  39. Curtze C, Nutt JG, Carlson-Kuhta P, Mancini M, Horak FB (2016) Objective gait and balance impairments relate to balance confidence and perceived mobility in people with Parkinson disease. Phys Ther 96(11):1734–1743

    Article  Google Scholar 

  40. Terayama K, Sakakibara R, Ogawa A (2018) Wearable gait sensors to measure ataxia due to spinocerebellar degeneration. Neurol Clin Neurosci 6(1):9–12. https://doi.org/10.1111/ncn3.12174

    Article  Google Scholar 

  41. Nguyen H, Lebel K, Bogard S, Goubault E, Boissy P, Duval C (2018) Using inertial sensors to automatically detect and segment activities of daily living in people with Parkinson’s disease. IEEE Trans Neural Syst Rehabil Eng 26(1):197–204. https://doi.org/10.1109/TNSRE.2017.2745418

    Article  PubMed  Google Scholar 

  42. Goubault E et al (2018) Cardinal motor features of Parkinson’s disease coexist with peak-dose choreic-type drug-induced dyskinesia. J Parkinsons Dis 8(2):323–331. https://doi.org/10.3233/JPD-181312

    Article  PubMed  PubMed Central  Google Scholar 

  43. Adams JL et al (2017) Multiple wearable sensors in Parkinson and Huntington disease individuals: a pilot study in clinic and at home. Digit Biomark 1(1):52–63. https://doi.org/10.1159/000479018

    Article  PubMed  PubMed Central  Google Scholar 

  44. Thiede R, Toosizadeh N, Mills JL, Zaky M, Mohler J, Najafi B (2016) Gait and balance assessments as early indicators of frailty in patients with known peripheral artery disease. Clin Biomech 32:1–7

    Article  Google Scholar 

  45. Zhou H, Razjouyan J, Halder D, Naik AD, Kunik ME, Najafi B (2019) Instrumented trail-making task: application of wearable sensor to determine physical frailty phenotypes. Gerontology 65(2):186–197

    Article  Google Scholar 

  46. Zahiri M et al (2019) Using wearables to screen motor performance deterioration because of cancer and chemotherapy-induced peripheral neuropathy (CIPN) in adults - toward an early diagnosis of CIPN. J Geriatr Oncol 10(6):960–967. https://doi.org/10.1016/j.jgo.2019.01.010

    Article  PubMed  PubMed Central  Google Scholar 

  47. Ashley M., Brouillette Gülin, Öz Christopher M., Gomez (2015) Cerebrospinal Fluid Biomarkers in Spinocerebellar Ataxia: A Pilot Study. Disease Markers 20151-6 10.1155/2015/413098

Download references

Acknowledgements

The authors express their appreciation to Drs. Bob Dagher, MD, and Joseph T. Gwin, PhD, for providing insightful suggestions and comments related to the study design and protocol. The authors also express their appreciation to Dr. Anne-Marie Wills, MD, for providing feedback and comments related to the manuscript, and Manuel Gardea for assistance in data collection.

Funding

This study was funded by the Cadent Therapeutics, Inc.

Author information

Authors and Affiliations

  1. BioSensics LLC, Newton, MA, USA

    He Zhou, Hung Nguyen, Ana Enriquez, Louie Morsy & Ashkan Vaziri

  2. Cadent Therapeutics, Cambridge, MA, USA

    Michael Curtis, Timothy Piser & Christopher Kenney

  3. Ataxia Center, Department of Neurology, Massachusetts General Hospital, Boston, MA, USA

    Christopher D. Stephen, Anoopum S. Gupta & Jeremy D. Schmahmann

Authors
  1. He Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hung Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ana Enriquez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Louie Morsy
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michael Curtis
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Timothy Piser
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Christopher Kenney
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Christopher D. Stephen
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Anoopum S. Gupta
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jeremy D. Schmahmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Ashkan Vaziri
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

HZ performed statistical analysis of the data, helped with the interpretation of the results, and contributed to the drafting of the manuscript. HN processed the data, assisted in the interpretation of the results, helped with the statistical analysis of the results, and contributed to the drafting the manuscript; AE contributed to the data acquisition and assisted in the drafting of the manuscript; LM contributed to data acquisition and assisted in the drafting of the manuscript; MC assisted in the interpretation of the results and contributed to the drafting of the manuscript; TP contributed to the design and conceptualization the study, assisted in the interpretation of the results, and contributed to the drafting of the manuscript; CK assisted in the interpretation of the results and contributed to drafting the manuscript; CS provided expert clinical rating of ataxia, contributed to the interpretation of the results, and assisted in the drafting the manuscript; AG provided expert clinical rating of ataxia, assisted in the interpretation of the results, and contributed to drafting the manuscript; JS contributed to the design and conceptualization the study, managed the recruitment of the study, provided expert clinical rating of ataxia, assisted in the interpretation of the results, and contributed to drafting the manuscript; AV helped with the design and conceptualization the study, assisted in the interpretation of the results, and contributed to drafting the manuscript.

Corresponding author

Correspondence to Hung Nguyen.

Ethics declarations

Ethic approval

This study was approved by the Partners HealthCare System Institutional Review Board and written informed consent was obtained from all participants.

Consent to participate

Informed written consent was obtained for all participants to participate in the study.

Consent for publication

Informed written consent was obtained for all participants that results from the study will be used for publication; however, their data will be anonymized.

Conflict of interest

This study was sponsored by Cadent Therapeutics in collaboration with BioSensics and the Ataxia Center at Massachusetts General Hospital. The sensors used in the study were developed and commercialized by BioSensics. H. Zhou was a Senior Research Scientist at BioSensics. H. Nguyen is currently a Principal Research Scientist at BioSensics. A. Enrique is currently a Senior Clinical Operations Manager at BioSensics. L. Morsy is currently a Senior Clinical Operations Manager at BioSensics. M. Curtis was the President and Head of R&D at Cadent Therapeutics. T. Piser is currently the Chief Scientific Officer at Cadent Therapeutics. C. Kenney is currently the Chief Medical Officer at Cadent Therapeutics. C. Stephen has provided scientific advisory for Xenon Pharmaceuticals and SwanBio Pharma and received research funding from Sanofi-Genzyme for a study of video oculography in late-onset GM2 gangliosidosis. He has received financial support from Sanofi-Genzyme, Biogen, and Biohaven for the conduct of clinical trials. A.Gupta has received research funding from Biogen and consults for Biogen, Triplet Therapeutics, and Remix Therapeutics. J. Schmahmann is site Principal Investigator for Biohaven clinical trials NCT03701399, NCT02960893, and NCT03952806. He consults for Biogen, Bayer, and Cadent Therapeutics, and is the author of the BARS and BARS2 which are copyrighted by the General Hospital Corporation. A.Vaziri is the Founder and Chief Executive Officer of BioSensics.

Additional information

Publisher's note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PNG 627 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhou, H., Nguyen, H., Enriquez, A. et al. Assessment of gait and balance impairment in people with spinocerebellar ataxia using wearable sensors. Neurol Sci 43, 2589–2599 (2022). https://doi.org/10.1007/s10072-021-05657-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10072-021-05657-6

Keywords

Search

Navigation