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Digital measures of freezing of gait across the spectrum of normal, non-freezers, possible freezers and definite freezers

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Abstract

Over the course of the disease, freezing of gait (FoG) will gradually impact over 80% of people with Parkinson’s disease (PD). Clinical decision-making and research design are often based on classification of patients as ‘freezers’ or ‘non-freezers’. We derived an objective measure of FoG severity from inertial sensors on the legs to examine the continuum of FoG from absent to possible and severe in people with PD and in healthy controls. One hundred and forty-seven people with PD (Off-medication) and 83 healthy control subjects turned 360° in-place for 1 minute while wearing three wearable sensors used to calculate a novel Freezing Index. People with PD were classified as: ‘definite freezers’, new FoG questionnaire (NFOGQ) score > 0 and clinically observed FoG; ‘non-freezers’, NFOGQ = 0 and no clinically observed FoG; and ‘possible freezers’, either NFOGQ > 0 but no FoG observed or NFOGQ = 0 but FoG observed. Linear mixed models were used to investigate differences in participant characteristics among groups. The Freezing Index significantly increased from healthy controls to non-freezers to possible freezers and to definite freezers and showed, in average, excellent test–retest reliability (ICC = 0.89). Unlike the Freezing Index, sway, gait and turning impairments were similar across non-freezers, possible and definite freezers. The Freezing Index was significantly related to NFOG-Q, disease duration, severity, balance confidence, and the SCOPA-Cog (p < 0.01). An increase in the Freezing Index, objectively assessed with wearable sensors during a turning- in-place test, may help identify prodromal FoG in people with PD prior to clinically-observable or patient-perceived freezing. Future work should follow objective measures of FoG longitudinally.

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Data availability

All data contained within this study is available upon reasonable request from the corresponding author.

References

  1. Nutt JG et al (2011) Freezing of gait: moving forward on a mysterious clinical phenomenon. Lancet Neurol 10(8):734–744. https://doi.org/10.1016/S1474-4422(11)70143-0

    Article  PubMed  PubMed Central  Google Scholar 

  2. Snijders AH et al (2008) Clinimetrics of freezing of gait. Mov Disord 23(Suppl 2):S468–S474. https://doi.org/10.1002/mds.22144

    Article  PubMed  Google Scholar 

  3. Schaafsma JD et al (2003) Characterization of freezing of gait subtypes and the response of each to levodopa in Parkinson’s disease. Eur J Neurol 10(4):391–398

    Article  CAS  PubMed  Google Scholar 

  4. Lewis S et al (2022) Stepping up to meet the challenge of freezing of gait in Parkinson’s disease. Transl Neurodegen 11(1):23. https://doi.org/10.1186/s40035-022-00298-x

    Article  Google Scholar 

  5. Bloem BR et al (2004). Falls and freezing of gait in Parkinson's disease: a review of two interconnected, episodic phenomena [Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S. Review]. Mov Disord 19(8):871–84. https://doi.org/10.1002/mds.20115

  6. Moore ST, MacDougall HG, Ondo WG (2008) Ambulatory monitoring of freezing of gait in Parkinson's disease [Research Support, U.S. Gov't, Non-P.H.S.]. J Neurosci Methods 167(2):340–348. https://doi.org/10.1016/j.jneumeth.2007.08.023

  7. Hausdorff JM, Balash Y, Giladi N (2003) Time series analysis of leg movements during freezing of gait in Parkinson’s disease: akinesia, rhyme or reason? Phys A Stat Mech Appl 321(3):565–570. https://doi.org/10.1016/S0378-4371(02)01744-2

    Article  Google Scholar 

  8. Delval A et al (2010) Objective detection of subtle freezing of gait episodes in Parkinson's disease [Research Support, Non-U.S. Gov't]. Mov Disord 25(11):1684–1693. https://doi.org/10.1002/mds.23159

  9. Zach H et al (2015) Identifying freezing of gait in Parkinson’s disease during freezing provoking tasks using waist-mounted accelerometry. Parkinson Relat Disord 21(11):1362–1366. https://doi.org/10.1016/j.parkreldis.2015.09.051

    Article  Google Scholar 

  10. Jacobs JV et al (2009) Knee trembling during freezing of gait represents multiple anticipatory postural adjustments [Research Support, N.I.H., Extramural]. Exp Neurol 215(2):334–341. https://doi.org/10.1016/j.expneurol.2008.10.019

  11. Welch PD (1967) The use of fast fourier transform for the estimation of power spectra: a method based on time averaging over short, modified periodograms. IEEE Trans Audio Electroacoust AU-15:70–73

  12. Mancini M et al (2017) The clinical significance of freezing while turning in Parkinson’s disease. Neuroscience 343:222–228. https://doi.org/10.1016/j.neuroscience.2016.11.045

    Article  CAS  PubMed  Google Scholar 

  13. D’Cruz N et al (2022) Dual task turning in place: a reliable, valid, and responsive outcome measure of freezing of gait. Mov Disord 37(2):269–278. https://doi.org/10.1002/mds.28887

    Article  PubMed  Google Scholar 

  14. Hughes AJ et al (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55(3):181–184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Goetz CG et al (2008) Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord 23(15):2129–2170. https://doi.org/10.1002/mds.22340

    Article  PubMed  Google Scholar 

  16. Marinus J et al (2003) Assessment of cognition in Parkinson’s disease. Neurology 61(9):1222–1228. https://doi.org/10.1212/01.Wnl.0000091864.39702.1c

    Article  CAS  PubMed  Google Scholar 

  17. Nasreddine ZS et al (2005) The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 53(4):695–699. https://doi.org/10.1111/j.1532-5415.2005.53221.x

    Article  PubMed  Google Scholar 

  18. Nieuwboer A et al (2009) Reliability of the new freezing of gait questionnaire: agreement between patients with Parkinson’s disease and their carers. Gait Posture 30(4):459–463. https://doi.org/10.1016/j.gaitpost.2009.07.108

    Article  PubMed  Google Scholar 

  19. Powell LE, Myers AM (1995) The Activities-specific Balance Confidence (ABC) Scale. J Gerontol A Biol Sci Med Sci 50A(1):M28-34

    Article  CAS  PubMed  Google Scholar 

  20. Jenkinson C et al (1997) The Parkinson’s Disease Questionnaire (PDQ-39): development and validation of a Parkinson’s disease summary index score. Age Ageing 26(5):353–357

    Article  CAS  PubMed  Google Scholar 

  21. Snijders AH et al (2012) Freezer or non-freezer: clinical assessment of freezing of gait. Parkinson Relat Disord 18(2):149–154. https://doi.org/10.1016/j.parkreldis.2011.09.006

    Article  Google Scholar 

  22. Jung SH et al (2020) Effects of the agility boot camp with cognitive challenge (ABC-C) exercise program for Parkinson’s disease. NPJ Parkinsons Dis 6(1):31. https://doi.org/10.1038/s41531-020-00132-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. King LA et al (2020) Cognitively challenging agility boot camp program for freezing of gait in Parkinson disease. Neurorehabil Neural Repair 34(5):417–427. https://doi.org/10.1177/1545968320909331

    Article  PubMed  PubMed Central  Google Scholar 

  24. Morris R et al (2020) Cognitive function in people with and without freezing of gait in Parkinson’s disease. NPJ Parkinsons Dis 6:9. https://doi.org/10.1038/s41531-020-0111-7

    Article  PubMed  PubMed Central  Google Scholar 

  25. Peterson DS et al (2020) Relating Parkinson freezing and balance domains: a structural equation modeling approach. Parkinson Relat Disord 79:73–78. https://doi.org/10.1016/j.parkreldis.2020.08.027

    Article  Google Scholar 

  26. El-Gohary M et al (2013) Continuous monitoring of turning in patients with movement disability. Sensors (Basel) 14(1):356–369. https://doi.org/10.3390/s140100356

    Article  PubMed  Google Scholar 

  27. Hasegawa N et al (2019) How to select balance measures sensitive to parkinson’s disease from body-worn inertial sensors-separating the trees from the forest. Sensors (Basel). https://doi.org/10.3390/s19153320

    Article  PubMed  Google Scholar 

  28. Glickman ME, Rao SR, Schultz MR (2014) False discovery rate control is a recommended alternative to Bonferroni-type adjustments in health studies. J Clin Epidemiol 67(8):850–857. https://doi.org/10.1016/j.jclinepi.2014.03.012

    Article  PubMed  Google Scholar 

  29. Washabaugh EP et al (2017) Validity and repeatability of inertial measurement units for measuring gait parameters. Gait Posture 55:87–93. https://doi.org/10.1016/j.gaitpost.2017.04.013

    Article  PubMed  PubMed Central  Google Scholar 

  30. Giladi N et al (2001) Freezing of gait in PD: prospective assessment in the DATATOP cohort. Neurology 56(12):1712–1721. https://doi.org/10.1212/wnl.56.12.1712

    Article  CAS  PubMed  Google Scholar 

  31. Bartels AL et al (2003) Relationship between freezing of gait (FOG) and other features of Parkinson’s: FOG is not correlated with bradykinesia. J Clin Neurosci 10(5):584–588. https://doi.org/10.1016/s0967-5868(03)00192-9

    Article  CAS  PubMed  Google Scholar 

  32. Amboni M et al (2008) Freezing of gait and executive functions in patients with Parkinson’s disease. Mov Disord 23(3):395–400. https://doi.org/10.1002/mds.21850

    Article  PubMed  Google Scholar 

  33. Bekkers EMJ et al (2018) Balancing between the two: are freezing of gait and postural instability in Parkinson’s disease connected? Neurosci Biobehav Rev 94:113–125. https://doi.org/10.1016/j.neubiorev.2018.08.008

    Article  CAS  PubMed  Google Scholar 

  34. 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. https://doi.org/10.1155/2012/459321

    Article  Google Scholar 

  35. Giladi N et al (2001) Freezing of gait in patients with advanced Parkinson’s disease. J Neural Transm (Vienna) 108(1):53–61. https://doi.org/10.1007/s007020170096

    Article  CAS  PubMed  Google Scholar 

  36. Macht M et al (2007) Predictors of freezing in Parkinson’s disease: a survey of 6,620 patients. Mov Disord 22(7):953–956. https://doi.org/10.1002/mds.21458

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors thank all participants for generously donating their time to participate; Peter Fino, Carolin Curtze, Mike Fleming, Heather Schlueter, Peter Martin, and Graham Harker for helping with data collection; Katrijn Smulders for data collection and help with study procedures; and Edward King for helping with data collection and management. This research was funded by the National Institutes of Health under award numbers R00 HD078492 (Mancini), R01AG006457 (Horak), and Department of Veterans Affairs Merit award number 5I01RX001075 (Horak).

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Authors and Affiliations

  1. Balance Disorders Laboratory, Department of Neurology, Oregon Health and Science University, 3181 SW Sam Jackson Road, OP-32, Portland, OR, 97239, USA

    Martina Mancini, Naoya Hasegawa, Fay B. Horak & John G. Nutt

  2. Department of Rehabilitation Science, Hokkaido University, Sapporo, Japan

    Naoya Hasegawa

  3. College of Health Solutions, Arizona State University, Phoenix, AZ, USA

    Daniel S. Peterson

Authors
  1. Martina Mancini
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  2. Naoya Hasegawa
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  3. Daniel S. Peterson
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  4. Fay B. Horak
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  5. John G. Nutt
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Contributions

MM: conceptualization of the study, obtained funding, data analysis, drafting, and editing of the manuscript. NH: data analysis and editing of the manuscript. DSP: conceptualization of the study and editing of the manuscript. FH: conceptualization of the study, obtained funding, and editing of the manuscript. JGN: conceptualization of the study and editing of the manuscript. All authors contributed to the article and approved the submitted version.

Corresponding author

Correspondence to Martina Mancini.

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Conflicts of interest

FH has an equity interest in APDM Wearable Technologies, a Clario company, that may have a commercial interest in the results of this study. This potential conflict of interest has been reviewed and managed by the Research and Development Committee at the Oregon Health & Science University. They have put in place a plan to help ensure that this research study is not affected by the financial interest. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Ethical standard

This work was approved by the joint Oregon Health & Science University (OHSU) and Veterans Affairs Portland Health Care System (VAPORHCS) institutional review board ethics committees.

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Each participant provided written informed consent.

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Mancini, M., Hasegawa, N., Peterson, D.S. et al. Digital measures of freezing of gait across the spectrum of normal, non-freezers, possible freezers and definite freezers. J Neurol 270, 4309–4317 (2023). https://doi.org/10.1007/s00415-023-11773-4

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