Identification of Characteristic Motor Patterns Preceding Freezing of Gait in Parkinson's Disease Using Wearable Sensors

Luca Palmerini, Laura Rocchi, Sinziana Mazilu, Eran Gazit, Jeffrey M Hausdorff, Lorenzo Chiari, Luca Palmerini, Laura Rocchi, Sinziana Mazilu, Eran Gazit, Jeffrey M Hausdorff, Lorenzo Chiari

Abstract

Freezing of gait (FOG) is a disabling symptom that is common among patients with advanced Parkinson's disease (PD). External cues such as rhythmic auditory stimulation can help PD patients experiencing freezing to resume walking. Wearable systems for automatic freezing detection have been recently developed. However, these systems detect a FOG episode after it has happened. Instead, in this study, a new approach for the prediction of FOG (before it actually happens) is presented. Prediction of FOG might enable preventive cueing, reducing the likelihood that FOG will occur. Moreover, understanding the causes and circumstances of FOG is still an open research problem. Hence, a quantitative characterization of movement patterns just before FOG (the pre-FOG phase) is of great importance. In this study, wearable inertial sensors were used to identify and quantify the characteristics of gait during the pre-FOG phase and compare them with the characteristics of gait that do not precede FOG. The hypothesis of this study is based on the threshold-based model of FOG, which suggests that before FOG occurs, there is a degradation of the gait pattern. Eleven PD subjects were analyzed. Six features extracted from movement signals recorded by inertial sensors showed significant differences between gait and pre-FOG. A classification algorithm was developed in order to test if it is feasible to predict FOG (i.e., detect it before it happens). The aim of the classification procedure was to identify the pre-FOG phase. Results confirm that there is a degradation of gait occurring before freezing. Results also provide preliminary evidence on the feasibility of creating an automatic algorithm to predict FOG. Although some limitations are present, this study shows promising findings for characterizing and identifying pre-FOG patterns, another step toward a better understanding, prediction, and prevention of this disabling symptom.

Keywords: Parkinson’s disease; classification; data analysis; freezing of gait; inertial measurement unit; machine learning; prediction; wearable sensors.

Figures

Figure 1
Figure 1
Setup that was considered for the analysis.
Figure 2
Figure 2
Workflow of data processing.
Figure 3
Figure 3
An example of the segmentation of the recorded signal in gait and pre-FOG windows. The first plot from the top shows the recorded angular velocities of the sensors on the left and right ankles together with the segmentation of the windows. The second plot is the norm of the angular velocity of the sensors on the left and right ankles. The third plot is the norm of the acceleration of the sensor on the lower back. These two norms are used to perform the check for sufficient motion in a window.
Figure 4
Figure 4
Paired t-test results for each feature. For each feature, two plots are present. On the left the mean and SD values are reported, together with corresponding p-value and statistical significance (*). On the right, the values of each pair that was considered in the statistical testing are reported.
Figure 5
Figure 5
An example of the application of the classifier. The first plot from the top shows the recorded angular velocities of the left and right ankles together with the segmentation of the windows, as in Figure 3. The second plot reports the probability of incoming FOG, as predicted by the classifier. This probability is computed for each gait and pre-FOG window. The threshold on probability is also reported: if the probability is higher than the threshold, then the classifier predicts a FOG (i.e., it identifies the window as pre-FOG), otherwise, the classifier identifies the window as gait. In the last three plots, the values of the three features which are used in the classifier are reported.

References

    1. Nutt JG, Bloem BR, Giladi N, Hallett M, Horak FB, Nieuwboer A. Freezing of gait: moving forward on a mysterious clinical phenomenon. Lancet Neurol (2011) 10(8):734–44.10.1016/S1474-4422(11)70143-0
    1. Bloem BR, Hausdorff JM, Visser JE, Giladi N. Falls and freezing of gait in Parkinson’s disease: a review of two interconnected, episodic phenomena. Mov Disord (2004) 19(8):871–84.10.1002/mds.20115
    1. Okuma Y. Freezing of gait in Parkinson’s disease. J Neurol (2006) 253(Suppl):VII27–32.10.1007/s00415-006-7007-2
    1. Silva de Lima AL, Evers LJW, Hahn T, Bataille L, Hamilton JL, Little MA, et al. Freezing of gait and fall detection in Parkinson’s disease using wearable sensors: a systematic review. J Neurol (2017) 264(8):1642–54.10.1007/s00415-017-8424-0
    1. Nonnekes J, Snijders AH, Nutt JG, Deuschl G, Giladi N, Bloem BR. Freezing of gait: a practical approach to management. Lancet Neurol (2015) 14(7):768–78.10.1016/S1474-4422(15)00041-1
    1. Rodríguez-Martín D, Samà A, Pérez-López C, Català A, Moreno Arostegui JM, Cabestany J, et al. Home detection of freezing of gait using support vector machines through a single waist-worn triaxial accelerometer. PLoS One (2017) 12(2):e0171764.10.1371/journal.pone.0171764
    1. Hausdorff JM, Balash Y, Giladi N. Time series analysis of leg movements during freezing of gait in Parkinson’s disease: akinesia, rhyme or reason? Phys A Stat Mech Appl (2003) 321(3–4):565–70.10.1016/S0378-4371(02)01744-2
    1. Bächlin M, Plotnik M, Roggen D, Maidan I, Hausdorff JM, Giladi N, et al. Wearable assistant for Parkinson’s disease patients with the freezing of gait symptom. IEEE Trans Inf Technol Biomed (2010) 14(2):436–46.10.1109/TITB.2009.2036165
    1. Tripoliti EE, Tzallas AT, Tsipouras MG, Rigas G, Bougia P, Leontiou M, et al. Automatic detection of freezing of gait events in patients with Parkinson’s disease. Comput Methods Programs Biomed (2013) 110(1):12–26.10.1016/j.cmpb.2012.10.016
    1. Mancini M, Smulders K, Cohen RG, Horak FB, Giladi N, Nutt JG. The clinical significance of freezing while turning in Parkinson’s disease. Neuroscience (2017) 343:222–8.10.1016/j.neuroscience.2016.11.045
    1. Pepa L, Ciabattoni L, Verdini F, Capecci M, Ceravolo MG. Smartphone based Fuzzy Logic freezing of gait detection in Parkinson’s Disease. 2014 IEEE/ASME 10th International Conference on Mechatronic and Embedded Systems and Applications (MESA) Ancona, Italy: IEEE (2014). p. 1–6.
    1. Coste CA, Sijobert B, Pissard-Gibollet R, Pasquier M, Espiau B, Geny C. Detection of freezing of gait in Parkinson disease: preliminary results. Sensors (Basel) (2014) 14(4):6819–27.10.3390/s140406819
    1. Rezvanian S, Lockhart T. Towards real-time detection of freezing of gait using wavelet transform on wireless accelerometer data. Sensors (Basel) (2016) 16(4):475.10.3390/s16040475
    1. Moore ST, MacDougall HG, Ondo WG. Ambulatory monitoring of freezing of gait in Parkinson’s disease. J Neurosci Methods (2008) 167(2):340–8.10.1016/j.jneumeth.2007.08.023
    1. Moore ST, Yungher DA, Morris TR, Dilda V, MacDougall HG, Shine JM, et al. Autonomous identification of freezing of gait in Parkinson’s disease from lower-body segmental accelerometry. J Neuroeng Rehabil (2013) 10(1):19.10.1186/1743-0003-10-19
    1. Maidan I, Bernad-Elazari H, Gazit E, Giladi N, Hausdorff JM, Mirelman A. Changes in oxygenated hemoglobin link freezing of gait to frontal activation in patients with Parkinson disease: an fNIRS study of transient motor-cognitive failures. J Neurol (2015) 262(4):899–908.10.1007/s00415-015-7650-6
    1. Maidan I, Plotnik M, Mirelman A, Weiss A, Giladi N, Hausdorff JM. Heart rate changes during freezing of gait in patients with Parkinson’s disease. Mov Disord (2010) 25(14):2346–54.10.1002/mds.23280
    1. Brugger F, Abela E, Hägele-Link S, Bohlhalter S, Galovic M, Kägi G. Do executive dysfunction and freezing of gait in Parkinson’s disease share the same neuroanatomical correlates? J Neurol Sci (2015) 356(1–2):184–7.10.1016/j.jns.2015.06.046
    1. Rubino A, Assogna F, Piras F, Di Battista ME, Imperiale F, Chiapponi C, et al. Does a volume reduction of the parietal lobe contribute to freezing of gait in Parkinson’s disease? Parkinsonism Relat Disord (2014) 20(10):1101–3.10.1016/j.parkreldis.2014.07.002
    1. Teramoto H, Morita A, Ninomiya S, Shiota H, Kamei S. Relation between freezing of gait and frontal function in Parkinson’s disease. Parkinsonism Relat Disord (2014) 20(10):1046–9.10.1016/j.parkreldis.2014.06.022
    1. Vercruysse S, Spildooren J, Heremans E, Wenderoth N, Swinnen SP, Vandenberghe W, et al. The neural correlates of upper limb motor blocks in Parkinson’s disease and their relation to freezing of gait. Cereb Cortex (2014) 24(12):3154–66.10.1093/cercor/bht170
    1. Nieuwboer A, Giladi N. Characterizing freezing of gait in Parkinson’s disease: models of an episodic phenomenon. Mov Disord (2013) 28(11):1509–19.10.1002/mds.25683
    1. Plotnik M, Giladi N, Hausdorff JM. Is freezing of gait in Parkinson’s disease a result of multiple gait impairments? Implications for treatment. Parkinsons Dis (2012) 2012:459321.10.1155/2012/459321
    1. Bhatt H, Pieruccini-Faria F, Almeida QJ. Dynamics of turning sharpness influences freezing of gait in Parkinson’s disease. Parkinsonism Relat Disord (2013) 19(2):181–5.10.1016/j.parkreldis.2012.09.006
    1. Schaafsma JD, Balash Y, Gurevich T, Bartels AL, Hausdorff JM, Giladi N. Characterization of freezing of gait subtypes and the response of each to levodopa in Parkinson’s disease. Eur J Neurol (2003) 10(4):391–8.10.1046/j.1468-1331.2003.00611.x
    1. Nieuwboer A, Dom R, De Weerdt W, Desloovere K, Fieuws S, Broens-Kaucsik E. Abnormalities of the spatiotemporal characteristics of gait at the onset of freezing in Parkinson’s disease. Mov Disord (2001) 16(6):1066–75.10.1002/mds.1206
    1. Bengevoord A, Vervoort G, Spildooren J, Heremans E, Vandenberghe W, Bloem BR, et al. Center of mass trajectories during turning in patients with Parkinson’s disease with and without freezing of gait. Gait Posture (2016) 43:54–9.10.1016/j.gaitpost.2015.10.021
    1. Nieuwboer A, Dom R, De Weerdt W, Desloovere K, Janssens L, Stijn V. Electromyographic profiles of gait prior to onset of freezing episodes in patients with Parkinson’s disease. Brain (2004) 127(Pt 7):1650–60.10.1093/brain/awh189
    1. Shine JM, Handojoseno AMA, Nguyen TN, Tran Y, Naismith SL, Nguyen H, et al. Abnormal patterns of theta frequency oscillations during the temporal evolution of freezing of gait in Parkinson’s disease. Clin Neurophysiol (2014) 125(3):569–76.10.1016/j.clinph.2013.09.006
    1. Mazilu S, Calatroni A, Gazit E, Mirelman A, Hausdorff JM, Tröster G. Prediction of freezing of gait in Parkinson’s from physiological wearables: an exploratory study. IEEE J Biomed Heal Inf (2015) 19:1843–54.10.1109/JBHI.2015.2465134
    1. Mazilu S, Calatroni A, Gazit E, Roggen D, Hausdorff JM, Tröster G. Feature learning for detection and prediction of freezing of gait in Parkinson’s disease. In: Perner P, editor. Machine Learning and Data Mining in Pattern Recognition, 9th International Conference, MLDM 2013, Proceedings; 2013 July 19–25; New York, NY, USA. Berlin, Heidelberg: Springer (2013). p. 144–58. (Lecture Notes in Computer Science; vol. 7988).
    1. Ferster ML, Mazilu S, Tröster G. Gait parameters change prior to freezing in Parkinson’s disease: a data-driven study with wearable inertial units. Proceedings of the 10th EAI International Conference on Body Area Networks Sydney, Australia: ICST (2015). p. 159–66.
    1. Goetz CG, Fahn S, Martinez-Martin P, Poewe W, Sampaio C, Stebbins GT, et al. Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): process, format, and clinimetric testing plan. Mov Disord (2007) 22(1):41–7.10.1002/mds.21198
    1. Nieuwboer A, Rochester L, Herman T, Vandenberghe W, Emil GE, Thomaes T, et al. Reliability of the new freezing of gait questionnaire: agreement between patients with Parkinson’s disease and their carers. Gait Posture (2009) 30(4):459–63.10.1016/j.gaitpost.2009.07.108
    1. Harms H, Amft O, Winkler R, Schumm J, Kusserow M, Troester G. ETHOS: miniature orientation sensor for wearable human motion analysis. 2010 IEEE Sensors Hawaii, USA: IEEE (2010). p. 1037–42.
    1. Nieuwboer A, Chavret F, Willems AM, Desloovere K. Does freezing in Parkinson’s disease change limb coordination? A kinematic analysis. J Neurol (2007) 254(9):1268–77.10.1007/s00415-006-0514-3
    1. 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(5):656–63.10.1002/ana.20452
    1. Benjamini Y, Yekutieli D. The control of the false discovery rate in multiple testing under dependency. Ann Stat (2001) 29:1165–88.10.1214/aos/1013699998
    1. Krzanowski WJ. Principles of Multivariate Analysis: A User’s Perspective. Oxford: Oxford University Press; (1988). 563 p.
    1. Youden WJ. Index for rating diagnostic tests. Cancer (1950) 3(1):32–5.10.1002/1097-0142(1950)3:1<32::AID-CNCR2820030106>;2-3
    1. Plotnik M, Giladi N, Hausdorff JM. Bilateral coordination of walking and freezing of gait in Parkinson’s disease. Eur J Neurosci (2008) 27(8):1999–2006.10.1111/j.1460-9568.2008.06167.x
    1. Weiss A, Herman T, Giladi N, Hausdorff JM. New evidence for gait abnormalities among Parkinson’s disease patients who suffer from freezing of gait: insights using a body-fixed sensor worn for 3 days. J Neural Transm (2015) 122:403–10.10.1007/s00702-014-1279-y
    1. Barthel C, Mallia E, Debû B, Bloem BR, Ferraye MU. The practicalities of assessing freezing of gait. J Parkinsons Dis (2016) 6(4):667–74.10.3233/JPD-160927
    1. Ziegler K, Schroeteler F, Ceballos-Baumann AO, Fietzek UM. A new rating instrument to assess festination and freezing gait in Parkinsonian patients. Mov Disord (2010) 25(8):1012–8.10.1002/mds.22993
    1. El-Gohary M, Pearson S, McNames J, Mancini M, Horak F, Mellone S, et al. Continuous monitoring of turning in patients with movement disability. Sensors (Basel) (2013) 14(1):356–69.10.3390/s140100356

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