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Article

Parkinson’s Disease Wearable Gait Analysis: Kinematic and Dynamic Markers for Diagnosis

by
Lazzaro di Biase
1,2,3,*,
Luigi Raiano
4,
Maria Letizia Caminiti
1,2,
Pasquale Maria Pecoraro
1,2 and
Vincenzo Di Lazzaro
1,2
1
Research Unit of Neurology, Neurophysiology and Neurobiology, Department of Medicine and Surgery, Università Campus Bio-Medico di Roma, Via Alvaro del Portillo 21, 00128 Roma, Italy
2
Operative Research Unit of Neurology, Fondazione Policlinico Universitario Campus Bio-Medico, Via Alvaro del Portillo 200, 00128 Rome, Italy
3
Brain Innovations Lab, Università Campus Bio-Medico di Roma, Via Álvaro del Portillo 21, 00128 Rome, Italy
4
NeXT: Neurophysiology and Neuroengineering of Human-Technology Interaction Research Unit, Campus Bio-Medico University, 00128 Rome, Italy
*
Author to whom correspondence should be addressed.
Sensors 2022, 22(22), 8773; https://doi.org/10.3390/s22228773
Submission received: 29 August 2022 / Revised: 2 November 2022 / Accepted: 7 November 2022 / Published: 13 November 2022

Abstract

:
Introduction: Gait features differ between Parkinson’s disease (PD) and healthy subjects (HS). Kinematic alterations of gait include reduced gait speed, swing time, and stride length between PD patients and HS. Stride time and swing time variability are increased in PD patients with respect to HS. Additionally, dynamic parameters of asymmetry of gait are significantly different among the two groups. The aim of the present study is to evaluate which kind of gait analysis (dynamic or kinematic) is more informative to discriminate PD and HS gait features. Methods: In the present study, we analyzed gait dynamic and kinematic features of 108 PD patients and 88 HS from four cohorts of two datasets. Results: Kinematic features showed statistically significant differences among PD patients and HS for gait speed and time Up and Go test and for selected kinematic dispersion indices (standard deviation and interquartile range of swing, stance, and double support time). Dynamic features did not show any statistically significant difference between PD patients and HS. Discussion: Despite kinematics features like acceleration being directly proportional to dynamic features like ground reaction force, the results of this study showed the so-called force/rhythm dichotomy since kinematic features were more informative than dynamic ones.

1. Introduction

Parkinson’s disease (PD) diagnosis and symptoms monitoring rely mainly on clinical evaluation of the cardinal motor symptoms (bradykinesia, rest tremor, and rigidity) [1,2]. To date, following the in vivo diagnostic criteria [3], the error rate is about 20% [4]. This is mainly due to the lack of objective biomarkers for the in vivo diagnosis of Parkinson’s disease.
Wearable motion sensors are a promising solution to objectively describe PD motor symptoms [5,6], like bradykinesia [7,8,9], rigidity [9,10,11,12], tremor [13,14,15,16], and axial symptoms like gait, balance, and postural issues [17,18,19,20,21]. In addition, the symptom identification process through motion sensors [22] could also improve the therapy management process [23]. Generally speaking, body motion can be analyzed from two different points of view: kinetics (dynamics) analysis, which takes into account the forces that generate the motion and their effect on the body. On the other hand, kinematic analysis, defined as the geometry of motion, describes the movement of the body in terms of position, time, velocity, acceleration, or angle of body segments (Figure 1) [21,24,25].
In literature, kinematic analysis in PD patients showed that the stride variability is increased, and the ability to maintain a steady gait rhythm and a stable, steady walking pattern with minimal stride-to-stride changes is impaired [26,27,28,29]. PD patients show decreased swing time and reduced stride length compared to controls and stride time, i.e., the gait cycle durations is increased with respect to control group but not significantly different, while stride-to-stride variability is increased significantly from the control group [30].
Increased stride variability has been associated with an increased fall risk in older adults in general, as well as in patients with PD [31,32,33], suggesting that this aspect of gait may have clinical utility as an aid in fall risk assessment.
On the dynamics analysis side, the features studied are the forces that cause the motion and their effect on gait. During the stance phase, where feet are in contact with the ground, a level of center of pressure (CoP) is applied the ground reaction force (GRF) which represents the results of gravity force and muscular activation forces counterbalanced by the contact with ground [21,24,25]. Gait dynamics studies have highlighted how some features of GRF vary in different phases of PD, while others are preserved. Components of the GRF are the peak-force at the heel-strike and at toe-off. In the novo early PD there is a delayed heel-strike and an earlier forefoot loading. These parameters seems to be altered independently from the stages of the disease or the pharmacotherapy, instead representing an early marker of the disease [34]. GRF measurement could also be useful to determine gait asymmetry. Su et al. [35] demonstrated how VGRF can reveal the asymmetry of gait by comparing the VGRF of both lower limbs between PD patients and healthy controls. Results showed that PD group has a higher degree of gait asymmetry of the GRF wavelet profile compared to healthy subjects [35]. This metric, compared to conventional asymmetry measures of kinematic features, like step time, stance time, double stance time, or dynamic features like the two peak and the one dep forces of GRF profile, all resulting with higher asymmetry compared to healthy subjects but with lower diagnostic accuracy [35].
The aim of the present study is to evaluate which kind of gait analysis (dynamic or kinematic) can be considered as more informative for discriminating PD and healthy subjects (HS) on the basis of gait features.

2. Materials and Methods

2.1. Subjects

For the present study, gait data were collected for a total of 108 PD patients and 88 HS from four cohorts [36,37,38] collected in two publicly available datasets [37,38] (Table 1).
For all the four cohorts, inclusion criteria for Parkinson’s disease patients were: idiopathic PD diagnosis, according to the UK Brain Bank criteria [39], and Hoehn and Yahr stage between 2 and 3 [40], a stable antiparkinsonian medication regimen, ability to ambulate independently, and absence of motor fluctuations. Control subjects were included if they did not have Parkinson’s disease or other common exclusion criteria for the Parkinson’s disease group: dementia, clinically significant musculo-skeletal disease, cardio-vascular disease, respiratory disease, other neurological disease, major depression, or uncorrected visual disturbances.
The first dataset (cohort 1 [36], 2 [37], 3 [30]) was composed of 93 PD patients and 72 HS, while the second dataset (cohort 4) [38] was composed of 15 PD patients and 16 HS. Regarding the demographic analysis cohorts 1, 2, and 3, the 72 HS are age-matched with PD patients. For cohort 4 the 16 HS are younger than PD patients, therefore, although mitigated by the 72 age-matched HS from the other cohorts, we need to take it into account as a possible bias of the study. For all the four cohorts, for both Parkinson’s disease patients and HS, gait-related data were collected through an instrumented force-sensitive insole [43] placed in subjects’ shoes, containing each eight pressure-sensitive sensors (Figure 2), thus allowing the experimenters to record the time series of the GRF while subjects were asked to walk on level ground. In the first and third cohort subjects walked for two minutes, in the second cohort for 100 m (around 80 s), and in the fourth cohort for 5 min. Considering that in each cohort PD and HS walked with the same protocol, and that around 10 m or 10 s of gait recording are sufficient to catch the gait pattern in PD and HS, the data available in the four cohorts are sufficient to describe the gait kinematic and dynamic. However, the inhomogeneity of gait duration protocol across cohorts should be considered as a limit of the present study.
All patients gave informed consent, and the study was approved by local research ethics committees in accordance with the Declaration of Helsinki.

2.2. Data Analysis

In the first dataset, only the gait dynamic data were available. Therefore, in order to analyze kinematic data, the recorded GRF signals were used to segment the single gait cycle periods for each patient.
According to Figure 3, the segmentation of the gait cycle was implemented using the differential Ground Reaction Force (GRF) ( δ ) between total right force and total left force:
δ = R f o o t , t o t L f o o t , t o t    
In (Equation (1)), R f o o t , t o t and L f o o t , t o t denote the sum of the forces (expressed in newton) measured by all the sensors embedded in the insole worn under the right foot and the left foot, respectively.
On the basis of δ , each gait cycle for each patient was selected between the first double limb support (DLS) and the left single limb support (SLS-L) (Figure 3).
For each cycle, we computed the following parameters related to the gait:
  • Right and Left Stance, expressed both in seconds and as percentage of the stride length;
  • Right and Left Swing, expressed both in seconds and as percentage of the stride length;
  • Double Limb Supports, expressed both in seconds and as percentage of the stride length
  • Right and Left Single Limb Supports, expressed both in seconds and as percentage of the stride length;
  • Right and Left Step Duration, expressed both in seconds and as percentage of the stride length;
  • Gait velocity expressed in m/s
  • Time up and go test expressed in seconds
Such parameters were then averaged along all cycles for each subject.
Moreover, in order to remove single cycle outliers, we compared the duration of each cycle (i.e., stride length) with the average duration ( S L ¯ ) computed for each subject. To this aim, we marked and then discarded all those cycles whose duration was higher then S L ¯ + 2 · S D ( S L ) , denoting with S D ( S L ) the standard deviation of the stride length of all cycles.
Considering the second dataset [38,39], two sources of data were available: raw data of the instrumented insoles (containing the whole gait dynamics) and the processed data already containing gait interval parameters (gait kinematics). Therefore, considering the second dataset, no further data manipulation was performed.
For the sake of simplicity, we summarized the main data manipulation steps performed with the two datasets in Table 2.

2.3. Dynamic Analysis

In order to estimate the force applied during the gait, we used the raw data of the instrumented insoles from both datasets. However, the data available within the second dataset were not calibrated, i.e., they were expressed in volts. Therefore, in order to compare the data between the two group of subjects, we divided the recorded signals by the maximal output of the electronic system composing the insole, according to [43]. This allowed us to obtain signals expressed in percentage of the maximal detectable force by the insole. For comparing the two groups (PD vs. HS), we computed the following central tendency and dispersion features: (1) mean, (2) standard deviation (SD), (3) median, (4) interquartile range (IQR). We computed such features along the whole trial duration, for each subject and each group, and we used t-test analysis to statistically test the difference between the two groups.

2.4. Kinematic Analysis

The following gait kinematic parameters were included in the analysis:
  • Right and Left Stance, expressed both in seconds and as percentage of the stride length;
  • Right and Left Swing, expressed both in seconds and as percentage of the stride length;
  • Double Limb Supports, expressed both in seconds and as percentage of the stride length;
  • Gait velocity expressed in m/s
  • Time up and go test expressed in seconds
Similar to the data analysis presented in Section 2.3 from the raw force data, we computed the following central tendency and dispersion features for the gait kinematics parameters: (1) average (ave), (2) standard deviation (SD), (3) median (med), (4) interquartile range (IQR). We computed such features along the whole trial duration for each subject and each group, and we used t-test analysis to statistically test the difference between the two groups.
For both kinematic and dynamic analysis, Bonferroni correction was applied, considering a correction factor of 50, deriving from the number of dynamic and kinematic parameters. Therefore, the statistically significant value (p) threshold is equal to 0.001 (0.05/50).

3. Results

3.1. Kinematic Analysis

Considering the central tendency indices related to Gait Speed and Time Up and Go test, t-tests showed a significant difference between HS and PD (p < 0.001) (Table 3, Figure 4), while all other kinematic central tendency indices t-test showed a non-significant difference in HS and PD (Table 2).
Moreover, t-tests showed a significant difference in HS and PD (p < 0.001) (Table 2, Figure 4) considering the dispersion indices computed for the following parameters:
-
Standard deviation (SD) left and right SWING absolute and percentage value
-
Standard deviation (SD) left and right STANCE percentage value
-
Standard deviation (SD) DOUBLE SUPPORT percentage value
-
Interquartile range (IQR) left and right SWING absolute and percentage value
-
Interquartile range (IQR) left and right STANCE absolute and percentage value
-
Interquartile range (IQR) DOUBLE SUPPORT percentage value
Conversely, for the other kinematic dispersion indices, t-test showed a non-significant difference between HS and PD (Table 2).

ROC Analysis

A ROC analysis was performed for all kinematic values which showed a significant t-test difference in HS and PD. It was implemented considering a diagnosis of PD over HS as the target (Figure 5). The value of AUC with upper and lower limits (95% C.I.), the standard error, and the p value are listed in Table 4.
As shown in Figure 5 and Table 4, with the exception of “IQR left STANCE”, and “IQR DOUBLE SUPPORT %”, all the kinematic predictors analysed showed a statistically significant ROC AUC value in the discrimination between diagnosis of PD over HS.

3.2. Dynamic Analysis

For all the dynamic central and dispersion indices, t-test showed a non-significant difference in HS and PD (p > 0.001) (Table 5).
In Figure 6 and Figure 7 (and Supplementary Video S1), the average gait cycle dynamic, respectively, in HS and PD groups are summarized, showing no difference in gait cycle dynamic profile in the two groups.

4. Discussion

Gait features differ between PD patients and HS under normal conditions. In this article we compared the kinematic and dynamic markers of gait between PD patients and HS. The statistical analyses related to the kinematic parameters showed significant differences among PD patients and HS for gait speed and time Up and Go test, and for selected kinematic dispersion indices, with statistically significant ROC AUC values indicating good discrimination ability between the two groups of these parameters. These results are in line with literature data showing an increased stride-to-stride variability in PD patients compared to HS [26,27,28,29,30]. This may reflect mechanisms that underline disease pathology, such as reduced automaticity and damaged locomotor synergies. Indeed, different studies showed that stride variability is reduced by levodopa therapy, demonstrating the role of dopaminergic pathways in the gait rhythmicity [27,28,44,45,46]. Moreover, increased gait variability could be a byproduct of bradykinesia and of a lower gait speed. In literature, no significant increase in stride time variability was observed in healthy elderly subjects, even though they walked significantly slower than young adults [47,48,49]. Several studies aimed to define the relationship between gait speed and stride time variability. Gait speed seems to be related to stride length, stride time, swing time, and stride time variability, with similar relationships in patients with PD and in controls. A U-shaped relationship between stride length variability and gait speed was described when healthy subjects walked on a treadmill [50]. Other studies observed a linear relationship between gait speed and stride time variability, and the range of walking speeds tested and differences in study populations may explain this apparent contradiction [51]. Indeed, mechanical and energy expenditure optimizations may be affected by aging and disease [52]. Interestingly, in a study of young and older adults, it was reported that gait speed did not affect the variability of walking velocity, stride length, or stride time [53]. The increased swing time variability in PD is apparently independent of gait speed. Furthermore, even when patients with PD walk at the same speed as controls, swing time variability is increased in PD [51].
In our study dynamic features did not show any statistically significant difference between PD patients and HS. The reason for the differences between kinematic and dynamic analysis, from which kinematic parameters seem to be more sensitive to identify PD patient features with respect to HS, could be found in the dynamic analysis technique. For dynamic analysis, GRF has several characteristics that make it suitable for gait study. Above all, the acceleration of the center of gravity of the body (COM) is directly proportional to the GRF, which implies that many gait features can be extracted from the GRF. GRF is a continuous signal, unlike kinematic parameters such as oscillation time or stride length, which are considered discrete variables. A great advantage of continuous signals is the possibility of being characterized in terms of time and frequency. However, to simplify the cost and complexity of instrumental devices, only the vertical component of the GRF (VGRF) is usually measured. VGRF is the component of the force with the greatest extent that the ground affects the body, and the majority of dynamic studies are focused on different characteristics of VGRF between patients with PD and controls [35,54]. The result of the present study compared to literature data on dynamic studies showed that to catch a difference between PD and HS a more deep dynamic analysis is necessary, like asymmetry between the two sides [35], or analysis not only of the global GRF but of the dynamics of the individual foot sensors sections (e.g., forefoot heel) [34].
The novelty of the present study is in the direct comparison of the two kinds of gait analysis (dynamic and kinematic). Despite kinematics features like acceleration that are directly proportional to dynamic features like ground reaction force, the results of this study showed the so-called force/rhythm dichotomy, since kinematic features were more informative than dynamic ones. In literature, the two kinds of analysis are very well described, with a lack of a direct comparison between the two on the same data. The limits of the present study, which are related to the source of data that comes from available datasets of previous studies, are the inhomogeneity of gait duration protocol across cohorts and the younger age of HS of cohort 4 with respect to other subjects. Therefore, future clinical trials are needed to confirm these results and additional approaches could be devoted to applying machine learning algorithms to more precisely assess and combine kinematics and dynamics parameters, and weigh the impact of single features.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/s22228773/s1, Video S1: Average gait cycle dynamic, in healthy subjects (HS) and Parkinson's disease (PD) group.

Author Contributions

Conceptualization, L.d.B., L.R. and V.D.L.; Data curation, L.d.B. and L.R.; Formal analysis, L.d.B. and L.R.; Methodology, L.d.B.; Supervision, V.D.L.; Writing—original draft, L.d.B., L.R., M.L.C. and P.M.P.; Writing—review & editing, L.d.B. and V.D.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

The studies of the dataset were conducted in accordance with the Declaration of Helsinki, and approved by the local Institutional Review Boards.

Informed Consent Statement

Informed consent was obtained from all subjects involved in the original dataset studies.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Bloem, B.R.; Okun, M.S.; Klein, C. Parkinson’s disease. Lancet 2021, 397, 2284–2303. [Google Scholar] [CrossRef]
  2. Poewe, W.; Seppi, K.; Tanner, C.M.; Halliday, G.M.; Brundin, P.; Volkmann, J.; Schrag, A.E.; Lang, A.E. Parkinson disease. Nat. Rev. Dis. Primers 2017, 3, 17013. [Google Scholar] [CrossRef] [PubMed]
  3. Gibb, W.R.G.; Lees, A.J. The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson’s disease. J. Neurol. Neurosurg. Psychiatry 1988, 51, 745–752. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  4. Rizzo, G.; Copetti, M.; Arcuti, S.; Martino, D.; Fontana, A.; Logroscino, G. Accuracy of clinical diagnosis of Parkinson disease A systematic review and meta-analysis. Neurology 2016, 91, e479–e489. [Google Scholar] [CrossRef]
  5. Sanchez-Ferro, A.; Elshehabi, M.; Godinho, C.; Salkovic, D.; Hobert, M.A.; Domingos, J.; van Uem, J.M.; Ferreira, J.J.; Maetzler, W. New methods for the assessment of Parkinson’s disease (2005 to 2015): A systematic review. Mov. Disord. Off. J. Mov. Disord. Soc. 2016, 31, 1283–1292. [Google Scholar] [CrossRef] [Green Version]
  6. Anand, V.; Bilal, E.; Ho, B.; Rice, J.J. Towards motor evaluation of Parkinson’s Disease Patients using wearable inertial sensors. AMIA Annu. Symp. Proc. AMIA Symp. 2020, 2020, 203–212. [Google Scholar]
  7. Stamatakis, J.; Ambroise, J.; Cremers, J.; Sharei, H.; Delvaux, V.; Macq, B.; Garraux, G. Finger tapping clinimetric score prediction in Parkinson’s disease using low-cost accelerometers. Comput. Intell. Neurosci. 2013, 2013, 717853. [Google Scholar] [CrossRef]
  8. Summa, S.; Tosi, J.; Taffoni, F.; Di Biase, L.; Marano, M.; Rizzo, A.C.; Tombini, M.; Di Pino, G.; Formica, D. Assessing Bradykinesia in Parkinson’s Disease Using Gyroscope Signals. In Proceedings of the 2017 International Conference on Rehabilitation Robotics (ICORR), London, UK, 17–20 July 2017; IEEE: Piscataway, NJ, USA, 2017; pp. 1556–1561. [Google Scholar]
  9. Di Biase, L.; Summa, S.; Tosi, J.; Taffoni, F.; Marano, M.; Cascio Rizzo, A.; Vecchio, F.; Formica, D.; Di Lazzaro, V.; Di Pino, G.; et al. Quantitative Analysis of Bradykinesia and Rigidity in Parkinson’s Disease. Front. Neurol. 2018, 9, 121. [Google Scholar] [CrossRef] [Green Version]
  10. Endo, T.; Okuno, R.; Yokoe, M.; Akazawa, K.; Sakoda, S. A novel method for systematic analysis of rigidity in Parkinson’s disease. Mov. Disord. Off. J. Mov. Disord. Soc. 2009, 24, 2218–2224. [Google Scholar] [CrossRef]
  11. Kwon, Y.; Park, S.H.; Kim, J.W.; Ho, Y.; Jeon, H.M.; Bang, M.J.; Koh, S.B.; Kim, J.H.; Eom, G.M. Quantitative evaluation of parkinsonian rigidity during intra-operative deep brain stimulation. Bio-Med. Mater. Eng. 2014, 24, 2273–2281. [Google Scholar] [CrossRef] [Green Version]
  12. Raiano, L.; Di Pino, G.; Di Biase, L.; Tombini, M.; Tagliamonte, N.L.; Formica, D. PDMeter: A Wrist Wearable Device for an at-home Assessment of the Parkinson’s Disease Rigidity. IEEE Trans. Neural Syst. Rehabil. Eng. 2020, 28, 1325–1333. [Google Scholar] [CrossRef] [PubMed]
  13. Deuschl, G.; Krack, P.; Lauk, M.; Timmer, J. Clinical neurophysiology of tremor. J. Clin. Neurophysiol. 1996, 13, 110–121. [Google Scholar] [CrossRef] [PubMed]
  14. Di Pino, G.; Formica, D.; Melgari, J.-M.; Taffoni, F.; Salomone, G.; di Biase, L.; Caimo, E.; Vernieri, F.; Guglielmelli, E. Neurophysiological bases of tremors and accelerometric parameters analysis. In Proceedings of the 2012 4th IEEE RAS & EMBS International Conference on Biomedical Robotics and Biomechatronics (BioRob), Rome, Italy, 24–27 June 2012; pp. 1820–1825. [Google Scholar]
  15. Di Biase, L.; Brittain, J.S.; Shah, S.A.; Pedrosa, D.J.; Cagnan, H.; Mathy, A.; Chen, C.C.; Martin-Rodriguez, J.F.; Mir, P.; Timmerman, L.; et al. Tremor stability index: A new tool for differential diagnosis in tremor syndromes. Brain J. Neurol. 2017, 140, 1977–1986. [Google Scholar] [CrossRef]
  16. Di Biase, L.; Brittain, J.-s.; Peter, B.; Di LAZZARO, V.; Shah, S.A. Methods and System for Characterising Tremors. Patent WO/2018/134579, 26 July 2018. [Google Scholar]
  17. Moore, S.T.; MacDougall, H.G.; Gracies, J.M.; Cohen, H.S.; Ondo, W.G. Long-term monitoring of gait in Parkinson’s disease. Gait Posture 2007, 26, 200–207. [Google Scholar] [CrossRef] [PubMed]
  18. Schlachetzki, J.C.M.; Barth, J.; Marxreiter, F.; Gossler, J.; Kohl, Z.; Reinfelder, S.; Gassner, H.; Aminian, K.; Eskofier, B.M.; Winkler, J.; et al. Wearable sensors objectively measure gait parameters in Parkinson’s disease. PLoS ONE 2017, 12, e0183989. [Google Scholar] [CrossRef]
  19. Tosi, J.; Summa, S.; Taffoni, F.; Biase, L.d.; Marano, M.; Rizzo, A.C.; Tombini, M.; Schena, E.; Formica, D.; Pino, G.D. Feature Extraction in Sit-to-Stand Task Using M-IMU Sensors and Evaluatiton in Parkinson’s Disease. In Proceedings of the 2018 IEEE International Symposium on Medical Measurements and Applications (MeMeA), Rome, Italy, 11–13 June 2018; pp. 1–6. [Google Scholar]
  20. Suppa, A.; Kita, A.; Leodori, G.; Zampogna, A.; Nicolini, E.; Lorenzi, P.; Rao, R.; Irrera, F. L-DOPA and freezing of gait in Parkinson’s disease: Objective assessment through a wearable wireless system. Front. Neurol. 2017, 8, 406. [Google Scholar] [CrossRef] [PubMed]
  21. Di Biase, L.; Di Santo, A.; Caminiti, M.L.; De Liso, A.; Shah, S.A.; Ricci, L.; Di Lazzaro, V. Gait analysis in Parkinson’s disease: An overview of the most accurate markers for diagnosis and symptoms monitoring. Sensors 2020, 20, 3529. [Google Scholar] [CrossRef]
  22. Di Biase, L.; Raiano, L.; Caminiti, M.L.; Pecoraro, P.M.; Di Lazzaroo, V. Artificial intelligence in Parkinson’s disease—Symptoms identification and monitoring. In Augmenting Neurological Disorder Prediction and Rehabilitation Using Artificial Intelligence; Elsevier: Amsterdam, The Netherlands, 2022; pp. 35–52. [Google Scholar]
  23. Di Biase, L.; Tinkhauser, G.; Martin Moraud, E.; Caminiti, M.L.; Pecoraro, P.M.; Di Lazzaro, V. Adaptive, personalized closed-loop therapy for Parkinson’s disease: Biochemical, neurophysiological, and wearable sensing systems. Expert Rev. Neurother. 2021, 21, 1371–1388. [Google Scholar] [CrossRef]
  24. Dicharry, J. Kinematics and kinetics of gait: From lab to clinic. Clin. Sports Med. 2010, 29, 347–364. [Google Scholar] [CrossRef]
  25. Webster, J.B.; Darter, B.J. Principles of Normal and Pathologic Gait. In Atlas of Orthoses and Assistive Devices; Elsevier: Amsterdam, The Netherlands, 2019; pp. 49–62.e1. [Google Scholar]
  26. Sica, M.; Tedesco, S.; Crowe, C.; Kenny, L.; Moore, K.; Timmons, S.; Barton, J.; O’Flynn, B.; Komaris, D.-S. Continuous home monitoring of Parkinson’s disease using inertial sensors: A systematic review. PLoS ONE 2021, 16, e0246528. [Google Scholar] [CrossRef]
  27. Schaafsma, J.D.; Giladi, N.; Balash, Y.; Bartels, A.L.; Gurevich, T.; Hausdorff, J.M. Gait dynamics in Parkinson’s disease: Relationship to Parkinsonian features, falls and response to levodopa. J. Neurol. Sci. 2003, 212, 47–53. [Google Scholar] [CrossRef]
  28. Blin, O.; Ferrandez, A.M.; Pailhous, J.; Serratrice, G. Dopa-sensitive and dopa-resistant gait parameters in Parkinson’s disease. J. Neurol. Sci. 1991, 103, 51–54. [Google Scholar] [CrossRef]
  29. Del Olmo, M.F.; Cudeiro, J. Temporal variability of gait in Parkinson disease: Effects of a rehabilitation programme based on rhythmic sound cues. Parkinsonism Relat. Disord. 2005, 11, 25–33. [Google Scholar] [CrossRef] [PubMed]
  30. Frenkel-Toledo, S.; Giladi, N.; Peretz, C.; Herman, T.; Gruendlinger, L.; Hausdorff, J.M. Treadmill walking as an external pacemaker to improve gait rhythm and stability in Parkinson’s disease. Mov. Disord. Off. J. Mov. Disord. Soc. 2005, 20, 1109–1114. [Google Scholar] [CrossRef]
  31. Pieruccini-Faria, F.; Montero-Odasso, M.; Hausdorff, J.M. Gait variability and fall risk in older adults: The role of cognitive function. In Falls and Cognition in Older Persons; Springer: Berlin/Heidelberg, Germany, 2020; pp. 107–138. [Google Scholar]
  32. Hausdorff, J.M.; Rios, D.A.; Edelberg, H.K. Gait variability and fall risk in community-living older adults: A 1-year prospective study. Arch. Phys. Med. Rehabil. 2001, 82, 1050–1056. [Google Scholar] [CrossRef]
  33. Maki, B.E. Gait changes in older adults: Predictors of falls or indicators of fear. J. Am. Geriatr. Soc. 1997, 45, 313–320. [Google Scholar] [CrossRef] [PubMed]
  34. Baltadjieva, R.; Giladi, N.; Gruendlinger, L.; Peretz, C.; Hausdorff, J.M. Marked alterations in the gait timing and rhythmicity of patients with de novo Parkinson’s disease. Eur. J. Neurosci. 2006, 24, 1815–1820. [Google Scholar] [CrossRef]
  35. Su, B.; Song, R.; Guo, L.; Yen, C.-W. Characterizing gait asymmetry via frequency sub-band components of the ground reaction force. Biomed. Signal Process. Control 2015, 18, 56–60. [Google Scholar] [CrossRef]
  36. Yogev, G.; Giladi, N.; Peretz, C.; Springer, S.; Simon, E.S.; Hausdorff, J.M. Dual tasking, gait rhythmicity, and Parkinson’s disease: Which aspects of gait are attention demanding? Eur. J. Neurosci. 2005, 22, 1248–1256. [Google Scholar] [CrossRef]
  37. Hausdorff, J.M.; Lowenthal, J.; Herman, T.; Gruendlinger, L.; Peretz, C.; Giladi, N. Rhythmic auditory stimulation modulates gait variability in Parkinson’s disease. Eur. J. Neurosci. 2007, 26, 2369–2375. [Google Scholar] [CrossRef]
  38. Hausdorff, J.M.; Lertratanakul, A.; Cudkowicz, M.E.; Peterson, A.L.; Kaliton, D.; Goldberger, A.L. Dynamic markers of altered gait rhythm in amyotrophic lateral sclerosis. J. Appl. Physiol. 2000, 88, 2045–2053. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  39. Goldberger, A.L.; Amaral, L.A.; Glass, L.; Hausdorff, J.M.; Ivanov, P.C.; Mark, R.G.; Mietus, J.E.; Moody, G.B.; Peng, C.-K.; Stanley, H.E. PhysioBank, PhysioToolkit, and PhysioNet: Components of a new research resource for complex physiologic signals. Circulation 2000, 101, e215–e220. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  40. Gelb, D.J.; Oliver, E.; Gilman, S. Diagnostic criteria for Parkinson disease. Arch. Neurol. 1999, 56, 33–39. [Google Scholar] [CrossRef]
  41. Hoehn, M.M.; Yahr, M.D. Parkinsonism onset, progression, and mortality. Neurology 1967, 17, 427. [Google Scholar] [CrossRef] [Green Version]
  42. Fahn, S.; Elton, R.; UPDRS Development Committee. Recent Developments in Parkinson’s Disease; Macmillan Health Care Information: Folorham Park, NJ, USA, 1987; Volume 2, pp. 153–163, 293–304. [Google Scholar]
  43. Hausdorff, J.M.; Ladin, Z.; Wei, J.Y. Footswitch system for measurement of the temporal parameters of gait. J. Biomech. 1995, 28, 347–351. [Google Scholar] [CrossRef]
  44. Son, M.; Han, S.H.; Lyoo, C.H.; Lim, J.; Jeon, J.; Hong, K.-B.; Park, H. The effect of levodopa on bilateral coordination and gait asymmetry in Parkinson’s disease using inertial sensor. NPJ Parkinson’s Dis. 2021, 7, 42. [Google Scholar] [CrossRef] [PubMed]
  45. Blin, O.; Ferrandez, A.M.; Serratrice, G. Quantitative analysis of gait in Parkinson patients: Increased variability of stride length. J. Neurol. Sci. 1990, 98, 91–97. [Google Scholar] [CrossRef]
  46. Hausdorff, J.M.; Cudkowicz, M.E.; Firtion, R.; Wei, J.Y.; Goldberger, A.L. Gait variability and basal ganglia disorders: Stride-to-stride variations of gait cycle timing in Parkinson’s disease and Huntington’s disease. Mov. Disord. Off. J. Mov. Disord. Soc. 1998, 13, 428–437. [Google Scholar] [CrossRef] [PubMed]
  47. Gabell, A.; Nayak, U.S. The effect of age on variability in gait. J. Gerontol. 1984, 39, 662–666. [Google Scholar] [CrossRef]
  48. Hausdorff, J.M.; Mitchell, S.L.; Firtion, R.; Peng, C.K.; Cudkowicz, M.E.; Wei, J.Y.; Goldberger, A.L. Altered fractal dynamics of gait: Reduced stride-interval correlations with aging and Huntington’s disease. J. Appl. Physiol. 1997, 82, 262–269. [Google Scholar] [CrossRef]
  49. Hollman, J.H.; Von Arb, H.M.; Budreck, A.M.; Muehlemann, A.; Ness, D.K. Treadmill walking alters stride time dynamics in Parkinson’s disease. Gait Posture 2020, 77, 195–200. [Google Scholar] [CrossRef] [PubMed]
  50. Yamasaki, M.; Sasaki, T.; Torii, M. Sex difference in the pattern of lower limb movement during treadmill walking. Eur. J. Appl. Physiol. Occup. Physiol. 1991, 62, 99–103. [Google Scholar] [CrossRef] [PubMed]
  51. Frenkel-Toledo, S.; Giladi, N.; Peretz, C.; Herman, T.; Gruendlinger, L.; Hausdorff, J.M. Effect of gait speed on gait rhythmicity in Parkinson’s disease: Variability of stride time and swing time respond differently. J. Neuroeng. Rehabil. 2005, 2, 23. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  52. Malatesta, D.; Simar, D.; Dauvilliers, Y.; Candau, R.; Borrani, F.; Prefaut, C.; Caillaud, C. Energy cost of walking and gait instability in healthy 65- and 80-yr-olds. J. Appl. Physiol. 2003, 95, 2248–2256. [Google Scholar] [CrossRef] [Green Version]
  53. Grabiner, P.C.; Biswas, S.T.; Grabiner, M.D. Age-related changes in spatial and temporal gait variables. Arch. Phys. Med. Rehabil. 2001, 82, 31–35. [Google Scholar] [CrossRef]
  54. Alam, M.N.; Garg, A.; Munia, T.T.K.; Fazel-Rezai, R.; Tavakolian, K. Vertical ground reaction force marker for Parkinson’s disease. PLoS ONE 2017, 12, e0175951. [Google Scholar] [CrossRef]
Figure 1. Gait kinetics (upper figure) and kinematics features (lower figure) (modified under the terms and conditions of the Creative Commons Attribution (CC BY) license from [21]).
Figure 1. Gait kinetics (upper figure) and kinematics features (lower figure) (modified under the terms and conditions of the Creative Commons Attribution (CC BY) license from [21]).
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Figure 2. Force-sensitive insole. Each insole placed in subjects’ shoes contains eight pressure-sensitive sensors in order to record the time series of the ground reaction force (GRF), while subjects were asked to walk on level ground.
Figure 2. Force-sensitive insole. Each insole placed in subjects’ shoes contains eight pressure-sensitive sensors in order to record the time series of the ground reaction force (GRF), while subjects were asked to walk on level ground.
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Figure 3. Segmentation of the gait cycle implemented using the differential ground reaction force (GRF) between total right force and total left force. DLS: double limb support, GRF: ground reaction force, SLS-L: left single limb support, SLS-R: right single limb support.
Figure 3. Segmentation of the gait cycle implemented using the differential ground reaction force (GRF) between total right force and total left force. DLS: double limb support, GRF: ground reaction force, SLS-L: left single limb support, SLS-R: right single limb support.
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Figure 4. Average values of kinematic central tendency indices (gait speed and Time Up and Go) and dispersion indices of PD patients and HS with significant differences on the t-test. IQR = interquartile range. SD = standard deviation.
Figure 4. Average values of kinematic central tendency indices (gait speed and Time Up and Go) and dispersion indices of PD patients and HS with significant differences on the t-test. IQR = interquartile range. SD = standard deviation.
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Figure 5. ROC graph of statistically significant kinematic features, considering a diagnosis as a target of PD over HS. IQR: interquartile range, SD: standard deviation.
Figure 5. ROC graph of statistically significant kinematic features, considering a diagnosis as a target of PD over HS. IQR: interquartile range, SD: standard deviation.
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Figure 6. Healthy subjects gait dynamic. Right (R tot) (red line) and Left (L tot) (green line) total force averaged along gait cycles (GC) and subjects over the percentage of completion of the gait cycle (top). The bottom part of the figure represents a graphical visualization of the force measured by the single sensors embedded within the instrumented insole: the larger the circles (right red; left green), the larger the force measured.
Figure 6. Healthy subjects gait dynamic. Right (R tot) (red line) and Left (L tot) (green line) total force averaged along gait cycles (GC) and subjects over the percentage of completion of the gait cycle (top). The bottom part of the figure represents a graphical visualization of the force measured by the single sensors embedded within the instrumented insole: the larger the circles (right red; left green), the larger the force measured.
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Figure 7. Parkinson’s disease gait dynamic. Right (R tot) (red line) and Left (L tot) (green line) total force averaged along gait cycles (GC) and subjects over the percentage of completion of the gait cycle (top). The bottom part of the figure represents a graphical visualization of the force measured by the single sensors embedded within the instrumented insole: the larger the circles (right red; left green), the larger the force measured.
Figure 7. Parkinson’s disease gait dynamic. Right (R tot) (red line) and Left (L tot) (green line) total force averaged along gait cycles (GC) and subjects over the percentage of completion of the gait cycle (top). The bottom part of the figure represents a graphical visualization of the force measured by the single sensors embedded within the instrumented insole: the larger the circles (right red; left green), the larger the force measured.
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Table 1. Composition of cohorts.
Table 1. Composition of cohorts.
RefCohortDatasetData SourceGroupSubjects NumberGenderAge
(m ± SD)
Hoehn and Yahr
(m ± SD)
UPDRS (m ± SD)
[36]11Movement Disorders Unit at the Tel-Aviv Sourasky Medical CenterPD2969% male71 ± 82.3 ± 0.433 ± 12
HS1856% male72 ± 7
[37]21Movement Disorders Unit at the Tel Aviv Sourasky Medical CenterPD2955% male67 ± 92.4 ± 0.425 ± 8
HS2546% male65 ± 7
[30]31Movement Disorders Unit at the Tel-Aviv Sourasky Medical Center.PD3563% male62 ± 92.1 ± 0.236 ± 11
HS2962% male58 ± 7
[38]42Neurology Outpatient Clinic at Massachusetts General Hospital.PD1567% male67 ± 112.8 ± 0.9
HS1613% male39 ± 19
Legend: HS: healthy subjects, Hoehn and Yahr scale [41] is a clinical scale that describes the PD stage from 1 (unilateral body involvement) to 5 (confinement to bed or wheelchair), IQR: interquartile range, med: median, PD: Parkinson’s disease patients, m ± SD: mean ± standard deviation, UPDRS total: Unified Parkinson’s Disease Rating Scale [42] is a clinical scale used to follow Parkinson’s disease symptoms during the disease course.
Table 2. Overview of the main data manipulation steps.
Table 2. Overview of the main data manipulation steps.
First Dataset
Cohort 1-2-3
Second Dataset
Cohort 4
Type of Data Available
  • raw data of the instrumented insoles (gait dynamics)
  • raw data of the instrumented insoles (gait dynamics)
  • gait interval parameters (gait kinematics)
Data Manipulation
Kinematic Analysis:
  • Calculation of the differential ground reaction force ( δ ).
  • Extrapolation of the DLS and SLS parameters.
  • Calculation of the gait cycles and the main kinematic parameters (see Figure 1)
  • Normalization with respect to gait cycle.
Kinematic Analysis:
  • Kinematic parameters were already available; thus no further data manipulation was performed.
Dynamic Analysis:
  • Dynamic data already available, thus no further data manipulation was performed.
Dynamic Analysis:
  • Dynamic data available but expressed as raw signals of the instrumented insoles (expressed in volt). Thus, a normalization of the raw signals was performed in order with respect the maximal output of the electronic system composing the insole (according to [43]).
Table 3. Kinematic central tendency and dispersion indices.
Table 3. Kinematic central tendency and dispersion indices.
VariablesGroupNAverageStandard Deviationtdfp Value
Kinematiccentral tendency indicesGait Speed (m/s)HS881.2600.1668.278194<0.001 *
PD1081.0190.227
Time Up and Go (s)HS629.3001.604−5.187150<0.001 *
PD9012.0563.962
Ave left SWINGHS880.4420.0400.3611940.719
PD1080.4390.046
Ave right SWINGHS880.4430.0411.1581940.248
PD1080.4350.047
Ave left SWING %HS8841.8043.1431.9511940.053
PD10840.7814.018
Ave right SWING %HS8841.9163.4882.6821940.008
PD10840.3954.284
Ave left STANCEHS880.6180.071−2.1271940.035
PD1080.6460.109
Ave right STANCEHS880.6160.074−2.4311940.016
PD1080.6500.109
Ave left STANCE %HS8858.1963.143−1.9511940.053
PD10859.2194.018
Ave right STANCE %HS8858.0843.488−2.6821940.008
PD10859.6054.284
Ave DOUBLE SUPPORT HS880.1150.095−1.1061940.270
PD1080.1330.120
Ave DOUBLE SUPPORT %HS8810.6818.528−0.8081940.420
PD10811.7349.492
Med left SWINGHS880.4410.0400.1231940.902
PD1080.4400.048
Med right SWINGHS880.4420.0410.9631940.337
PD1080.4360.047
Med left SWING %HS8841.9993.1951.8441940.067
PD10841.0294.003
Med right SWING %HS8842.0643.4872.5021940.013
PD10840.6554.240
Med left STANCEHS880.6110.069−2.0431940.042
PD1080.6380.106
Med right STANCEHS880.6110.073−2.3031940.022
PD1080.6420.106
Med left STANCE %HS8858.0013.195−1.8441940.067
PD10858.9714.003
Med right STANCE %HS8857.9363.487−2.5021940.013
PD10859.3454.240
Med DOUBLE SUPPORTHS880.1130.094−0.9431940.347
PD1080.1270.110
Med DOUBLE SUPPORT%HS8810.4838.518−0.7421940.459
PD10811.4419.368
dispersion indices SD left SWINGHS880.0220.009−4.851194<0.001 *
PD1080.0320.017
SD right SWINGHS880.0220.008−4.357194<0.001 *
PD1080.0340.025
SD left SWING %HS881.6860.762−4.400194<0.001 *
PD1082.3571.254
SD right SWING %HS881.5680.613−6.093194<0.001 *
PD1082.3831.127
SD left STANCEHS880.0350.016−1.6401940.103
PD1080.0650.170
SD right STANCEHS880.0330.014−1.7361940.084
PD1080.0580.135
SD left STANCE %HS881.6860.762−4.400194<0.001 *
PD1082.3571.254
SD right STANCE %HS881.5680.613−6.093194<0.001 *
PD1082.3831.127
SD DOUBLE SUPPORTHS880.0190.015−1.4411940.151
PD1080.0450.171
SD DOUBLE SUPPORT %HS881.3860.718−3.396194<0.001 *
PD1082.0721.780
IQR left SWING HS880.0170.006−6.651194<0.001 *
PD1080.0270.014
IQR right SWING HS880.0170.006−5.821194<0.001 *
PD1080.0270.016
IQR left SWING %HS881.3260.323−6.279194<0.001 *
PD1081.8960.799
IQR right SWING %HS881.2290.337−7.009194<0.001 *
PD1081.9050.852
IQR left STANCE HS880.0260.009−4.577194<0.001 *
PD1080.0370.020
IQR right STANCE HS880.0260.009−4.902194<0.001 *
PD1080.0370.020
IQR left STANCE %HS881.3260.323−6.279194<0.001 *
PD1081.8960.799
IQR right STANCE %HS881.2290.337−7.009194<0.001 *
PD1081.9050.852
IQR DOUBLE SUPPORT HS880.0130.008−2.8751940.004
PD1080.0180.014
IQR_DOUBLE_SUPPORT %HS881.1410.502−3.446194<0.001 *
PD1081.6131.203
Legend: ave: average, HS: healthy subjects, IQR: interquartile range, med: median, PD: Parkinson’s disease patients, SD: standard deviation, *: t-test statistically significant p-value.
Table 4. ROC analysis of statistically significant kinematic features.
Table 4. ROC analysis of statistically significant kinematic features.
VariablesAUCStandard Errorp ValueLower LimitUpper Limit
Gait Speed (m/s)0.2000.035<0.001 *0.1300.269
Time Up and Go (s)0.8010.036<0.001 *0.7300.872
SD left SWING0.6820.044<0.001 *0.5950.768
SD right SWING0.7030.043<0.001 *0.6200.787
SD left SWING %0.6740.045<0.001 *0.5850.763
SD right SWING %0.7400.041<0.001 *0.6600.819
SD left STANCE %0.6740.045<0.001 *0.5850.763
SD right STANCE %0.7400.041<0.001 *0.6600.819
SD DOUBLE SUPPORT%0.6430.039<0.001 *0.5660.720
IQR left SWING 0.7780.037<0.001 *0.7040.851
IQR right SWING 0.7330.041<0.001 *0.6540.813
IQR left SWING %0.7760.037<0.001 *0.7030.848
IQR right SWING %0.8200.034<0.001 *0.7540.886
IQR left STANCE 0.6390.0450.0036 0.5510.727
IQR right STANCE 0.6670.044<0.001 *0.5800.754
IQR left STANCE %0.7760.037<0.001 *0.7030.848
IQR right STANCE %0.8200.034<0.001 *0.7540.886
IQR DOUBLE SUPPORT %0.6340.0400.0012 0.5560.712
Legend: IQR: interquartile range, SD: standard deviation, * ROC: statistically significant p-value.
Table 5. Dynamic central tendency and dispersion indices.
Table 5. Dynamic central tendency and dispersion indices.
VariablesGroupNAverageStandard Deviationtdfp Value
dynamiccentral tendency indicesAve Force leftHS88372.346181.982−0.8131940.417
PD108392.385162.683
Ave Force rightHS88369.036181.877−1.0441940.298
PD108394.455158.804
Med Force leftHS88467.395235.065−0.5371940.592
PD108484.518210.938
Med Force rightHS88459.291235.530−1.0251940.307
PD108491.887209.364
dispersion indices SD Force leftHS88324.871160.322−0.561 1940.576
PD108336.977141.656
SD Force rightHS88324.106160.490−0.608 1940.544
PD108337.011136.732
IQR Force leftHS88671.779332.736−0.764 1940.446
PD108706.230297.570
IQR Force rightHS88671.246332.261−0.8771940.382
PD108710.175288.892
Legend: ave: average, HS: healthy subjects, IQR: interquartile range, med: median, PD: Parkinson’s disease patients, SD: standard deviation.
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di Biase, L.; Raiano, L.; Caminiti, M.L.; Pecoraro, P.M.; Di Lazzaro, V. Parkinson’s Disease Wearable Gait Analysis: Kinematic and Dynamic Markers for Diagnosis. Sensors 2022, 22, 8773. https://doi.org/10.3390/s22228773

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di Biase L, Raiano L, Caminiti ML, Pecoraro PM, Di Lazzaro V. Parkinson’s Disease Wearable Gait Analysis: Kinematic and Dynamic Markers for Diagnosis. Sensors. 2022; 22(22):8773. https://doi.org/10.3390/s22228773

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di Biase, Lazzaro, Luigi Raiano, Maria Letizia Caminiti, Pasquale Maria Pecoraro, and Vincenzo Di Lazzaro. 2022. "Parkinson’s Disease Wearable Gait Analysis: Kinematic and Dynamic Markers for Diagnosis" Sensors 22, no. 22: 8773. https://doi.org/10.3390/s22228773

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