Agreement between Optoelectronic System and Wearable Sensors for the Evaluation of Gait Spatiotemporal Parameters in Progressive Supranuclear Palsy
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Population and Clinical Assessment
2.2. Gait Analysis Systems
- anthropometric measurements,
- positioning of passive markers on patients’ body (from the feet to the shoulders) according to the Davis protocol,
- standing phase,
- walking phases.
2.3. Study Protcol
- Cadence (steps/minute): stepping rate.
- Cycle duration (s): duration of a complete gait cycle.
- Speed (m/s): walking speed.
- Stance phase (% gait cycle time): average percentage of a gait cycle that either foot is on the ground.
- Swing phase (% gait cycle time): average percentage of a gait cycle that either foot is off the ground.
- Stride length (m): distance between two consecutive foot falls at the moments of initial contacts.
2.4. Statistical Analyses
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Hatanaka, N.; Sato, K.; Hishikawa, N.; Takemoto, M.; Ohta, Y.; Yamashita, T.; Abe, K. Comparative Gait Analysis in Progressive Supranuclear Palsy and Parkinson’s Disease. Eur. Neurol. 2016, 75, 282–289. [Google Scholar] [CrossRef] [PubMed]
- 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, 1066–1075. [Google Scholar] [CrossRef] [PubMed]
- Rogers, M.W. Disorders of Posture, Balance, and Gait in Parkinson’s Disease. Clin. Geriatr. Med. 1996, 12, 825–845. [Google Scholar] [CrossRef] [PubMed]
- Golbe, L.I.; Ohman-Strickland, P.A. A Clinical Rating Scale for Progressive Supranuclear Palsy. Brain 2007, 130, 1552–1565. [Google Scholar] [CrossRef] [PubMed]
- Nonnekes, J.; Goselink, R.J.M.; Růžička, E.; Fasano, A.; Nutt, J.G.; Bloem, B.R. Neurological Disorders of Gait, Balance and Posture: A Sign-Based Approach. Nat. Rev. Neurol. 2018, 14, 183–189. [Google Scholar] [CrossRef] [PubMed]
- Salarian, A.; Russmann, H.; Vingerhoets, F.J.G.; Dehollain, C.; Blanc, Y.; Burkhard, P.R.; Aminian, K. Gait Assessment in Parkinson’s Disease: Toward an Ambulatory System for Long-Term Monitoring. IEEE Trans. Biomed. Eng. 2004, 51, 1434–1443. [Google Scholar] [CrossRef]
- Sveinbjornsdottir, S. The Clinical Symptoms of Parkinson’s Disease. J. Neurochem. 2016, 139, 318–324. [Google Scholar] [CrossRef]
- Cesarelli, G.; Donisi, L.; Amato, F.; Romano, M.; Cesarelli, M.; D’Addio, G.; Ponsiglione, A.M.; Ricciardi, C. Using Features Extracted from Upper Limb Reaching Tasks to Detect Parkinson’s Disease by Means of Machine Learning Models. IEEE Trans. Neural Syst. Rehabil. Eng. 2023, 31, 1056–1063. [Google Scholar] [CrossRef]
- Morris, R.; Stuart, S.; McBarron, G.; Fino, P.C.; Mancini, M.; Curtze, C. Validity of Mobility Lab (Version 2) for Gait Assessment in Young Adults, Older Adults and Parkinson’s Disease. Physiol. Meas. 2019, 40, 095003. [Google Scholar] [CrossRef]
- Fasano, A.; Plotnik, M.; Bove, F.; Berardelli, A. The Neurobiology of Falls. Neurol. Sci. Off. J. Ital. Neurol. Soc. Ital. Soc. Clin. Neurophysiol. 2012, 33, 1215–1223. [Google Scholar] [CrossRef]
- Zago, M.; Sforza, C.; Pacifici, I.; Cimolin, V.; Camerota, F.; Celletti, C.; Condoluci, C.; De Pandis, M.F.; Galli, M. Gait Evaluation Using Inertial Measurement Units in Subjects with Parkinson’s Disease. J. Electromyogr. Kinesiol. 2018, 42, 44–48. [Google Scholar] [CrossRef] [PubMed]
- Warmerdam, E.; Schumacher, M.; Beyer, T.; Nerdal, P.T.; Schebesta, L.; Stürner, K.H.; Zeuner, K.E.; Hansen, C.; Maetzler, W. Postural Sway in Parkinson’s Disease and Multiple Sclerosis Patients During Tasks with Different Complexity. Front. Neurol. 2022, 13, 857406. [Google Scholar] [CrossRef] [PubMed]
- Picillo, M.; Ricciardi, C.; Tepedino, M.F.; Abate, F.; Cuoco, S.; Carotenuto, I.; Erro, R.; Ricciardelli, G.; Russo, M.; Cesarelli, M.; et al. Gait Analysis in Progressive Supranuclear Palsy Phenotypes. Front. Neurol. 2021, 12, 674495. [Google Scholar] [CrossRef] [PubMed]
- Abate, F.; Russo, M.; Ricciardi, C.; Tepedino, M.F.; Romano, M.; Erro, R.; Pellecchia, M.T.; Amboni, M.; Barone, P.; Picillo, M. Wearable Sensors for Assessing Disease Severity and Progression in Progressive Supranuclear Palsy. Park. Relat. Disord. 2023, 109, 105345. [Google Scholar] [CrossRef] [PubMed]
- Stamatakis, J.; Crémers, J.; Maquet, D.; Macq, B.; Garraux, G. Gait Feature Extraction in Parkinson’s Disease Using Low-Cost Accelerometers. In Proceedings of the 2011 Annual International Conference of the IEEE Engineering in Medicine and Biology Society, Boston, MA, USA, 30 August–3 September 2011; pp. 7900–7903. [Google Scholar]
- Zhou, H.; Hu, H. Human Motion Tracking for Rehabilitation—A Survey. Biomed. Signal Process. Control 2008, 3, 1–18. [Google Scholar] [CrossRef]
- Hreljac, A.; Marshall, R.N. Algorithms to Determine Event Timing during Normal Walking Using Kinematic Data. J. Biomech. 2000, 33, 783–786. [Google Scholar] [CrossRef] [PubMed]
- McGinley, J.L.; Baker, R.; Wolfe, R.; Morris, M.E. The Reliability of Three-Dimensional Kinematic Gait Measurements: A Systematic Review. Gait Posture 2009, 29, 360–369. [Google Scholar] [CrossRef]
- Saggio, G.; Tombolini, F.; Ruggiero, A. Technology-Based Complex Motor Tasks Assessment: A 6-DOF Inertial-Based System Versus a Gold-Standard Optoelectronic-Based One. IEEE Sens. J. 2021, 21, 1616–1624. [Google Scholar] [CrossRef]
- Santos, T.M.O.; Barroso, M.F.S.; Ricco, R.A.; Nepomuceno, E.G.; Alvarenga, É.L.F.C.; Penoni, Á.C.O.; Santos, A.F. A Low-Cost Wireless System of Inertial Sensors to Postural Analysis during Human Movement. Measurement 2019, 148, 106933. [Google Scholar] [CrossRef]
- Wu, Y.; Su, Y.; Feng, R.; Yu, N.; Zang, X. Wearable-Sensor-Based Pre-Impact Fall Detection System with a Hierarchical Classifier. Measurement 2019, 140, 283–292. [Google Scholar] [CrossRef]
- Muro-de-la-Herran, A.; Garcia-Zapirain, B.; Mendez-Zorrilla, A. Gait Analysis Methods: An Overview of Wearable and Non-Wearable Systems, Highlighting Clinical Applications. Sensors 2014, 14, 3362–3394. [Google Scholar] [CrossRef] [PubMed]
- Donisi, L.; Pagano, G.; Cesarelli, G.; Coccia, A.; Amitrano, F.; D’Addio, G. Benchmarking between Two Wearable Inertial Systems for Gait Analysis Based on a Different Sensor Placement Using Several Statistical Approaches. Measurement 2021, 173, 108642. [Google Scholar] [CrossRef]
- Mancini, M.; Smulders, K.; Harker, G.; Stuart, S.; Nutt, J.G. Assessment of the Ability of Open- and Closed-Loop Cueing to Improve Turning and Freezing in People with Parkinson’s Disease. Sci. Rep. 2018, 8, 12773. [Google Scholar] [CrossRef] [PubMed]
- Muthukrishnan, N.; Abbas, J.J.; Shill, H.A.; Krishnamurthi, N. Cueing Paradigms to Improve Gait and Posture in Parkinson’s Disease: A Narrative Review. Sensors 2019, 19, 5468. [Google Scholar] [CrossRef] [PubMed]
- Bugané, F.; Benedetti, M.G.; Casadio, G.; Attala, S.; Biagi, F.; Manca, M.; Leardini, A. Estimation of Spatial-Temporal Gait Parameters in Level Walking Based on a Single Accelerometer: Validation on Normal Subjects by Standard Gait Analysis. Comput. Methods Programs Biomed. 2012, 108, 129–137. [Google Scholar] [CrossRef] [PubMed]
- Mariani, B.; Hoskovec, C.; Rochat, S.; Büla, C.; Penders, J.; Aminian, K. 3D Gait Assessment in Young and Elderly Subjects Using Foot-Worn Inertial Sensors. J. Biomech. 2010, 43, 2999–3006. [Google Scholar] [CrossRef]
- Webster, K.E.; Wittwer, J.E.; Feller, J.A. Validity of the GAITRite® Walkway System for the Measurement of Averaged and Individual Step Parameters of Gait. Gait Posture 2005, 22, 317–321. [Google Scholar] [CrossRef]
- Fernández-González, P.; Koutsou, A.; Cuesta-Gómez, A.; Carratalá-Tejada, M.; Miangolarra-Page, J.C.; Molina-Rueda, F. Reliability of Kinovea® Software and Agreement with a Three-Dimensional Motion System for Gait Analysis in Healthy Subjects. Sensors 2020, 20, 3154. [Google Scholar] [CrossRef]
- Piche, E.; Guilbot, M.; Chorin, F.; Guerin, O.; Zory, R.; Gerus, P. Validity and Repeatability of a New Inertial Measurement Unit System for Gait Analysis on Kinematic Parameters: Comparison with an Optoelectronic System. Measurement 2022, 198, 111442. [Google Scholar] [CrossRef]
- Bartoszek, A.; Struzik, A.; Jaroszczuk, S.; Wozniewski, M.; Pietraszewski, B. Comparison of the Optoelectronic BTS Smart System and IMU-Based MyoMotion System for the Assessment of Gait Variables. Acta Bioeng. Biomech. Wroclaw Univ. Technol. 2022, 24, 103–116. [Google Scholar] [CrossRef]
- Muthukrishnan, N.; Abbas, J.J.; Krishnamurthi, N. A Wearable Sensor System to Measure Step-Based Gait Parameters for Parkinson’s Disease Rehabilitation. Sensors 2020, 20, 6417. [Google Scholar] [CrossRef] [PubMed]
- Cimolin, V.; Vismara, L.; Ferraris, C.; Amprimo, G.; Pettiti, G.; Lopez, R.; Galli, M.; Cremascoli, R.; Sinagra, S.; Mauro, A.; et al. Computation of Gait Parameters in Post Stroke and Parkinson’s Disease: A Comparative Study Using RGB-D Sensors and Optoelectronic Systems. Sensors 2022, 22, 824. [Google Scholar] [CrossRef] [PubMed]
- Vítečková, S.; Horáková, H.; Poláková, K.; Krupička, R.; Růžička, E.; Brožová, H. Agreement between the GAITRite® System and the Wearable Sensor BTS G-Walk® for Measurement of Gait Parameters in Healthy Adults and Parkinson’s Disease Patients. PeerJ 2020, 8, e8835. [Google Scholar] [CrossRef] [PubMed]
- Tomlinson, C.L.; Stowe, R.; Patel, S.; Rick, C.; Gray, R.; Clarke, C.E. Systematic Review of Levodopa Dose Equivalency Reporting in Parkinson’s Disease. Mov. Disord. 2010, 25, 2649–2653. [Google Scholar] [CrossRef] [PubMed]
- Davis, R.B.; Õunpuu, S.; Tyburski, D.; Gage, J.R. A Gait Analysis Data Collection and Reduction Technique. Hum. Mov. Sci. 1991, 10, 575–587. [Google Scholar] [CrossRef]
- Ricciardi, C.; Amboni, M.; De Santis, C.; Ricciardelli, G.; Improta, G.; D’Addio, G.; Cuoco, S.; Picillo, M.; Barone, P.; Cesarelli, M. Machine Learning Can Detect the Presence of Mild Cognitive Impairment in Patients Affected by Parkinson’s Disease. In Proceedings of the 2020 IEEE International Symposium on Medical Measurements and Applications (MeMeA), Bari, Italy, 1 June–1 July 2020; pp. 1–6. [Google Scholar]
- Landolfi, A.; Ricciardi, C.; Donisi, L.; Cesarelli, G.; Troisi, J.; Vitale, C.; Barone, P.; Amboni, M. Machine Learning Approaches in Parkinson’s Disease. Curr. Med. Chem. 2021, 28, 6548–6568. [Google Scholar] [CrossRef]
- Blair, R.C.; Cole, S. Two-Sided Equivalence Testing of the Difference Between Two Means. J. Mod. Appl. Stat. Methods 2002, 1, 18. [Google Scholar] [CrossRef]
- Passing, H.; Bablok, W. A New Biometrical Procedure for Testing the Equality of Measurements from Two Different Analytical Methods. Application of linear regression procedures for method comparison studies in Clinical Chemistry, Part I. Clin. Chem. Lab. Med. (CCLM) 1983, 21, 709–720. [Google Scholar] [CrossRef]
- Benchoufi, M.; Matzner-Lober, E.; Molinari, N.; Jannot, A.-S.; Soyer, P. Interobserver Agreement Issues in Radiology. Diagn. Interv. Imaging 2020, 101, 639–641. [Google Scholar] [CrossRef]
- Ludbrook, J. Confidence in Altman–Bland Plots: A Critical Review of the Method of Differences. Clin. Exp. Pharmacol. Physiol. 2010, 37, 143–149. [Google Scholar] [CrossRef]
- Mansournia, M.A.; Waters, R.; Nazemipour, M.; Bland, M.; Altman, D.G. Bland-Altman Methods for Comparing Methods of Measurement and Response to Criticisms. Glob. Epidemiol. 2021, 3, 100045. [Google Scholar] [CrossRef] [PubMed]
- Sotirakis, C.; Conway, N.; Su, Z.; Villarroel, M.; Tarassenko, L.; FitzGerald, J.J.; Antoniades, C.A. Longitudinal Monitoring of Progressive Supranuclear Palsy Using Body-Worn Movement Sensors. Mov. Disord. 2022, 37, 2263–2271. [Google Scholar] [CrossRef] [PubMed]
- Dale, M.L.; Prewitt, A.L.; Harker, G.R.; McBarron, G.E.; Mancini, M. Perspective: Balance Assessments in Progressive Supranuclear Palsy: Lessons Learned. Front. Neurol. 2022, 13, 801291. [Google Scholar] [CrossRef] [PubMed]
Clinical Parameters | Mean ± SD |
---|---|
Age (years) | 68.13 ± 4.97 |
Disease duration (years) | 3.13 ± 2.07 |
PSP-RS limb | 3.33 ± 2.29 |
PSP-RS gait/midline | 5.20 ± 4.78 |
LEDD (mg) | 322.00 ± 177.13 |
BMI (kg/m2) | 27.48 ± 3.84 |
Spatiotemporal Parameters | BTS SMART DX System | Opal System | p-Value | Test Type |
---|---|---|---|---|
Cadence (steps/min) | 91.72 ± 14.23 | 99.14 ± 14.28 | 0.002 | Wilcoxon test |
Cycle duration (s) | 1.36 ± 0.33 | 1.21 ± 0.30 | 0.003 | Wilcoxon test |
Speed (m/s) | 0.61 ± 0.20 | 0.65 ± 0.19 | 0.192 | Wilcoxon test |
Stance phase (% gait cycle time) | 63.96 ± 2.92 | 62.12 ± 2.11 | 0.037 | Wilcoxon test |
Swing phase (% gait cycle time) | 36.83 ± 3.92 | 36.88 ± 2.11 | 0.159 | Wilcoxon test |
Stride length (m) | 0.41 ± 0.10 | 0.78 ± 0.20 | <0.001 | T-Student test |
Spatiotemporal Parameters | m * | LB_m | UB_m | q ** | LB_q | UB_q |
---|---|---|---|---|---|---|
Cadence (steps/min) | 1.09 | 0.74 | 1.81 | −3.02 | −67.89 | 30.17 |
Cycle duration (s) | 1.03 | 0.63 | 1.74 | −0.10 | −1.04 | 0.40 |
Speed (m/s) | 1.02 | 0.71 | 1.45 | 0.05 | −0.17 | 0.22 |
Stance phase (% gait cycle time) | 0.63 | 0.46 | 0.85 | 23.09 | 8.78 | 33.34 |
Swing phase (% gait cycle time) | 0.58 | 0.32 | 0.74 | 15.96 | 10.13 | 25.68 |
Stride length (m) | 2.10 | 1.64 | 2.69 | −0.06 | −0.28 | 0.13 |
Spatiotemporal Parameters | Bias | LB_b | UB_b | LB_LA | UB_LA |
---|---|---|---|---|---|
Cadence (steps/min) | −7.43 | −11.36 | −3.50 | −28.95 | 14.10 |
Cycle duration (s) | 0.15 | 0.05 | 0.25 | −0.40 | 0.70 |
Speed (m/s) | −0.03 | −0.08 | 0.02 | −0.31 | 0.25 |
Stance phase (% gait cycle time) | 0.84 | 0.11 | 1.57 | −3.17 | 4.84 |
Swing phase (% gait cycle time) | −0.05 | −1.37 | 1.27 | −7.30 | 7.20 |
Stride length (m) | −0.37 | −0.42 | −0.32 | −0.63 | −0.11 |
Spatiotemporal Parameters | Level of Agreement | Error Types |
---|---|---|
Cadence (steps/min) | Very close agreement | Constant systematic error |
Cycle duration (s) | Very close agreement | Constant systematic error |
Speed (m/s) | Agreement | / |
Stance phase (% gait cycle time) | No agreement | Constant and proportional systematic errors |
Swing phase (% gait cycle time) | No agreement | Constant and proportional systematic errors |
Stride length (m) | No agreement | Constant and proportional systematic errors |
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Ricciardi, C.; Pisani, N.; Donisi, L.; Abate, F.; Amboni, M.; Barone, P.; Picillo, M.; Cesarelli, M.; Amato, F. Agreement between Optoelectronic System and Wearable Sensors for the Evaluation of Gait Spatiotemporal Parameters in Progressive Supranuclear Palsy. Sensors 2023, 23, 9859. https://doi.org/10.3390/s23249859
Ricciardi C, Pisani N, Donisi L, Abate F, Amboni M, Barone P, Picillo M, Cesarelli M, Amato F. Agreement between Optoelectronic System and Wearable Sensors for the Evaluation of Gait Spatiotemporal Parameters in Progressive Supranuclear Palsy. Sensors. 2023; 23(24):9859. https://doi.org/10.3390/s23249859
Chicago/Turabian StyleRicciardi, Carlo, Noemi Pisani, Leandro Donisi, Filomena Abate, Marianna Amboni, Paolo Barone, Marina Picillo, Mario Cesarelli, and Francesco Amato. 2023. "Agreement between Optoelectronic System and Wearable Sensors for the Evaluation of Gait Spatiotemporal Parameters in Progressive Supranuclear Palsy" Sensors 23, no. 24: 9859. https://doi.org/10.3390/s23249859
APA StyleRicciardi, C., Pisani, N., Donisi, L., Abate, F., Amboni, M., Barone, P., Picillo, M., Cesarelli, M., & Amato, F. (2023). Agreement between Optoelectronic System and Wearable Sensors for the Evaluation of Gait Spatiotemporal Parameters in Progressive Supranuclear Palsy. Sensors, 23(24), 9859. https://doi.org/10.3390/s23249859