Distinguishing Parkinson’s Disease with GLCM Features from the Hankelization of EEG Signals
Abstract
:1. Introduction
2. Materials and Methods
2.1. Datasets
2.2. Preprocessing
2.3. Feature Extraction and Selection
2.4. Classification
2.4.1. Feed-Forward Network
2.4.2. Support Vector Machine
2.4.3. K-Nearest Neighbor
2.4.4. Cross-Validation
2.4.5. Leave One out Cross-Validation
2.5. Performance Parameters
3. Results
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Donaldson, I.M. James Parkinson’s essay on the shaking palsy. J. R. Coll. Physicians Edinb. 2015, 45, 84–86. [Google Scholar] [CrossRef] [PubMed]
- de Lau, L.M.; Breteler, M.M. Epidemiology of Parkinson’s disease. Lancet Neurol. 2006, 5, 525–535. [Google Scholar] [CrossRef]
- Telarović, S. Epidemiology of Parkinson’s Disease. Arch. Psychiatry Res. 2023, 59, 147–148. [Google Scholar] [CrossRef]
- World Health Organization. Parkinson Disease. Available online: https://www.who.int/news-room/fact-sheets/detail/parkinson-disease (accessed on 5 March 2023).
- Parkinson’s Foundation. Understanding Parkinson’s Statistics. Available online: https://www.parkinson.org/understanding-parkinsons/statistics (accessed on 5 March 2023).
- Li, K.; Ao, B.; Wu, X.; Wen, Q.; Ul Haq, E.; Yin, J. Parkinson’s disease detection and classification using EEG based on deep CNN-LSTM model. Biotechnol. Genet. Eng. Rev. 2023, 1–20. [Google Scholar] [CrossRef] [PubMed]
- Akbayır, E.; Şen, M.; Ay, U.; Şenyer, S.; Tüzün, E.; Küçükali, C.İ. Parkinson Hastalığının Etyopatogenezi. Deney. Tip Derg. 2017, 7, 1–23. [Google Scholar]
- 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, 86, 566–576. [Google Scholar] [CrossRef]
- Qiu, L.; Li, J.; Pan, J. Parkinson’s disease detection based on multi-pattern analysis and multi-scale convolutional neural networks. Front. Neurosci. 2022, 16, 957181. [Google Scholar] [CrossRef]
- Kingdom, Parkinson’s Disease Society of the United. Types of Parkinsonism. Available online: https://www.parkinsons.org.uk/information-and-support/types-parkinsonism (accessed on 4 April 2023).
- Feraco, P.; Gagliardo, C.; La Tona, G.; Bruno, E.; D’Angelo, C.; Marrale, M.; Del Poggio, A.; Malaguti, M.C.; Geraci, L.; Baschi, R.; et al. Imaging of Substantia Nigra in Parkinson’s Disease: A Narrative Review. Brain Sci. 2021, 11, 769. [Google Scholar] [CrossRef]
- Brooks, D.J. Imaging approaches to Parkinson disease. J. Nucl. Med. 2010, 51, 596–609. [Google Scholar] [CrossRef]
- Tolosa, E.; Wenning, G.; Poewe, W. The diagnosis of Parkinson’s disease. Lancet Neurol. 2006, 5, 75–86. [Google Scholar] [CrossRef]
- Oueslati, A. Implication of Alpha-Synuclein Phosphorylation at S129 in Synucleinopathies: What Have We Learned in the Last Decade? J. Park. Dis. 2016, 6, 39–51. [Google Scholar] [CrossRef]
- Anjum, M.F.; Dasgupta, S.; Mudumbai, R.; Singh, A.; Cavanagh, J.F.; Narayanan, N.S. Linear predictive coding distinguishes spectral EEG features of Parkinson’s disease. Park. Relat. Disord. 2020, 79, 79–85. [Google Scholar] [CrossRef] [PubMed]
- Ananthi, A.; Subathra, M.S.P.; George, S.T.; Prasanna, J. A review on-EEG signals by motor imagery based brain computer interface. AIP Conf. Proc. 2022, 2670, 020010. [Google Scholar] [CrossRef]
- Tinkhauser, G.; Pogosyan, A.; Tan, H.; Herz, D.M.; Kuhn, A.A.; Brown, P. Beta burst dynamics in Parkinson’s disease OFF and ON dopaminergic medication. Brain 2017, 140, 2968–2981. [Google Scholar] [CrossRef] [PubMed]
- Maitín, A.M.; García-Tejedor, A.J.; Muñoz, J.P.R. Machine Learning Approaches for Detecting Parkinson’s Disease from EEG Analysis: A Systematic Review. Appl. Sci. 2020, 10, 8662. [Google Scholar] [CrossRef]
- Wang, Q.; Meng, L.; Pang, J.; Zhu, X.; Ming, D. Characterization of EEG Data Revealing Relationships with Cognitive and Motor Symptoms in Parkinson’s Disease: A Systematic Review. Front. Aging Neurosci. 2020, 12, 587396. [Google Scholar] [CrossRef]
- Maitin, A.M.; Romero Muñoz, J.P.; García-Tejedor, Á.J. Survey of Machine Learning Techniques in the Analysis of EEG Signals for Parkinson’s Disease: A Systematic Review. Appl. Sci. 2022, 12, 6967. [Google Scholar] [CrossRef]
- Haralick, R.M.; Shanmugam, K.; Dinstein, I.H. Textural features for image classification. IEEE Trans. Syst. Man Cybern. 1973, SMC-3, 610–621. [Google Scholar] [CrossRef]
- Gantmacher, F.R.; Brenner, J.L. Applications of the Theory of Matrices; Courier Corporation, Dover Publications Inc.: Mineola, NY, USA, 2005. [Google Scholar]
- Cavanagh, J.F.; Napolitano, A.; Wu, C.; Mueen, A. The Patient Repository for EEG Data + Computational Tools (PRED + CT). Front. Neuroinform. 2017, 11, 67. [Google Scholar] [CrossRef]
- Railo, H.; Suuronen, I.; Kaasinen, V.; Murtojärvi, M.; Pahikkala, T.; Airola, A. Resting state EEG as a biomarker of Parkinson’s disease: Influence of measurement conditions. bioRxiv 2020. [Google Scholar] [CrossRef]
- Delorme, A.; Makeig, S. EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J. Neurosci. Methods 2004, 134, 9–21. [Google Scholar] [CrossRef]
- Makeig, S.; Debener, S.; Onton, J.; Delorme, A. Mining event-related brain dynamics. Trends Cogn. Sci. 2004, 8, 204–210. [Google Scholar] [CrossRef]
- Haralick, R.M.; Shapiro, L.G. Computer and Robot Vision; Addison-Wesley Reading: Boston, MA, USA, 1992; Volume 1. [Google Scholar]
- Soh, L.-K.; Tsatsoulis, C. Texture analysis of SAR sea ice imagery using gray level co-occurrence matrices. IEEE Trans. Geosci. Remote Sens. 1999, 37, 780–795. [Google Scholar] [CrossRef]
- Clausi, D.A. An analysis of co-occurrence texture statistics as a function of grey level quantization. Can. J. Remote Sens. 2002, 28, 45–62. [Google Scholar] [CrossRef]
- Lofstedt, T.; Brynolfsson, P.; Asklund, T.; Nyholm, T.; Garpebring, A. Gray-level invariant Haralick texture features. PLoS ONE 2019, 14, e0212110. [Google Scholar] [CrossRef] [PubMed]
- Glcmfeatures(Glcm) 2.1.1.0, Version 2.1.1.0; MATLAB Central File Exchange. Available online: https://www.mathworks.com/matlabcentral/fileexchange/55034-glcmfeatures-glcm (accessed on 4 March 2023).
- Onwuegbuche, F.C.; Jurcut, D.A.; Pasquale, L. Enhancing Ransomware Classification with Multi-Stage Feature Selection and Data Imbalance Correction. In Proceedings of the 7th International Symposium on Security, Cryptography and Machine Learning, Be’er Sheva, Israel, 29–30 June 2023. [Google Scholar]
- Liu, H.; Setiono, R. Chi2: Feature Selection and Discretization of Numeric Attributes. In Proceedings of the 7th IEEE International Conference on Tools with Artificial Intelligence, Herndon, VA, USA, 5–8 November 1995. [Google Scholar]
- Krogh, A. What are artificial neural networks? Nat. Biotechnol. 2008, 26, 195–197. [Google Scholar] [CrossRef]
- Avuçlu, E. Determining the most accurate machine learning algorithms for medical diagnosis using the monk’problems database and statistical measurements. J. Exp. Theor. Artif. Intell. 2023, 1–20. [Google Scholar] [CrossRef]
- Istiadi, I.; Rahman, A.Y.; Wisnu, A.D.R. Identification of Tempe Fermentation Maturity Using Principal Component Analysis and K-Nearest Neighbor. Sink. J. Dan Penelit. Tek. Inform. 2023, 8, 286–294. [Google Scholar] [CrossRef]
- Chen, D.; Song, Q.; Zhang, Y.; Li, L.; Yang, Z. Identification of Network Traffic Intrusion Using Decision Tree. J. Sens. 2023, 2023, 5997304. [Google Scholar] [CrossRef]
- Refaeilzadeh, P.; Tang, L.; Liu, H. Cross-validation. Encycl. Database Syst. 2009, 5, 532–538. [Google Scholar]
- Shah, D.; Gopika, G.K.; Sinha, N. Analysis of EEG for Parkinson’s Disease Detection. In Proceedings of the 2022 IEEE International Conference on Signal Processing and Communications (SPCOM), Bangalore, India, 11–15 July 2022; pp. 1–5. [Google Scholar]
- Kurbatskaya, A.; Jaramillo-Jimenez, A.; Ochoa-Gomez, J.F.; Brønnick, K.; Fernandez-Quilez, A. Machine Learning-Based Detection of Parkinson’s Disease From Resting-State EEG: A Multi-Center Study. arXiv 2023, arXiv:2303.01389. [Google Scholar]
- Suuronen, I.; Airola, A.; Pahikkala, T.; Murtojarvi, M.; Kaasinen, V.; Railo, H. Budget-based classification of Parkinson’s disease from resting state EEG. IEEE J. Biomed. Health Inform. 2023, 1–9. [Google Scholar] [CrossRef] [PubMed]
- Chaturvedi, M.; Hatz, F.; Gschwandtner, U.; Bogaarts, J.G.; Meyer, A.; Fuhr, P.; Roth, V. Quantitative EEG (QEEG) Measures Differentiate Parkinson’s Disease (PD) Patients from Healthy Controls (HC). Front. Aging Neurosci. 2017, 9, 3. [Google Scholar] [CrossRef] [PubMed]
- Sugden, R.; Diamandis, P. Generalizable electroencephalographic classification of Parkinson’s Disease using deep learning. medRxiv 2022. [Google Scholar] [CrossRef]
- Shabanpour, M.; Kaboodvand, N.; Iravani, B. Parkinson’s disease is characterized by sub-second resting-state spatio-oscillatory patterns: A contribution from deep convolutional neural network. Neuroimage Clin. 2022, 36, 103266. [Google Scholar] [CrossRef] [PubMed]
- Vanneste, S.; Song, J.J.; De Ridder, D. Thalamocortical dysrhythmia detected by machine learning. Nat. Commun. 2018, 9, 1103. [Google Scholar] [CrossRef]
- Yuvaraj, R.; Acharya, U.R.; Hagiwara, Y. A novel Parkinson’s Disease Diagnosis Index using higher-order spectra features in EEG signals. Neural Comput. Appl. 2016, 30, 1225–1235. [Google Scholar] [CrossRef]
- Lee, S.B.; Kim, Y.J.; Hwang, S.; Son, H.; Lee, S.K.; Park, K.I.; Kim, Y.G. Predicting Parkinson’s disease using gradient boosting decision tree models with electroencephalography signals. Park. Relat. Disord. 2022, 95, 77–85. [Google Scholar] [CrossRef]
- Aljalal, M.; Aldosari, S.A.; Molinas, M.; AlSharabi, K.; Alturki, F.A. Detection of Parkinson’s disease from EEG signals using discrete wavelet transform, different entropy measures, and machine learning techniques. Sci. Rep. 2022, 12, 22547. [Google Scholar] [CrossRef]
- Avvaru, S.; Parhi, K.K. Effective Brain Connectivity Extraction by Frequency-Domain Convergent Cross-Mapping (FDCCM) and its Application in Parkinson’s Disease Classification. IEEE Trans. Biomed. Eng. 2023, 1–11. [Google Scholar] [CrossRef]
- Lee, S.; Hussein, R.; Ward, R.; Jane Wang, Z.; McKeown, M.J. A convolutional-recurrent neural network approach to resting-state EEG classification in Parkinson’s disease. J. Neurosci. Methods 2021, 361, 109282. [Google Scholar] [CrossRef] [PubMed]
- Aljalal, M.; Aldosari, S.A.; AlSharabi, K.; Abdurraqeeb, A.M.; Alturki, F.A. Parkinson’s Disease Detection from Resting-State EEG Signals Using Common Spatial Pattern, Entropy, and Machine Learning Techniques. Diagnostics 2022, 12, 1033. [Google Scholar] [CrossRef] [PubMed]
Data Source | Dataset | Eyes Condition | Drug Condition |
---|---|---|---|
UNM | UNM_ALL | Open/Closed | On |
UNM_OPEN | Open | On | |
UNM_CLOSED | Closed | On | |
UNM_OFF | Open/Closed | Off | |
UI | UI | Open/Closed | On |
UT | UT_OPEN | Open | Off |
UT_CLOSED | Closed | Off |
(Mean ± STD) | UNM | UI | UT | |||
---|---|---|---|---|---|---|
Condition | PD | Control | PD | Control | PD | Control |
Sex | 17 M/10 F | 17 M/10 F | 6 M/8 F | 6 M/8 F | 9 M/11 F | 8 M/12 F |
Age | 69.5 ± 8.7 | 69.5 ± 9.3 | 70.5 ± 8.7 | 70.5 ± 8.7 | 69.8 ± 7.2 | 67.8 ± 6.2 |
MMSE | 28.7 ± 1 | 28.8 ± 1 | - | - | 27.8 ± 1.8 | 28.2 ± 1.5 |
MOCA | - | - | 25.9 ± 2.7 | 27.2 ± 1.7 | - | - |
UPDRS | 22.2 ± 10.3 | - | 13.4 ± 6.6 | - | 28.9 ± 16.4 | 5.1 ± 3.5 |
Years from Diagnosis | 5.7 ± 4.2 | - | 5.6 ± 3.2 | - | 6.4(4.9) | - |
Recording Minute | 3.59 ± 1 | 3.63 ± 1.8 | 3.11 ± 1.2 | 3.17 ± 0.9 | 2.55 ± 0.06 | 2.51 ± 0.2 |
BDI | 7.6 ± 5.3 | 4.8 ± 4.8 | - | - | 8.4 ± 6.2 | 5.0 ± 3.0 |
LED | 707.4 ± 448.6 | - | 796 ± 409 | - | 663.2 ± 509.1 | - |
NAART | 45.2 ± 10.3 | 47.1 ± 7.5 | - | - | - | - |
FF | SVM | KNN |
---|---|---|
Layer Size = [10] Activation Function = Relu | Kernel Function = Linear Kernel Scale = 1 Box Constraint = 1 | 1 Neighbor Euclidean Distance |
AUC | ACC | SENS | SPEC | PPV | NPV | |
---|---|---|---|---|---|---|
UNM_All | 92.84 | 92.41 | 92.96 | 91.85 | 91.96 | 92.96 |
(91.08–94.24) | (90.74–94.44) | (88.89–96.3) | (88.89–92.59) | (89.29–92.86) | (89.29–96.15) | |
UNM_Closed | 94.44 | 89.07 | 90 | 88.15 | 88.38 | 89.84 |
(92.18–95.47) | (87.04–90.74) | (88.89–92.59) | (85.19–88.89) | (85.71–89.29) | (88.46–92.31) | |
UNM_Open | 94.9 | 89.44 | 89.63 | 89.26 | 89.46 | 89.66 |
(92.87–95.61) | (87.04–94.44) | (85.19–92.59) | (85.19–96.3) | (85.71–96.15) | (85.71–92.86) | |
UNM_Off | 90.66 | 83.89 | 88.15 | 79.63 | 81.34 | 87.16 |
(87.93–92.46) | (79.63–87.04) | (81.48–92.59) | (70.37–85.19) | (75.76–85.71) | (80.77–91.67) | |
UI | 87.4 | 85.71 | 94.29 | 77.14 | 80.5 | 93.31 |
(82.14–89.8) | (82.14–89.29) | (85.71–100) | (71.43–78.57) | (76.47–82.35) | (84.62–100) | |
UT_Closed | 84 | 77.18 | 73 | 81.58 | 80.86 | 74.45 |
(77.37–88.95) | (66.67–84.62) | (60–85) | (68.42–89.47) | (70–88.89) | (63.64–84.21) | |
UT_Open | 67.85 | 63.25 | 77 | 49.5 | 60.49 | 68.26 |
(64.75–71.25) | (60–67.5) | (70–80) | (40–55) | (57.14–64) | (62.5–73.33) |
AUC | ACC | SENS | SPEC | PPV | NPV | |
---|---|---|---|---|---|---|
UNM_All | 94.39 | 93.7 | 93.22 | 94.16 | 94.16 | 93.51 |
(87.72–100) | (90.74–98.15) | (88–100) | (88.89–100) | (88.46–100) | (88.46–100) | |
UNM_Closed | 94.11 | 89.26 | 92.22 | 86.23 | 87.26 | 91.68 |
(89.71–96.98) | (83.33–92.59) | (88–96.15) | (74.07–96) | (78.13–96.3) | (88.89–96.67) | |
UNM_Open | 94.55 | 87.04 | 86.23 | 87.76 | 86.88 | 87.23 |
(90.67–98.32) | (77.78–92.59) | (72–96.3) | (81.25–95.83) | (72.73–96.43) | (78.79–96) | |
UNM_Off | 91.07 | 83.33 | 87.99 | 78.53 | 80.45 | 87.29 |
(83.68–95.45) | (72.22–88.89) | (74.07–96.3) | (70.37–90.63) | (71.43–88.89) | (73.08–95) | |
UI | 85.21 | 82.5 | 88.9 | 75.35 | 79.42 | 85.82 |
(78.06–96.11) | (75–92.86) | (78.57–100) | (57.14–94.44) | (66.67–93.75) | (71.43–100) | |
UT_Closed | 83.21 | 76.92 | 73.97 | 80.65 | 80.57 | 73.07 |
(72.86–91.3) | (66.67–84.62) | (64–85.71) | (70–93.75) | (66.67–94.12) | (52.63–90.48) | |
UT_Open | 61.93 | 59.75 | 78.61 | 41.53 | 55.29 | 68.31 |
(39.64–80.3) | (45–75) | (47.06–89.47) | (23.53–68.18) | (38.1–68.18) | (50–83.33) |
UNM_All | UI | UT_Closed | |||
---|---|---|---|---|---|
Shah et al. [39] | 88.5 | Qiu et al. [9] | 96.31 | Kurbatskaya et al. [40] | 82.2 |
Anjum et al. [15] | 85.2 | Anjum et al. [15] | 85.7 | Suuronen et al. [41] | 76 |
Chaturverdi et al. [42] | 72.2 | Sugden et al. [43] | 83.8 | Shabanpour et al. [44] | 63.44 |
Vanneste et al. [45] | 72.2 | Proposed | 85.71 | Proposed | 76.92 |
Yuvaraj et al. [46] | 59.3 | ||||
Lee et al. [47] | 89.3 | ||||
Sugden et al. [43] | 69.2 | ||||
Aljalal et al. [48] | 87.04 | ||||
Avvaru et al. [49] | 79.25 | ||||
Proposed | 93.7 |
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Karakaş, M.F.; Latifoğlu, F. Distinguishing Parkinson’s Disease with GLCM Features from the Hankelization of EEG Signals. Diagnostics 2023, 13, 1769. https://doi.org/10.3390/diagnostics13101769
Karakaş MF, Latifoğlu F. Distinguishing Parkinson’s Disease with GLCM Features from the Hankelization of EEG Signals. Diagnostics. 2023; 13(10):1769. https://doi.org/10.3390/diagnostics13101769
Chicago/Turabian StyleKarakaş, Mehmet Fatih, and Fatma Latifoğlu. 2023. "Distinguishing Parkinson’s Disease with GLCM Features from the Hankelization of EEG Signals" Diagnostics 13, no. 10: 1769. https://doi.org/10.3390/diagnostics13101769
APA StyleKarakaş, M. F., & Latifoğlu, F. (2023). Distinguishing Parkinson’s Disease with GLCM Features from the Hankelization of EEG Signals. Diagnostics, 13(10), 1769. https://doi.org/10.3390/diagnostics13101769