Fusing convolutional learning and attention-based Bi-LSTM networks for early Alzheimer's diagnosis from EEG signals towards IoMT.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
29 10 2024
Historique:
received: 14 06 2024
accepted: 25 10 2024
medline: 30 10 2024
pubmed: 30 10 2024
entrez: 30 10 2024
Statut: epublish

Résumé

The Internet of Medical Things (IoMT) is poised to play a pivotal role in future medical support systems, enabling pervasive health monitoring in smart cities. Alzheimer's disease (AD) afflicts millions globally, and this paper explores the potential of electroencephalogram (EEG) data in addressing this challenge. We propose the Convolutional Learning Attention-Bidirectional Time-Aware Long-Short-Term Memory (CL-ATBiLSTM) model, a deep learning approach designed to classify different AD phases through EEG data analysis. The model utilizes Discrete Wavelet Transform (DWT) to decompose EEG data into distinct frequency bands, allowing for targeted analysis of AD-related brain activity patterns. Additionally, the data is segmented into smaller windows to handle the dynamic nature of EEG signals, and these segments are transformed into spectrogram images, visually depicting brain activity distribution over time and frequency. The CL-ATBiLSTM model incorporates convolutional layers to capture spatial features, attention mechanisms to emphasize crucial data, and BiLSTM networks to explore temporal relationships within the sequences. To optimize the model's performance, Bayesian optimization is employed to fine-tune the hyperparameters of the ATBiLSTM network, enhancing its ability to generalize and accurately classify AD stages. Incorporating Bayesian learning ensures the most effective model configuration, improving sensitivity and specificity for identifying AD-related patterns. Our model extracts discriminative features from EEG data to differentiate between AD, Mild Cognitive Impairment (MCI), and healthy controls (CO), offering a more comprehensive approach than existing two-class detection algorithms. By including the MCI category, our method facilitates earlier identification and potentially more impactful therapy interventions. Achieving a 96.52% accuracy on Figshare datasets containing AD, MCI, and CO groups, our approach demonstrates strong potential for practical use, accelerating AD identification, enhancing patient care, and contributing to the development of targeted treatments for this debilitating condition.

Identifiants

pubmed: 39472526
doi: 10.1038/s41598-024-77876-8
pii: 10.1038/s41598-024-77876-8
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

26002

Informations de copyright

© 2024. The Author(s).

Références

Perez-Valero, E., Lopez-Gordo, M. Á., Gutiérrez, C. M., Carrera-Muñoz, I. & Vílchez-Carrillo, R. M. <ArticleTitle Language=“En”>A self-driven approach for multi-class discrimination in Alzheimer’s disease based on wearable EEG. Comput. Biol. Med.220, 106841. https://doi.org/10.1016/j.cmpb.2022.106841 (2022).
doi: 10.1016/j.cmpb.2022.106841
Petersen, R. C. Mild cognitive impairment. CONTIN Lifelong Learn. Neurol.22, 404. https://doi.org/10.1212/CON.0000000000000313 (2016).
doi: 10.1212/CON.0000000000000313
Petersen, R. C. et al. Mild cognitive impairment: Clinical characterization and outcome. Arch. Neurol.56 (3), 303–308. https://doi.org/10.1001/archneur.56.3.303 (1999).
doi: 10.1001/archneur.56.3.303 pubmed: 10190820
Dugger, B. N., Tu, M., Murray, M. E., Dickson, D. W. & University of Washington Alzheimer’s Disease Research Center. Neuropathological comparisons of amnestic and nonamnestic mild cognitive impairment. BMC Neurol.15 (1), 1–8. https://doi.org/10.1186/s12883-015-0344-0 (2015).
doi: 10.1186/s12883-015-0344-0
Jessen, F. et al. The characterisation of subjective cognitive decline. Lancet Neurol.19 (3), 271–278. https://doi.org/10.1016/S1474-4422(19)30368-0 (2020).
doi: 10.1016/S1474-4422(19)30368-0 pubmed: 31958406 pmcid: 7062546
Venkata Phanikrishna, B., Prakash, J., Suchismitha, C. & A., & Deep review of machine learning techniques on detection of drowsiness using EEG signal. IETE J. Res.69 (6), 3104–3119. https://doi.org/10.1080/03772063.2021.1913070 (2023).
doi: 10.1080/03772063.2021.1913070
Gawel, M., Zalewska, E., Szmidt-Sałkowska, E. & Kowalski, J. The value of quantitative EEG in differential diagnosis of Alzheimer’s disease and subcortical vascular dementia. J. Neurol. Sci.283 (1–2), 127–133. https://doi.org/10.1016/j.jns.2009.02.332 (2009).
doi: 10.1016/j.jns.2009.02.332 pubmed: 19268969
Oltu, B., Akşahin, M. F. & Kibaroğlu, S. A novel electroencephalography based approach for Alzheimer’s disease and mild cognitive impairment detection. Biomed. Signal Process. Control. 63, 102223. https://doi.org/10.1016/j.bspc.2020.102223 (2021).
doi: 10.1016/j.bspc.2020.102223
Azami, H. et al. Beta to theta power ratio in EEG periodic components as a potential biomarker in mild cognitive impairment and Alzheimer’s dementia. Alzheimers Res. Ther.15 (1), 1–12. https://doi.org/10.1186/S13195-023-01280-Z/FIGURES/5 (2023).
doi: 10.1186/S13195-023-01280-Z/FIGURES/5
Li, R. X., Ma, Y. H., Tan, L., Yu, J. T. & Prospective biomarkers of Alzheimer’s disease: A systematic review and meta-analysis. Ageing Res. Rev.81, 101699. https://doi.org/10.1016/J.ARR.2022.101699 (2022).
doi: 10.1016/J.ARR.2022.101699 pubmed: 35905816
Khan, P. et al. Machine learning and deep learning approaches for brain disease diagnosis: Principles and recent advances. IEEE Access.9, 37622–37655. https://doi.org/10.1109/ACCESS.2021.3062484 (2021).
doi: 10.1109/ACCESS.2021.3062484
Safi, M. S. & Safi, S. M. M. Early detection of Alzheimer’s disease from EEG signals using Hjorth parameters. Biomed. Signal Process. Control. 65, 102338. https://doi.org/10.1016/J.BSPC.2020.102338 (2021).
doi: 10.1016/J.BSPC.2020.102338
Gong, S., Xing, K., Cichocki, A. & Li, J. Deep learning in EEG: Advance of the last ten-year critical period. IEEE Trans. Cogn. Dev. Syst.14 (2), 348–365. https://doi.org/10.1109/TCDS.2021.3079712 (2021).
doi: 10.1109/TCDS.2021.3079712
Miltiadous, A. et al. Alzheimer’s Disease and Frontotemporal Dementia: A Robust Classification Method of EEG Signals and a Comparison of Validation Methods. Diagnostics. 11 (8), 1437. https://doi.org/10.3390/DIAGNOSTICS11081437 (2021).
doi: 10.3390/DIAGNOSTICS11081437 pubmed: 34441371 pmcid: 8391578
Alsharabi, K., Salamah, B., Abdurraqeeb, Y., Aljalal, A. M., Alturki, F. A. & M., & EEG Signal Processing for Alzheimer’s Disorders Using Discrete Wavelet Transform and Machine Learning Approaches. IEEE Access.10, 89781–89797. https://doi.org/10.1109/ACCESS.2022.3198988 (2022).
doi: 10.1109/ACCESS.2022.3198988
Tautan, A. M. et al. Preliminary study on the impact of EEG density on TMS-EEG classification in Alzheimer’s disease. In: Proceedings of the Annual International Conference of the IEEE Engineering in Medicine and Biology Society, EMBS (Vol. 2022-July, pp. 394–397). (2022). https://doi.org/10.1109/EMBC48229.2022.9870920
Alvi, A. M., Siuly, S. & Wang, H. A long short-term memory based framework for early detection of mild cognitive impairment from EEG signals. IEEE Trans. Emerg. Top. Comput. Intell.7 (2), 375–388. https://doi.org/10.1109/TETCI.2022.3186180 (2022).
doi: 10.1109/TETCI.2022.3186180
Alessandrini, M. et al. EEG-Based Alzheimer’s Disease Recognition Using Robust-PCA and LSTM Recurrent Neural Network. Sensors. 22 (10), 3696. https://doi.org/10.3390/S22103696 (2022).
doi: 10.3390/S22103696 pubmed: 35632105 pmcid: 9145212
Amini, M., Pedram, M. M., Moradi, A. R. & Ouchani, M. Diagnosis of Alzheimer’s Disease by Time-Dependent Power Spectrum Descriptors and Convolutional Neural Network Using EEG Signal. Computational and Mathematical Methods in Medicine, 2021. (2021). https://doi.org/10.1155/2021/5511922
Senturk, U., Polat, K. & Yucedag, I. A non-invasive continuous cuffless blood pressure estimation using dynamic Recurrent Neural Networks. Appl. Acoust.170, 107534. https://doi.org/10.1016/J.APACOUST.2020.107534 (2020).
doi: 10.1016/J.APACOUST.2020.107534
Sharma, G., Parashar, A. & Joshi, A. M. DepHNN: A novel hybrid neural network for electroencephalogram (EEG)-based screening of depression. Biomed. Signal Process. Control. 66, 102393. https://doi.org/10.1016/J.BSPC.2020.102393 (2021).
doi: 10.1016/J.BSPC.2020.102393
Klepl, D., He, F., Wu, M., Blackburn, D. J. & Sarrigiannis, P. G. Apr. Adaptive Gated Graph Convolutional Network for Explainable Diagnosis of Alzheimer’s Disease using EEG Data. Accessed: May 26, 2023. [Online]. Available: (2023). https://arxiv.org/abs/2304.05874v1
Shikalgar, A. & Sonavane, S. Hybrid Deep Learning Approach for Classifying Alzheimer Disease Based on Multimodal Data. Adv. Intell. Syst. Comput., 1025, 511–520. https://doi.org/10.1007/978-981-32-9515-5_49/COVER (2020).
Fouladi, S., Safaei, A. A., Mammone, N., Ghaderi, F. & Ebadi, M. J. Efficient Deep Neural Networks for Classification of Alzheimer’s Disease and Mild Cognitive Impairment from Scalp EEG Recordings. Cogn. Comput.14 (4), 1247–1268. https://doi.org/10.1007/S12559-022-10033-3 (2022).
doi: 10.1007/S12559-022-10033-3
Huggins, C. J. et al. Deep learning of resting-state electroencephalogram signals for three-class classification of Alzheimer’s disease, mild cognitive impairment and healthy ageing. J. Neural Eng.18 (4), 046087. https://doi.org/10.1088/1741-2552/AC05D (2021).
doi: 10.1088/1741-2552/AC05D
Ambeth Kumar, V. D. et al. An Internet of Medical Things-Based Mental Disorder Prediction System Using EEG Sensor and Big Data Mining. J. Circuits Syst. Computers, 2450197. https://doi.org/10.1142/S0218126624501974 . (2024).
Dahan, F. et al. A smart IoMT based architecture for E-healthcare patient monitoring system using artificial intelligence algorithms. Front. Physiol.14, 1125952. https://doi.org/10.3389/fphys.2023.1125952 (2023).
doi: 10.3389/fphys.2023.1125952 pubmed: 36793418 pmcid: 9923105
Imani, M. Alzheimer’s diseases diagnosis using fusion of high informative BiLSTM and CNN features of EEG signal. Biomed. Signal Process. Control. 86, 105298. https://doi.org/10.1016/J.BSPC.2023.105298 (2023).
doi: 10.1016/J.BSPC.2023.105298
Nobukawa, S. et al. Classification Methods Based on Complexity and Synchronization of Electroencephalography Signals in Alzheimer’s Disease. Front. Psychiatry. 11, 511787. https://doi.org/10.3389/FPSYT.2020.00255/BIBTEX (2020).
doi: 10.3389/FPSYT.2020.00255/BIBTEX
Yu, H., Lei, X., Song, Z., Liu, C. & Wang, J. Supervised Network-Based Fuzzy Learning of EEG Signals for Alzheimer’s Disease Identification. IEEE Trans. Fuzzy Syst.28 (1), 60–71. https://doi.org/10.1109/TFUZZ.2019.2903753 (2020).
doi: 10.1109/TFUZZ.2019.2903753
Bi, X. & Wang, H. Early Alzheimer’s disease diagnosis based on EEG spectral images using deep learning. Neural Netw.114, 119–135. https://doi.org/10.1016/J.NEUNET.2019.02.005 (2019).
doi: 10.1016/J.NEUNET.2019.02.005 pubmed: 30903945
Miltiadous, A., Gionanidis, E., Tzimourta, K. D., Giannakeas, N. & Tzallas, A. T. DICENet: A Novel Convolution-Transformer Architecture for Alzheimer Detection in EEG Signals. IEEE Access.11, 71840–71858. https://doi.org/10.1109/ACCESS.2023.3294618 (2023).
doi: 10.1109/ACCESS.2023.3294618
Lopes, M., Cassani, R. & Falk, T. H. Using CNN saliency maps and EEG modulation spectra for improved and more interpretable machine learning-based alzheimer’s disease diagnosis. Computational Intelligence and Neuroscience, 2023. (2023). https://doi.org/10.1155/2023/3198066
Fouad, I. A., El-Zahraa, F. & Labib, M. Identification of Alzheimer’s disease from central lobe EEG signals utilizing machine learning and residual neural network. Biomed. Signal Process. Control. 86, 105266. https://doi.org/10.1016/J.BSPC.2023.105266 (2023).
doi: 10.1016/J.BSPC.2023.105266
kumar Ravikanti, D. & Saravanan, S. EEGAlzheimer’sNet: Development of transformer-based attention long short term memory network for detecting Alzheimer disease using EEG signal. Biomed. Signal Process. Control. 86, 105318. https://doi.org/10.1016/j.bspc.2023.105318 (2023).
doi: 10.1016/j.bspc.2023.105318
Xie, J. et al. A transformer-based approach combining deep learning network and spatial–temporal information for raw EEG classification. IEEE Trans. Neural Syst. Rehabil Eng.30, 2126–2136. https://doi.org/10.1109/TNSRE.2022.3194600 (2022).
doi: 10.1109/TNSRE.2022.3194600 pubmed: 35914032
Ferri, R. et al. Stacked autoencoders as new models for an accurate Alzheimer’s disease classification support using resting-state EEG and MRI measurements. Clin. Neurophysiol.132 (1), 232–245. https://doi.org/10.1016/j.clinph.2020.09.015 (2021).
doi: 10.1016/j.clinph.2020.09.015 pubmed: 33433332
You, Z., Zeng, R., Lan, X., Ren, H. & Guo, Y. Alzheimer’s disease classification with a cascade neural network. Front. Public. Health. 8, 584387. https://doi.org/10.3389/fpubh.2020.584387 (2020).
doi: 10.3389/fpubh.2020.584387 pubmed: 33251178 pmcid: 7673399
Rad, E. M. et al. Diagnosis of mild Alzheimer’s disease by EEG and ERP signals using linear and nonlinear classifiers. Biomed. Signal Process. Control. 70, 103049. https://doi.org/10.1016/j.bspc.2021.103049 (2021).
doi: 10.1016/j.bspc.2021.103049
Morabito, F. C., Ieracitano, C. & Mammone, N. An explainable artificial intelligence approach to study MCI to AD conversion via HD-EEG processing. Clin. EEG Neurosci. 15500594211063662. https://doi.org/10.1177/15500594211063662 (2021).
Araújo, T., Teixeira, J. P. & Rodrigues, P. M. Smart-data-driven system for Alzheimer disease detection through electroencephalographic signals. Bioengineering. 9 (4), 141. https://doi.org/10.3390/bioengineering9040141 (2022).
doi: 10.3390/bioengineering9040141 pubmed: 35447701 pmcid: 9031324
Nour, M., Senturk, U. & Polat, K. A novel hybrid model in the diagnosis and classification of Alzheimer’s disease using EEG signals: Deep ensemble learning (DEL) approach. Biomed. Signal Process. Control. 89, 105751. https://doi.org/10.1016/j.bspc.2023.105751 (2024).
doi: 10.1016/j.bspc.2023.105751
Siddiqui, M. K., Huang, X., Morales-Menendez, R., Hussain, N. & Khatoon, K. Machine learning based novel cost-sensitive seizure detection classifier for imbalanced EEG data sets. Int. J. Interact. Des. Manuf. (IJIDeM). 14, 1491–1509. https://doi.org/10.1007/s12008-020-00715-3 (2020).
doi: 10.1007/s12008-020-00715-3
Siddiqui, M. K., Morales-Menendez, R., Huang, X. & Hussain, N. A review of epileptic seizure detection using machine learning classifiers. Brain Inf.7 (1), 5. https://doi.org/10.1186/s40708-020-00105-1 (2020).
doi: 10.1186/s40708-020-00105-1
Ieracitano, C., Mammone, N., Hussain, A. & Morabito, F. C. A novel multi-modal machine learning based approach for automatic classification of EEG recordings in dementia. Neural Netw.123, 176–190. https://doi.org/10.1016/j.neunet.2019.12.006 (2020).
doi: 10.1016/j.neunet.2019.12.006 pubmed: 31884180
Song, Z., Deng, B., Wang, J. & Yi, G. An EEG-based systematic explainable detection framework for probing and localizing abnormal patterns in Alzheimer’s disease. J. Neural Eng.19 (3), 036007. https://doi.org/10.1088/1741-2552/ac697d (2022).
doi: 10.1088/1741-2552/ac697d
Zhang, D., Jin, X., Shi, P. & Chew, X. Real-time load forecasting model for the smart grid using bayesian optimized CNN-BiLSTM. Front. Energy Res.11, 1193662. https://doi.org/10.3389/fenrg.2023.1193662 (2023).
doi: 10.3389/fenrg.2023.1193662
Li, H. et al. Automatic electrocardiogram detection and classification using bidirectional long short-term memory network improved by Bayesian optimization. Biomed. Signal Process. Control. 73, 103424. https://doi.org/10.1016/j.bspc.2021.103424 (2022).
doi: 10.1016/j.bspc.2021.103424
Cejnek, M., Vysata, O., Valis, M. & Bukovsky, I. Novelty detection-based approach for Alzheimer’s disease and mild cognitive impairment diagnosis from EEG. Med. Biol. Eng. Comput.59 (11), 2287–2296. https://doi.org/10.1007/s11517-021-02427-6 (2021).
doi: 10.1007/s11517-021-02427-6 pubmed: 34535856 pmcid: 8558189
Fiscon, G. et al. Combining EEG signal processing with supervised methods for Alzheimer’s patients classification. BMC Med. Inf. Decis. Mak.18 (1), 1–10. https://doi.org/10.1186/s12911-018-0613-y (2018).
doi: 10.1186/s12911-018-0613-y
Trambaiolli, L. R., Spolaôr, N., Lorena, A. C., Anghinah, R. & Sato, J. R. Feature selection before EEG classification supports the diagnosis of Alzheimer’s disease. Clin. Neurophysiol.128 (10), 2058–2067. https://doi.org/10.1016/j.clinph.2017.06.251 (2017).
doi: 10.1016/j.clinph.2017.06.251 pubmed: 28866471
Amezquita-Sanchez, J. P., Mammone, N., Morabito, F. C., Marino, S. & Adeli, H. A novel methodology for automated differential diagnosis of mild cognitive impairment and the Alzheimer’s disease using EEG signals. J. Neurosci. Methods. 322, 88–95. https://doi.org/10.1016/j.jneumeth.2019.04.013 (2019).
doi: 10.1016/j.jneumeth.2019.04.013 pubmed: 31055026
Triggiani, A. I. et al. Classification of healthy subjects and Alzheimer’s disease patients with dementia from cortical sources of resting state EEG rhythms: a study using artificial neural networks. Front. NeuroSci.10, 604. https://doi.org/10.3389/fnins.2016.00604 (2017).
doi: 10.3389/fnins.2016.00604 pubmed: 28184183 pmcid: 5266711
Cassani, R. et al. Towards automated electroencephalography-based Alzheimer’s disease diagnosis using portable low-density devices. Biomed. Signal Process. Control. 33, 261–271. https://doi.org/10.1016/j.bspc.2016.12.009 (2017).
doi: 10.1016/j.bspc.2016.12.009
Morabito, F. C. et al. Deep convolutional neural networks for classification of mild cognitive impaired and Alzheimer’s disease patients from scalp EEG recordings. In 2016 IEEE 2nd International Forum on Research and Technologies for Society and Industry Leveraging a better tomorrow (RTSI) (pp. 1–6). (2016)., September https://doi.org/10.1109/RTSI.2016.7740576
Bevilacqua, V. et al. Advanced classification of Alzheimer’s disease and healthy subjects based on EEG markers. In 2015 International Joint Conference on Neural Networks (IJCNN) (pp. 1–5). (2015)., July https://doi.org/10.1109/IJCNN.2015.7280463
Kanda, P. A. M. et al. Clinician’s road map to wavelet EEG as an Alzheimer’s disease biomarker. Clin. EEG Neurosci.45 (2), 104–112. https://doi.org/10.1177/1550059413486272 (2014).
doi: 10.1177/1550059413486272 pubmed: 24131618
Siddiqui, M. K., Islam, M. Z. & Kabir, M. A. Analyzing performance of classification techniques in detecting epileptic seizure. InAdvanced Data Mining and Applications: 13th International Conference, ADMA 2017, Singapore, November 5–6, 2017, Proceedings 13 2017 (pp. 386–398). Springer International Publishing. https://doi.org/10.1007/978-3-319-69179-4_27
Cong, G., Peng, W. C., Zhang, W. E., Li, C. & Sun, A. (eds). Advanced Data Mining and Applications: 13th International Conference, ADMA 2017, Singapore, November 5–6, 2017, Proceedings (Vol. 10604). Springer. (2017). https://doi.org/10.1007/978-3-319-69179-4_27
Saab, K. et al. Towards trustworthy seizure onset detection using workflow notes. npj Digit. Med.7 (1), 42. https://doi.org/10.1038/s41746-024-01008-9 (2024).
doi: 10.1038/s41746-024-01008-9 pubmed: 38383884 pmcid: 10881468
Khosravi, M. et al. EEG signal-based machine learning approaches for Alzheimer’s disease: a review of methodological analysis, EICEEAI 2023, Jordan, Dec. (2023). https://doi.org/10.1109/EICEEAI60672.2023.10590088
Khosravi, M. et al. Dec., A novel EEG-based deep approach for diagnosing Alzheimer’s disease using attention-time-aware LSTM, EICEEAI 2023, Jordan, (2023). https://doi.org/10.1109/EICEEAI60672.2023.10590201

Auteurs

Mohamadreza Khosravi (M)

Department of Medical Physics and Engineering, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran. mohammadr.khosravi@iran.ir.
IT Services, Lidoma Sanat Mehregan Part Ltd., Shiraz 71581, Fars, Iran. mohammadr.khosravi@iran.ir.
Shandong Provincial University Laboratory for Protected Horticulture (SPUL4PH), Weifang University of Science and Technology, Weifang 262700, China. mohammadr.khosravi@iran.ir.

Hossein Parsaei (H)

Department of Medical Physics and Engineering, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran. hparsaei@sums.ac.ir.
Shiraz Neuroscience Research Center, Shiraz University of Medical Sciences, Shiraz, Iran. hparsaei@sums.ac.ir.

Khosro Rezaee (K)

Department of Biomedical Engineering, Meybod University, Meybod, Iran.

Mohammad Sadegh Helfroush (MS)

Department of Electrical Engineering, Shiraz University of Technology, Shiraz, Iran.

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