A multi-expert ensemble system for predicting Alzheimer transition using clinical features

Brain Informatics - Tập 9 - Trang 1-11 - 2022
Mario Merone1, Sebastian Luca D’Addario2,3,4, Pierandrea Mirino2,3,5, Francesca Bertino3, Cecilia Guariglia2,4, Rossella Ventura2,4, Adriano Capirchio5, Gianluca Baldassarre5,6, Massimo Silvetti3, Daniele Caligiore3,5
1Unit of Computer Systems and Bioinformatics, Department of Engineering, Università Campus Bio-Medico di Roma, Rome, Italy
2Department of Psychology, Sapienza University, Rome, Italy
3Computational and Translational Neuroscience Laboratory, Institute of Cognitive Sciences and Technologies, National Research Council (CTNLab-ISTC-CNR), Rome, Italy
4IRCCS, Fondazione Santa Lucia, Rome, Italy
5AI2Life s.r.l., Innovative Start-Up, ISTC-CNR Spin-Off, Rome, Italy
6Laboratory of Embodied Natural and Artificial Intelligence, Institute of Cognitive Sciences and Technologies, National Research Council (LENAI-ISTC-CNR), Rome, Italy

Tóm tắt

Alzheimer’s disease (AD) diagnosis often requires invasive examinations (e.g., liquor analyses), expensive tools (e.g., brain imaging) and highly specialized personnel. The diagnosis commonly is established when the disorder has already caused severe brain damage, and the clinical signs begin to be apparent. Instead, accessible and low-cost approaches for early identification of subjects at high risk for developing AD years before they show overt symptoms are fundamental to provide a critical time window for more effective clinical management, treatment, and care planning. This article proposes an ensemble-based machine learning algorithm for predicting AD development within 9 years from first overt signs and using just five clinical features that are easily detectable with neuropsychological tests. The validation of the system involved both healthy individuals and mild cognitive impairment (MCI) patients drawn from the ADNI open dataset, at variance with previous studies that considered only MCI. The system shows higher levels of balanced accuracy, negative predictive value, and specificity than other similar solutions. These results represent a further important step to build a preventive fast-screening machine-learning-based tool to be used as a part of routine healthcare screenings.

Tài liệu tham khảo

Wolters FJ, Chibnik LB, Waziry R et al (2020) Twenty-seven-year time trends in dementia incidence in Europe and the United States. Neurology 95:e519–e531. https://doi.org/10.1212/WNL.0000000000010022 Zhang XX, Tian Y, Wang ZT et al (2021) The epidemiology of Alzheimer’s disease modifiable risk factors and prevention. J Prev Alzheimer’s Dis 8:313–321 Scheltens P, Strooper BD, Kivipelto M et al (2021) Alzheimer’s disease. Lancet 397:1577–1590 Amieva H, Le Goff M, Millet X et al (2008) Prodromal Alzheimer’s disease: successive emergence of the clinical symptoms. Ann Neurol 64:492–498 Beason-Held LL, Goh JO, An Y et al (2013) Changes in brain function occur years before the onset of cognitive impairment. J Neurosci 33:18008–18014 Rajan KB, Wilson RS, Weuve J et al (2015) Cognitive impairment 18 years before clinical diagnosis of Alzheimer disease dementia. Neurology 85:898–904 Reiman EM, Quiroz YT, Fleisher AS et al (2012) Brain imaging and fluid biomarker analysis in young adults at genetic risk for autosomal dominant Alzheimer’s disease in the presenilin 1 E280A kindred: a case-control study. Lancet Neurol 11:1048–1056 Younes L, Albert M, Moghekar A et al (2019) Identifying changepoints in biomarkers during the preclinical phase of Alzheimer’s disease. Front Aging Neurosci 11:74. https://doi.org/10.3389/FNAGI.2019.00074 Isaacson R, Ganzer C, Hristov H et al (2018) The clinical practice of risk reduction for Alzheimer’s disease: a precision medicine approach. Alzheimer’s & Dementia 14:1663–1673 Yiannopoulou KG, Papageorgiou SG (2020) Current and future treatments in Alzheimer disease: an update. J Cent Nervous Syst Dis. https://doi.org/10.1177/1179573520907397 Matthews FE, Stephan BCM, Robinson L et al (2016) A two decade dementia incidence comparison from the Cognitive Function and Ageing Studies I and II. Nat Commun 7:1–8. https://doi.org/10.1038/ncomms11398 Norton S, Matthews F, Barnes D et al (2014) Potential for primary prevention of Alzheimer’s disease: an analysis of population-based data. Lancet Neurol 13:788–794 Rasmussen J, Langerman H (2019) Alzheimer’s disease—why we need early diagnosis. Degener Neurol Neuromuscul Dis 9:123–130 De Vugt ME, Verhey FR (2013) The impact of early dementia diagnosis and intervention on informal caregivers. Prog Neurobiol 110:54–62 Frias CE, Cabrera E, Zabalegui A (2020) Informal caregivers’ roles in dementia: the impact on their quality of life. Life (Basel) 10:251. https://doi.org/10.3390/life10110251 Petersen R, Parisi J, Dickson D et al (2006) Neuropathologic features of amnestic mild cognitive impairment. Arch Neurol 63:665–672 Roberts R, Knopman D, Mielke M et al (2014) Higher risk of progression to dementia in mild cognitive impairment cases who revert to normal. Neurology 82:317–325 Dukart J, Sambataro F, Bertolino A (2015) Accurate prediction of conversion to Alzheimer’s disease using imaging, genetic, and neuropsychological biomarkers. J Alzheimer’s Dis 49:1143–1159 Caligiore D, Silvetti M, D’Amelio M et al (2020) Computational modeling of catecholamines dysfunction in Alzheimer’s disease at pre-plaque stage. J Alzheimer’s Dis 77:275–290 Grassi M, Rouleaux N, Caldirola D et al (2019) A novel ensemble-based machine learning algorithm to predict the conversion from mild cognitive impairment to Alzheimer’s disease using socio-demographic characteristics, clinical information, and neuropsychological measures. Front Neurol 10:756. https://doi.org/10.3389/fneur.2019.00756 Moustafa AA (2021) Alzheimer’s disease : understanding biomarkers, big data, and therapy. Academic Press, London. ISBN 978-0-12-821334-6 Hampel H, Vergallo A, Perry G et al (2019) The Alzheimer precision medicine initiative. J Alzheimer’s Dis 68:1–24 Perna G, Grassi M, Caldirola D et al (2018) The revolution of personalized psychiatry: will technology make it happen sooner? Psychol Med 48:705–713 Grassi M, Perna G, Caldirola D et al (2018) A clinically-translatable machine learning algorithm for the prediction of Alzheimer’s disease conversion in individuals with mild and premild cognitive impairment. J Alzheimer’s Dis 61:1555–1573 Hojjati S, Ebrahimzadeh A, Khazaee A et al (2017) Predicting conversion from MCI to AD using resting-state fMRI, graph theoretical approach and SVM. J Neurosci Methods 282:69–80 Liu M, Cheng D, Wang K et al (2018) Multi-modality cascaded convolutional neural networks for Alzheimer’s disease diagnosis. Neuroinformatics 16:295–308 Long X, Chen L, Jiang C et al (2017) Prediction and classification of Alzheimer disease based on quantification of MRI deformation. PLOS ONE 12:e0173372. https://doi.org/10.1371/JOURNAL.PONE.0173372 Pan D, Zeng A, Jia L et al (2020) Early detection of Alzheimer’s disease using magnetic resonance imaging: a novel approach combining convolutional neural networks and ensemble learning. Front Neurosci 14:259. https://doi.org/10.3389/fnins.2020.00259 Platero C, Lin L, Tobar MC (2019) Longitudinal neuroimaging hippocampal markers for diagnosing Alzheimer’s disease. Neuroinformatics 17:43–61 Grueso S, Viejo-Sobera R (2021) Machine learning methods for predicting progression from mild cognitive impairment to Alzheimer’s disease dementia: a systematic review. Alzheimer’s Res Ther 13:1–29 Pradhan N, Singh AS, Singh A (2021) Alzheimer disease early diagnosis and prediction using deep learning techniques: a survey. In: Recent trends in communication and electronics, pp 590–593 Odusami M, Maskeliūnas R, Damaševičius R et al (2021) Analysis of features of Alzheimer’s disease: detection of early stage from functional brain changes in magnetic resonance images using a Finetuned ResNet18 Network. Diagnostics 11:1071. https://doi.org/10.3390/diagnostics11061071 Beltran J, Wahba B, Hose N et al (2020) Inexpensive, non-invasive biomarkers predict Alzheimer transition using machine learning analysis of the Alzheimer’s Disease Neuroimaging (ADNI) database. PLoS ONE 15:e0235663 Cammisuli DM, Cipriani G, Castelnuovo G (2022) Technological solutions for diagnosis, management and treatment of Alzheimer’s disease-related symptoms: a structured review of the recent scientific literature. Int J Environ Res Public Health. https://doi.org/10.3390/IJERPH19053122 Odusami M, Maskeliūnas R, Damaševičius R (2022) An intelligent system for early recognition of Alzheimerrsquo;s disease using neuroimaging. Sensors. https://doi.org/10.3390/S22030740 Silva-Spínola A, Baldeiras I, Arrais JP et al (2022) The road to personalized medicine in Alzheimer’s disease: the use of artificial intelligence. Biomedicines. https://doi.org/10.3390/BIOMEDICINES10020315 Khanna S, Domingo-Fernández D, Iyappan A et al (2018) Using multi-scale genetic, neuroimaging and clinical data for predicting Alzheimer’s disease and reconstruction of relevant biological mechanisms. Sci Rep. https://doi.org/10.1038/S41598-018-29433-3 Moscoso A, Silva-Rodríguez J, Aldrey JM et al (2019) Prediction of Alzheimer’s disease dementia with MRI beyond the short-term: implications for the design of predictive models. NeuroImage: Clin. https://doi.org/10.1016/j.nicl.2019.101837 Battista P, Salvatore C, Castiglioni I (2017) Optimizing neuropsychological assessments for cognitive, behavioral, and functional impairment classification: a machine learning study. Behav Neurol. https://doi.org/10.1155/2017/1850909 Kaplan E, Goodglass H, Weintraub S (1983) Boston naming test. Lea & Febiger, Philadelphia Hughes CP, Berg L, Danziger WL et al (1982) A new clinical scale for the staging of Dementia. Br J Psychiatry 140:566–572 Morris JC (1993) The Clinical Dementia Rating (CDR): current version and scoring rules. Neurology 43:2412–2414 Pinto E, Peters R (2009) Literature review of the Clock Drawing Test as a tool for cognitive screening. Dementia Geriatr Cognit Disord 27:201–213 Kueper JK, Speechley M, Montero-Odasso M (2018) The Alzheimer’s Disease Assessment Scale-Cognitive Subscale (ADAS-Cog): modifications and responsiveness in pre-dementia populations. A narrative review. J Alzheimer’s Dis 63:423–444 Rosen W, Mohs R, Davis K (1984) A new rating scale for Alzheimer’s disease. Am J Psychiatry 141:1356–1364 Yesavage JA, Brink TL, Rose TL et al (1982) Development and validation of a geriatric depression screening scale: a preliminary report. J Psychiatr Res 17:37–49 Cummings JL, Mega M, Gray K et al (1994) The Neuropsychiatric Inventory: comprehensive assessment of psychopathology in dementia. Neurology 44:2308–2314 Folstein MF, Robins LN, Helzer JE (1983) The mini-mental state examination. Arch Gen Psychiatry 40:812 Rey A (1964) The clinical psychological examination. Presses Universitaires de France, Paris Reitan RM (1971) Trail making test results for normal and brain-damaged children. Percept Motor Skills 33:575–581 Fonti V, Belitser E (2017) Feature selection using lasso. In: VU Amsterdam Research Paper in Business Analytics 30:1–25 Muthukrishnan R, Rohini R (2016) Lasso: a feature selection technique in predictive modeling for machine learning. In: 2016 IEEE international conference on advances in computer applications (ICACA), IEEE, pp 18–20 Bekkar M, Alitouche TA (2013) Imbalanced data learning approaches review. Int J Data Mining Knowl Manag Process 3:15–33 Cutler A, Cutler DR, Stevens JR (2012) Random forests. In: Ensemble machine learning. Springer, p 157–175 Goodfellow I, Bengio Y, Courville A (2016) Deep learning. MIT Press, Cambridge Svensén M, Bishop CM (2007) Pattern recognition and machine learning. Springer, Berlin Abdar M, Zomorodi-Moghadam M, Zhou X et al (2020) A new nested ensemble technique for automated diagnosis of breast cancer. Pattern Recogn Lett 132:123–131 Zhong Y, Chalise P, He J (2020) Nested cross-validation with ensemble feature selection and classification model for high-dimensional biological data. In: Communications in statistics-simulation and computation, pp 1–18 Ndiaye E, Le T, Fercoq O, et al (2019) Safe grid search with optimal complexity. In: International conference on machine learning, PMLR, pp 4771–4780 Kyriakides G, Margaritis KG (2019) Hands-on ensemble learning with python: build highly optimized ensemble machine learning models using scikit-learn and Keras. Packt Publishing Ltd, Birmingham Lim WS, Chin JJ, Lam CK et al (2005) Clinical dementia rating experience of a multi-racial Asian population. Alzheimer Dis Assoc Disord 19:135–142 Lee YM, Park JM, Lee BD et al (2012) Memory impairment, in mild cognitive impairment without significant cerebrovascular disease, predicts progression to Alzheimer’s disease. Dementia Geriatr Cognit Disord 33:240–244 Grober E, Cb Hall, Lipton RB et al (2008) Memory impairment, executive dysfunction, and intellectual decline in preclinical Alzheimer’s disease. J Int Neuropsychol Soc 14:266–278 Luukinen H, Viramo P, Koski K et al (1999) Head injuries and cognitive decline among older adults a population-based study. Neurology 52:557–557 Whiteneck GG, Gerhart KA, Cusick CP (2004) Identifying environmental factors that influence the outcomes of people with traumatic brain injury. J Head Trauma Rehabil 19:191–204 Plassman BL, Havlik RJ, Steffens DC et al (2000) Documented head injury in early adulthood and risk of Alzheimer’s disease and other dementias. Neurology 55:1158–1166 Rasmusson D, Brandt J, Martin D et al (1995) Head injury as a risk factor in Alzheimer’s disease. Brain Inj 9:213–219 Schofield P, Tang M, Marder K et al (1997) Alzheimer’s disease after remote head injury: an incidence study. J Neurol Neurosurg Psychiatry 62:119–124 Sivanandam TM, Thakur MK (2012) Traumatic brain injury: a risk factor for Alzheimer’s disease. Neurosci Biobehav Rev 36:1376–1381 Etgen T (2015) Kidney disease as a determinant of cognitive decline and dementia. Alzheimer’s Res Ther 7:29. https://doi.org/10.1186/s13195-015-0115-4 Buchman AS, Tanne D, Boyle PA et al (2009) Kidney function is associated with the rate of cognitive decline in the elderly. Neurology 73:920–927 Braga-Neto P, Pedroso JL, Alessi H et al (2013) Early-onset familial Alzheimer’s disease related to presenilin 1 mutation resembling autosomal dominant spinocerebellar ataxia. J Neurol 260:1177–1179 Testi S, Peluso S, Fabrizi GM et al (2014) A novel PSEN1 mutation in a patient with sporadic early-onset Alzheimer’s disease and prominent cerebellar ataxia. J Alzheimer’s Dis 41:709–714 Jacobs HIL, Hopkins DA, Mayrhofer HC et al (2018) The cerebellum in Alzheimer’s disease: evaluating its role in cognitive decline. Brain 141:37–47 Caligiore D, Helmich RC, Hallett M et al (2016) Parkinson’s disease as a system-level disorder. NPJ Parkinson’s Dis 2:1–9. https://doi.org/10.1038/npjparkd.2016.25 Jo T, Nho K, Risacher SL et al (2020) Deep learning detection of informative features in tau PET for Alzheimer’s disease classification. BMC Bioinform. https://doi.org/10.1186/S12859-020-03848-0 Lin CH, Chiu SI, Chen TF et al (2020) Classifications of neurodegenerative disorders using a multiplex blood biomarkers-based machine learning model. Int J Mol Sci 21:1–15 Nguyen DT, Ryu S, Qureshi MNI et al (2019) Hybrid multivariate pattern analysis combined with extreme learning machine for Alzheimer’s dementia diagnosis using multi-measure rs-fMRI spatial patterns. PLOS ONE. https://doi.org/10.1371/JOURNAL.PONE.0212582 Nunes A, Silva G, Duque C et al (2019) Retinal texture biomarkers may help to discriminate between Alzheimer’s, Parkinson’s, and healthy controls. PLoS ONE. https://doi.org/10.1371/JOURNAL.PONE.0218826 Clute-Reinig N, Jayadev S, Rhoads K et al (2021) Alzheimer’s disease diagnostics must be globally accessible. J Alzheimer’s Dis 84:1453–1455