Idiopathic Parkinson's Disease (iPD) is a common motor neurodegenerative disorder. It affects more frequently the elderly population, causing a significant emotional burden both for the patient and caregivers, due to the disease-related onset of motor and cognitive disabilities. iPD's clinical hallmark is the onset of cardinal motor symptoms such as bradykinesia, rest tremor, rigidity, and postural instability. However, these symptoms appear when the neurodegenerative process is already in an advanced stage. Furthermore, the greatest challenge is to distinguish iPD from other similar neurodegenerative disorders, "atypical parkinsonisms", such as Multisystem Atrophy, Progressive Supranuclear Palsy and Cortical Basal Degeneration, since they share many phenotypic manifestations, especially in the early stages. The diagnosis of these neurodegenerative motor disorders is essentially clinical. Consequently, the diagnostic accuracy mainly depends on the professional knowledge and experience of the physician. Recent advances in artificial intelligence have made it possible to analyze the large amount of clinical and instrumental information in the medical field. The application machine learning algorithms to the analysis of neuroimaging data appear to be a promising tool for identifying microstructural alterations related to the pathological process in order to explain the onset of symptoms and the spread of the neurodegenerative process. In this context, the search for quantitative biomarkers capable of identifying parkinsonian patients in the prodromal phases of the disease, of correctly distinguishing them from atypical parkinsonisms and of predicting clinical evolution and response to therapy represent the main goal of most current clinical research studies. Our aim was to review the recent literature and describe the current knowledge about the contribution given by machine learning applications to research and clinical management of parkinsonian syndromes.
Citation: Annalisa Vitale, Rossella Villa, Lorenzo Ugga, Valeria Romeo, Arnaldo Stanzione, Renato Cuocolo. Artificial intelligence applied to neuroimaging data in Parkinsonian syndromes: Actuality and expectations[J]. Mathematical Biosciences and Engineering, 2021, 18(2): 1753-1773. doi: 10.3934/mbe.2021091
Idiopathic Parkinson's Disease (iPD) is a common motor neurodegenerative disorder. It affects more frequently the elderly population, causing a significant emotional burden both for the patient and caregivers, due to the disease-related onset of motor and cognitive disabilities. iPD's clinical hallmark is the onset of cardinal motor symptoms such as bradykinesia, rest tremor, rigidity, and postural instability. However, these symptoms appear when the neurodegenerative process is already in an advanced stage. Furthermore, the greatest challenge is to distinguish iPD from other similar neurodegenerative disorders, "atypical parkinsonisms", such as Multisystem Atrophy, Progressive Supranuclear Palsy and Cortical Basal Degeneration, since they share many phenotypic manifestations, especially in the early stages. The diagnosis of these neurodegenerative motor disorders is essentially clinical. Consequently, the diagnostic accuracy mainly depends on the professional knowledge and experience of the physician. Recent advances in artificial intelligence have made it possible to analyze the large amount of clinical and instrumental information in the medical field. The application machine learning algorithms to the analysis of neuroimaging data appear to be a promising tool for identifying microstructural alterations related to the pathological process in order to explain the onset of symptoms and the spread of the neurodegenerative process. In this context, the search for quantitative biomarkers capable of identifying parkinsonian patients in the prodromal phases of the disease, of correctly distinguishing them from atypical parkinsonisms and of predicting clinical evolution and response to therapy represent the main goal of most current clinical research studies. Our aim was to review the recent literature and describe the current knowledge about the contribution given by machine learning applications to research and clinical management of parkinsonian syndromes.
[1] | A. H. Schapira, P. Jenner, Etiology and pathogenesis of Parkinson's disease, Mov.Disord., 26 (2011), 1049–1055. doi: 10.1002/mds.23732 |
[2] | W. Dauer, S. Przedborski, Parkinson's disease: Mechanisms and models, Neuron, 39 (2003), 889–909. doi: 10.1016/S0896-6273(03)00568-3 |
[3] | R. F. Pfeiffer, Non-motor symptoms in Parkinson's disease, Parkinson. Relat. Disord., 22 (2016), 119–122. |
[4] | A. J. Hughes, S. E. Daniel, L. Kilford, A. J. Lees, Accuracy of clinical diagnosis of idiopathic Parkinson's disease: A clinico-pathological study of 100 cases, J. Neurol. Neurosurg. Psych., 55 (1992), 181–184. doi: 10.1136/jnnp.55.3.181 |
[5] | R. B. Postuma, D. Berg, M. Stern, W. Poewe, C. W. Olanow, W. Oertel, et al., MDS clinical diagnostic criteria for Parkinson's disease, Mov. Disord., 30 (2015), 1591–1601. doi: 10.1002/mds.26424 |
[6] | E. Tolosa, G. Wenning, W. Poewe, The diagnosis of Parkinson's disease, Lancet Neurol., 5 (2006), 75–86. |
[7] | E. Hustad, A. H. Skogholt, K. Hveem, J. O. Aasly, The accuracy of the clinical diagnosis of Parkinson disease, The HUNT study, J. Neurol., 265 (2018), 2120–2124. |
[8] | J. Levin, A. Kurz, T. Arzberger, A. Giese, G. U. Höglinger, The differential diagnosis and treatment of atypical Parkinsonism, Dtsch. Arztebl. Int., 113 (2016), 61–69. |
[9] | A. M. Keener, Y. M. Bordelon, Parkinsonism, Semin. Neurol., 36 (2016), 330–334. |
[10] | U. Saeed, A. E. Lang, M. Masellis, Neuroimaging advances in Parkinson's disease and atypical Parkinsonian syndromes, Front. Neurol., 11 (2020), 572976. |
[11] | S. Mangesius, S. Mariotto, S. Ferrari, S. Jr Pereverzyev, H. Lerchner, L. Haider, et al., Novel decision algorithm to discriminate parkinsonism with combined blood and imaging biomarkers, Parkinson. Relat. Disord., 77 (2020), 57–63. doi: 10.1016/j.parkreldis.2020.05.033 |
[12] | A. Kaipainen, O. Jääskeläinen, Y. Liu, F. Haapalinna, N. Nykänen, R. Vanninen, et al., Cerebrospinal fluid and MRI biomarkers in neurodegenerative diseases: A retrospective memory clinic-based study, J. Alzheimers Dis., 75 (2020), 751–765. doi: 10.3233/JAD-200175 |
[13] | N. He, J. Langley, D. E. Huddleston, S. Chen, P. Huang, H. Ling, et al., Increased iron-deposition in lateral-ventral substantia nigra pars compacta: A promising neuroimaging marker for Parkinson's disease, Neuroimage Clin., 28 (2020), 102391. |
[14] | H. Sjöström, T. Granberg, F. Hashim, E. Westman, P. Svenningsson, Automated brainstem volumetry can aid in the diagnostics of parkinsonian disorders, Parkinson. Relat. Disord., 79 (2020), 18–25. doi: 10.1016/j.parkreldis.2020.08.004 |
[15] | X. Liu, N. Wang, C. Chen, P. Y. Wu, S. Piao, D. Geng, et al., Swallow tail sign on susceptibility map-weighted imaging (SMWI) for disease diagnosing and severity evaluating in parkinsonism, Acta Radiol., (2020), 284185120920793. |
[16] | M. Picillo, M. F. Tepedino, F. Abate, R. Erro, S. Ponticorvo, S. Tartaglione, et al., Midbrain MRI assessments in progressive supranuclear palsy subtypes, J. Neurol. Neurosurg. Psych., 9 (2020), 98–103. |
[17] | A. Quattrone, A. Antonini, D. E. Vaillancourt, K. Seppi, R. Ceravolo, A. P. Strafella, et al., A New MRI measure to early differentiate progressive supranuclear palsy from De novo Parkinson's dDisease in clinical practice: An international study, Mov. Disord., (2020). |
[18] | G. Arribarat, P. Péran, Quantitative MRI markers in Parkinson's disease and parkinsonian syndromes, Curr. Opin. Neurol., 33 (2020), 222–229. |
[19] | N. Pyatigorskaya, L. Yahia-Cherif, R. Gaurav, C. Ewenczyk, C. Gallea, R. Valabregue, et al., Multimodal magnetic resonance imaging quantification of brain changes in progressive supranuclear palsy, Mov. Disord., 35 (2020), 161–170. doi: 10.1002/mds.27877 |
[20] | B. Xiao, N. He, Q. Wang, Z. Cheng, Y. Jiao, E. M. Haacke, et al., Quantitative susceptibility mapping based hybrid feature extraction for diagnosis of Parkinson's disease, Neuro. Clin., 24 (2019), 102070. |
[21] | L. Chougar, N. Pyatigorskaya, B. Degos, D. Grabli, S. Lehéricy, The role of magnetic resonance imaging for the diagnosis of atypical parkinsonism, Front. Neurol., 11 (2020), 665. |
[22] | A. Quattrone, A. Sarica, D. La Torre, M. Morelli, B. Vescio, S. Nigro, et al., Magnetic resonance imaging biomarkers distinguish normal pressure hydrocephalus from progressive supranuclear palsy, Mov. Disord., 35(2020), 1406–1415. doi: 10.1002/mds.28087 |
[23] | D. B. Archer, T. Mitchell, R. G. Burciu, J. Yang, S. Nigro, A. Quattrone, et al., Magnetic resonance Imaging and neurofilament light in the differentiation of Parkinsonism, Mov. Disord., 35 (2020), 1388–1395. doi: 10.1002/mds.28060 |
[24] | M. Bocchetta, J. E. Iglesias, V. Chelban, E. Jabbari, R. Lamb, L. L. Russell, et al., Automated brainstem segmentation detects differential involvement in atypical parkinsonian syndromes, J. Mov. Disord., 13 (2020), 39–46. doi: 10.14802/jmd.19030 |
[25] | P. Mahlknecht, A. Hotter, A. Hussl, R. Esterhammer, M. Schocke, K. Seppi, Significance of MRI in diagnosis and differential diagnosis of Parkinson's disease, Neurodegener. Dis., 7 (2010), 300-318. doi: 10.1159/000314495 |
[26] | R. De Micco, A. Russo, A. Tessitore, Structural MRI in idiopathic Parkinson's disease, Int. Rev. Neurobio.l, 141(2018), 405–438. doi: 10.1016/bs.irn.2018.08.011 |
[27] | S. B. Kotsiantis, I. D. Zaharakis, P. E. Pintelas, Machine learning: A review of classification and combining techniques, Artif Intell. Rev., 26 (2006), 159–190. doi: 10.1007/s10462-007-9052-3 |
[28] | J. M. Mateos-Pérez, M. Dadar, M. Lacalle-Aurioles, Y. Iturria-Medina, Y. Zeighami, A. C. Evans, Structural neuroimaging as clinical predictor: A review of machine learning applications, Neuroimage Clin., 20 (2018), 506–522. doi: 10.1016/j.nicl.2018.08.019 |
[29] | R. Cuocolo, M. Caruso, T. Perillo, L. Ugga, M. Petretta, Machine learning in oncology: A clinical appraisal, Cancer Lett., 481 (2020), 55–62. doi: 10.1016/j.canlet.2020.03.032 |
[30] | L. Agnello, A. Comelli, E. Ardizzone, S. Vitabile, Unsupervised tissue classification of brain MR images for voxel-based morphometry analysis, Int. J. Imag. Syst. Technol., 26 (2016), 136–150. doi: 10.1002/ima.22168 |
[31] | A. Comelli, A. Stefano, S. Bignardi, C. Coronnello, G. Russo, M. G. Sabini, et al., Tissue classification to support local active delineation of brain tumors, in Medical Image Understanding and Analysis. MIUA (eds. Y.Zheng, B.Williams, K.Chen), Springer, 1065 (2019). |
[32] | C. Ricciardi, M. Amboni, C. Santis, G. Ricciardelli, G. Improta, G. Cesarelli, et al., Classifying patients affected by Parkinson's disease into freezers or non-freezers through machine learning, IEEE International Symposium on Medical Measurements and Applications, (2020), 1–6. |
[33] | C. Ricciardi, M. Amboni, C. De Santis, G. Ricciardelli, G. Improta, G. D'Addio, et al., Machine learning can detect the presence of Mild cognitive impairment in patients affected by Parkinson's Disease, IEEE International Symposium on Medical Measurements and Applications, (2020), 1–6. |
[34] | R. Prashanth, S. Dutta Roy, P. K. Mandal, S. Ghosh, High-accuracy detection of early Parkinson's disease through multimodal features and machine learning, Int. J. Med. Inform., 90 (2016), 13–21. doi: 10.1016/j.ijmedinf.2016.03.001 |
[35] | Ó. Peña-Nogales, T. M. Ellmore, R. De Luis-García, J. Suescun, M. C. Schiess, L. Giancardo, Longitudinal connectomes as a candidate progression marker for prodromal Parkinson's disease, Front. Neurosci., 12 (2019), 967. |
[36] | Y. Liu, Y. Wang, C. Huang, D. Zeng, Estimating personalized diagnostic rules depending on individualized characteristics, Stat. Med., 36 (2017), 1099–1117. doi: 10.1002/sim.7182 |
[37] | S. Shinde, S. Prasad, Y. Saboo, R. Kaushick, J. Saini, P.K. Pal, et al., Predictive markers for Parkinson's disease using deep neural nets on neuromelanin sensitive MRI, Neuro. Clin., 22 (2019), 101748. |
[38] | B. Peng, S. Wang, Z. Zhou, Y. Liu, B. Tong, T. Zhang, et al., A multilevel-ROI-features-based machine learning method for detection of morphometric biomarkers in Parkinson's disease, Neurosci. Lett., 651 (2017), 88–94. doi: 10.1016/j.neulet.2017.04.034 |
[39] | Y. Chen, G. Zhu, D. Liu, Y. Liu, T. Yuan, X. Zhang, et al., Brain morphological changes in hypokinetic dysarthria of Parkinson's disease and use of machine learning to predict severity, CNS Neurosci. Ther., 26 (2020), 711–719. doi: 10.1111/cns.13304 |
[40] | E. Glaab, J. P. Trezzi, A. Greuel, C. Jäger, Z. Hodak, A. Drzezga, et al., Integrative analysis of blood metabolomics and PET brain neuroimaging data for Parkinson's disease, Neurobiol. Dis., 124 (2019), 555–562. doi: 10.1016/j.nbd.2019.01.003 |
[41] | K. L. Poston, S. York Williams, K. Zhang, W. Cai, D. Everling, F. M. Tayim, et al., Compensatory neural mechanisms in cognitively unimpaired Parkinson disease, Ann. Neurol., 79 (2016), 448–463. doi: 10.1002/ana.24585 |
[42] | C. Salvatore, A. Cerasa, I. Castiglioni, F. Gallivanone, A. Augimeri, M. Lopez, et al., Machine learning on brain MRI data for differential diagnosis of Parkinson's disease and Progressive Supranuclear Palsy, J. Neurosci. Methods, 222 (2014), 230–237. doi: 10.1016/j.jneumeth.2013.11.016 |
[43] | M. M. Correia, T. Rittman, C. L. Barnes, I. T. Coyle-Gilchrist, B. Ghosh, L. E. Hughes, et al., Towards accurate and unbiased imaging-based differentiation of Parkinson's disease, progressive supranuclear palsy and corticobasal syndrome, Brain Commun., 2 (2020), fcaa051. |
[44] | D. B. Archer, J. T. Bricker, W. T. Chu, R. G. Burciu, J. L. Mccracken, S. Lai, et al., Development and validation of the automated imaging differentiation in Parkinsonism (AID-P): A multi-site machine learning study, Lancet Digit. Health, 1 (2019), e222–e231. |
[45] | G. Du, M. M. Lewis, S. Kanekar, N. W. Sterling, L. He, L. Kong, et al., Combined diffusion tensor imaging and apparent transverse relaxation rate differentiate Parkinson disease and atypical Parkinsonism, AJNR Am. J. Neuroradiol., 38 (2017), 966–972. doi: 10.3174/ajnr.A5136 |
[46] | N. Amoroso, M. La Rocca, A. Monaco, R. Bellotti, S. Tangaro, Complex networks reveal early MRI markers of Parkinson's disease, Med. Image Anal., 48 (2018), 12–24. doi: 10.1016/j.media.2018.05.004 |
[47] | Q. Gu, H. Zhang, M. Xuan, W. Luo, P. Huang, S. Xia, et al., Automatic classification on multi-modal MRI data for diagnosis of the postural instability and gait difficulty subtype of Parkinson's disease, J. Parkinsons Dis., 6(2016), 545–556. doi: 10.3233/JPD-150729 |
[48] | M. R. Salmanpour, M. Shamsaei, A. Saberi, I. S. Klyuzhin, J. Tang, V. Sossi, et al., Machine learning methods for optimal prediction of motor outcome in Parkinson's disease, Phys. Med., 69 (2020), 233–240. doi: 10.1016/j.ejmp.2019.12.022 |
[49] | S. Waninger, C. Berka, M. Stevanovic Karic, S. Korszen, P. D. Mozley, C. Henchcliffe, et al., Neurophysiological biomarkers of Parkinson's disease, J. Parkinsons Dis., 10 (2020), 471–480. doi: 10.3233/JPD-191844 |
[50] | J. Tang, B. Yang, M. P. Adams, N. N. Shenkov, I. S. Klyuzhin, S. Fotouhi, et al., Artificial neural network-based prediction of outcome in Parkinson's disease patients using DaTscan SPECT imaging features, Mol. Imag. Biol., 21 (2019), 1165–1173. doi: 10.1007/s11307-019-01334-5 |
[51] | Y. L. Chen, X. A. Zhao, S. H. Ng, C. S. Lu, Y. C. Lin, J. S. Cheng, et al., Prediction of the clinical severity of progressive supranuclear palsy by diffusion tensor imaging, J. Clin. Med., 9 (2019), 40. |
[52] | Y. Chen, G. Zhu, D. Liu, Y. Liu, T. Yuan, X. Zhang, et al., The morphology of thalamic subnuclei in Parkinson's disease and the effects of machine learning on disease diagnosis and clinical evaluation, J. Neurol. Sci., 411(2020), 116721. |
[53] | T. Chih-Chien, L. Yu-Chun, N. Shu-Hang, C. Yao-Liang, C. Jur-Shan, L. Chin-Song, et al., A method for the prediction of clinical outcome using diffusion magnetic resonance imaging: Application on Parkinson's disease, J. Clin. Med., 9 (2020), 647. |
[54] | M. Peralta, J. S. H. Baxter, A. R. Khan, C. Haegelen, P. Jannin, Striatal shape alteration as a staging biomarker for Parkinson's Disease, Neuroimage Clin., 27 (2020), 102272. |
[55] | H. Kaka, E. Zhang, N. Khan, Artificial intelligence and deep learning in neuroradiology: Exploring the new frontier, Can. Assoc. Radiol. J., (2020), 846537120954293. |
[56] | A. W. Olthof, P. M. A. van Ooijen, M. H. Rezazade Mehrizi, Promises of artificial intelligence in neuroradiology: A systematic technographic review, Neuroradiology, 62 (2020), 1265–1278. doi: 10.1007/s00234-020-02424-w |
[57] | T. C. Booth, M. Williams, A. Luis, J. Cardoso, K. Ashkan, H. Shuaib, Machine learning and glioma imaging biomarkers, Clin. Radiol., 75 (2020), 20–32. doi: 10.1016/j.crad.2019.07.001 |
[58] | H. Zhou, R. Hu, O. Tang, C. Hu, L. Tang, K. Chang, et al., Automatic machine learning to differentiate pediatric posterior fossa tumors on routine MR imaging, AJNR Am. J. Neuroradiol., 41 (2020), 1279–1285. doi: 10.3174/ajnr.A6621 |
[59] | S. J. Cho, L. Sunwoo, S. H. Baik, Y. J. Bae, B. S. Choi, J. H. Kim, Brain metastasis detection using machine learning: A systematic review and meta-analysis, Neuro. Oncol., (2020), noaa232. |
[60] | H. M. R. Afzal, S. Luo, S. Ramadan, J. Lechner-Scott, The emerging role of artificial intelligence in multiple sclerosis imaging, Mult. Scler., (2020), 1352458520966298. |
[61] | P. N. E. Young, M. Estarellas, E. Coomans, M. Srikrishna, H. Beaumont, A. Maass, et al., Imaging biomarkers in neurodegeneration: Current and future practices, Alzheimers Res. Ther., 12 (2020), 49. |
[62] | A. N. Nielsen, D. M. Barch, S. E. Petersen, B. L. Schlaggar, D. J. Greene, Machine learning with neuroimaging: Evaluating its applications in psychiatry, Biol. Psych. Cogn. Neurosci. Neuroimag., 5 (2020), 791–798. |
[63] | N. M. Murray, M. Unberath, G. D. Hager, F. K. Hui, Artificial intelligence to diagnose ischemic stroke and identify large vessel occlusions: A systematic review, J. Neuroint. Surg., 12 (2020), 156–164. doi: 10.1136/neurintsurg-2019-015135 |
[64] | S. Heinzel, D. Berg, T. Gasser, H. Chen, C. Yao, R. B. Postuma, MDS task force on the definition of Parkinson's disease. Update of the MDS research criteria for prodromal Parkinson's disease, Mov. Disord., 34 (2019), 1464–1470. doi: 10.1002/mds.27802 |
[65] | R. B. Postuma, D. Berg, Prodromal Parkinson's disease: The decade past, the decade to come, Mov. Disord., 34 (2019), 665–675. |
[66] | D. Salat, A. J. Noyce, A. Schrag, E. Tolosa, Challenges of modifying disease progression in prediagnostic Parkinson's disease, Lancet Neurol., 15(2016), 637–648. doi: 10.1016/S1474-4422(16)00060-0 |
[67] | R. B. Postuma, D. Berg, Advances in markers of prodromal Parkinson disease, Nat. Rev. Neurol., 12 (2016), 622–634. |
[68] | K. Marek, D. Jennings, S. Lasch, A. Siderowf, C. Tanner, T. Simuni, et al., Parkinson Progression Marker Initiative. The Parkinson Progression Marker Initiative (PPMI), Prog. Neurobiol., 95 (2011), 629–635. doi: 10.1016/j.pneurobio.2011.09.005 |
[69] | D. Frosini, M. Cosottini, D. Volterrani, R. Ceravolo, Neuroimaging in Parkinson's disease: Focus on substantia nigra and nigro-striatal projection, Curr. Opin. Neurol., 30 (2017), 416–426. doi: 10.1097/WCO.0000000000000463 |
[70] | G. L. Hedlund, A. G. Osborn, K. L. Salzman, Osborn's brain imaging, pathology and anatomy, Second edition, Elsevier, Philadelphia, 2018. |
[71] | L. Ugga, R. Cuocolo, S. Cocozza, G. Pontillo, A. Elefante, M. Quarantelli, et al., Magnetic resonance parkinsonism indices and interpeduncular angle in idiopathic normal pressure hydrocephalus and progressive supranuclear palsy, Neuroradiology, 62 (2020), 1657–1665. doi: 10.1007/s00234-020-02500-1 |
[72] | J. Xu, M. Zhang, Use of magnetic resonance imaging and artificial intelligence in studies of diagnosis of Parkinson's disease, ACS Chem. Neurosci., 10 (2019), 2658–2667. doi: 10.1021/acschemneuro.9b00207 |
[73] | M. A. Thenganatt, J. Jankovic, Parkinson disease subtypes, JAMA Neurol., 71 (2014), 499–504. |
[74] | D. Aleksovski, D. Miljkovic, D. Bravi, A. Antonini, Disease progression in Parkinson subtypes: The PPMI dataset, Neurol. Sci., 39 (2018), 1971–1976. doi: 10.1007/s10072-018-3522-z |