Abstract
Purpose
Parkinson disease (PD) is a common progressive neurodegenerative disorder in our ageing society. Early-stage PD biomarkers are desired for timely clinical intervention and understanding of pathophysiology. Since one of the characteristics of PD is the progressive loss of dopaminergic neurons in the substantia nigra pars compacta, we propose a feature extraction method for analysing the differences in the substantia nigra between PD and non-PD patients.
Method
We propose a feature-extraction method for volumetric images based on a rank-1 tensor decomposition. Furthermore, we apply a feature selection method that excludes common features between PD and non-PD. We collect neuromelanin images of 263 patients: 124 PD and 139 non-PD patients and divide them into training and testing datasets for experiments. We then experimentally evaluate the classification accuracy of the substantia nigra between PD and non-PD patients using the proposed feature extraction method and linear discriminant analysis.
Results
The proposed method achieves a sensitivity of 0.72 and a specificity of 0.64 for our testing dataset of 66 non-PD and 42 PD patients. Furthermore, we visualise the important patterns in the substantia nigra by a linear combination of rank-1 tensors with selected features. The visualised patterns include the ventrolateral tier, where the severe loss of neurons can be observed in PD.
Conclusions
We develop a new feature-extraction method for the analysis of the substantia nigra towards PD diagnosis. In the experiments, even though the classification accuracy with the proposed feature extraction method and linear discriminant analysis is lower than that of expert physicians, the results suggest the potential of tensorial feature extraction.









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Notes
This decomposition is also called as CANDECOMP, PARAFAC or CANDECOMP/PARAFAC (CP).
References
James SL, Abate D, Abate KH, Abay SM, Abbafati C, Abbasi N, Abbastabar H, Abd-Allah F, Abdela J, Abdelalim A, Abdollahpour I, Abdulkader RS, Abebe Z, Abera SF, Abil OZ, Abraha HN, Abu-Raddad LJ, Abu-Rmeileh NME, Accrombessi MMK, Acharya D et al (2018) Global, regional, and national incidence, prevalence, and years lived with disability for 354 diseases and injuries for 195 countries and territories, 1990–2017: a systematic analysis for the global burden of disease study 2017. The Lancet 392(10159):1789–1858
Berre AL, Kamagata K, Otsuka Y, Andica C, Hatano T, Saccenti L, Ogawa T, Takeshige-Amano H, Wada A, Suzuki M, Hagiwara A, Irie R, Hori M, Oyama G, Shimo Y, Umemura A, Hattori N, Aoki S (2019) Convolutional neural network-based segmentation can help in assessing the substantia nigra in neuromelanin MRI. Neuroradiology 61:1387–1395
He N, Chen Y, LeWitt PA, Yan F, Haacke EM (2023) Application of neuromelanin MR imaging in Parkinson disease. J Magn Resonance Imaging 57:337–352
Sasaki M, Shibata E, Tohyama K (2006) Neuromelanin magnetic resonance imaging of locus ceruleus and substantia nigra in Parkinson’s disease. Neuro Rep 17(11):1215–1218
Kashihara K, Shinya T, Higaki F (2011) Neuromelanin magnetic resonance imaging of nigral volume loss in patients with Parkinson’s disease. J Clin Neurosci 18(8):1093–1096
Drui G, Carnicella S, Carcenac C, Favier M, Bertrand A, Boulet S, Savasta M (2014) Loss of dopaminergic nigrostriatal neurons accounts for the motivational and affective deficits in Parkinsons disease. Mol Psychiatry 19:358–367
Hu T, Itoh H, Oda M, Hayashi Y, Lu Z, Saiki S, Hattori N, Kamagata K, Aoki S, Kumamaru KK, Akashi T, Mori K (2022) Enhancing model generalization for substantia nigra segmentation using a test-time normalization-based method. In: Proceedings of the 25th international conference on medical image computing and computer assisted intervention, LNCS 13437: 736–744
Hu T, Itoh H, Oda M, Saiki S, Hattori N, Kamagata K, Aoki S, Mori K (2023) Priority attention network with Bayesian learning for fully automatic segmentation of substantia Nigra from neuromelanin MRI. In: Proceedings of the SPIE medical imaging 2023: image processing SPIE 12464: 124643G
Itoh H, Hu T, Oda M, Saiki S, Kamagata K, Hattori N, Aoki S, Mori K (2022) Pattern analysis of substantia Nigra in Parkinson disease by fifth-order tensor decomposition and multi-sequence MRI. In: Proceedings of the 3rd international workshop on multiscale multimodal medical imaging LNCS 13594:63–75
Camacho M, Wilms M, Mouches P, Almgren H, Souza R, Camicioli R, Ismail Z, Monchi O, Forkert ND (2023) Explainable classification of Parkinson’s disease using deep learning trained on a large multi-center database of T1-weighted MRI datasets,. Neuro Image Clin 38:103405
Shinde S, Prasad S, Saboo Y, Kaushick R, Saini J, Pal PK, Ingalhalikar M (2019) Predictive markers for Parkinson’s disease using deep neural nets on neuromelanin sensitive MRI. NeuroImage: Clin 22:101748
Itoh H, Imiya A, Sakai T (2016) Pattern recognition in multilinear space and its applications: mathematics, computational algorithms and numerical validations. Mach Vis Appl 27:1259–1273
Smilde A, Bro R, Geladi P (2008) Multi-way analysis: applications in the chemical sciences, 1st edn. Wiley, New York
Kroonenberg PM (2008) Applied multiway data analysis, 1st edn. Wiley-Interscience, New York
Cichocki A, Zdunek R, Phan AH, Amari S (2009) Nonnegative matrix and tensor factorizations: applications to exploratory multi-way data analysis and blind source separation. Wiley, New York
Kolda TG, Bader BW (2009) Tensor decompositions and applications. SIAM Rev 51(3):455–500
Carroll J, Chang J-J (1970) Analysis of individual differences in multidimensional scaling via an n-way generalization of Eckart-Young decomposition. Psychometrika 35(3):283–319
Harshman RA (1970) Foundations of the PARAFAC procedure: Models and conditions for an "explanatory" multi-model factor analysis. UCLA Working Papers in Phonetics 16:1–84
Shashua A, Hazan T (2005) Non-negative tensor factorization with applications to statistics and computer vision. In: Proceedings of the international conference on machine learning, pp 792–799
Fukunaga K, Koontz WLG (1970) Application of the Karhunen-Loéve expansion to feature selection and ordering. IEEE Trans Comput c–19(4):311–318
Duda RO, Hart PE, Stork DH (2000) Pattern classification, 2nd edn. Wiley Interscience, New York
Hughes AJ, Susan ED, Linda K, Andrew JL (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg 55(3):181–184
Jenkinson M, Bannister P, Brady JM, Smith SM (2002) Improved optimisation for the robust and accurate linear registration and motion correction of brain images. NeuroImage 17(2):825–841. https://fsl.fmrib.ox.ac.uk/fsl/fslwiki/FLIRT
Chris R, Matthew B (2001) Stereotaxic display of brain lesions. Behav Neurol 12:192–200. https://www.nitrc.org/projects/mricron/
Vapnik V, Lerner A (1963) Pattern recognition using generalized portrait method. Autom Remote Control 24:774–780
Platt JC (1999) Probabilistic outputs for support vector machinesand comparisons to regularized likelihood methods. Adv Large Margin Classifier: 61-74
Ellison E, Chimelli L., Harding B, Love S, Lowe J, Roberts G, Vinters H (1998) Neuropathology. Mosby-Year Book
Rizzo G, Copetti M, Arcuti S, Martino D, Fontana A, Logroscino G (2016) Accuracy of clinical diagnosis of Parkinson disease. Neurology 86:566–576
Cho SJ, Bae YJ, Kim JM, Balik SH, Sunwoo L, Choi BS, Kim JH (2021) Diagnostic performance of neuromelanin-sensitive magnetic resonance imaging for patients with Parkinson’s disease and factor analysis for its heterogeneity: a systematic review and meta-analysis. Eur Radiol 31:1268–1280
Acknowledgements
This study was funded by grants from AMED (22dm0307101h0004), MEXT/JSPS KAKENHI (21K19898, 23K16900).
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Mori K is supported by Cybernet Systems and Olympus (research grant) and by NTT outside the submitted work. The other authors have no conflict of interest.
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All the procedures performed in studies involving human participants were in accordance with the ethical committees of Nagoya University (No. 382) and Juntendo University (H19-179) and the 1964 Helsinki Declaration and subsequent amendments or comparable ethical standards. Informed consent was obtained by an opt-out procedure from all individual participants in this study.
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Itoh, H., Oda, M., Saiki, S. et al. Preliminary study of substantia nigra analysis by tensorial feature extraction. Int J CARS 19, 2133–2142 (2024). https://doi.org/10.1007/s11548-024-03175-2
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DOI: https://doi.org/10.1007/s11548-024-03175-2