Cited by 85Dementia and Cognitive Impairment ResearchFunctional Brain Connectivity StudiesAlzheimer's disease research and treatments

A survey on machine and statistical learning for longitudinal analysis of neuroimaging data in Alzheimer’s disease

Martí-Juan, Gerard, Sanroma-Guell, Gerard, Piella, Gemma·2020·Computer Methods and Programs in Biomedicine

Abstract

Background and objectives Recently, longitudinal studies of Alzheimer's disease have gathered a substantial amount of neuroimaging data. New methods are needed to successfully leverage and distill meaningful information on the progression of the disease from the deluge of available data. Machine learning has been used successfully for many different tasks, including neuroimaging related problems. In this paper, we review recent statistical and machine learning applications in Alzheimer's disease using longitudinal neuroimaging. Methods We search for papers using longitudinal imaging data, focused on Alzheimer's Disease and published between 2007 and 2019 on four different search engines. Results After the search, we obtain 104 relevant papers. We analyze their approach to typical challenges in longitudinal data analysis, such as missing data and variability in the number and extent of acquisitions. Conclusions Reviewed works show that machine learning methods using longitudinal data have potential for disease progression modelling and computer-aided diagnosis. We compare results and models, and propose future research directions in the field.

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  • One widely used hypothesis-driven analysis assesses statistical differences of tracts of interest between groups using statistical group-wise comparison methods such as Student's t-test, ANOVA, or more advanced methods.

    “Usually, given a quantitative measure of interest, a selected summary statistic (e.g. mean of the chosen microstructural measure) is extracted from the tract(s)-of-interest and is used to compute the level of group differences (e.g., the p-value) using statistical group-wise comparison methods such as Student’s t-test, ANOVA, or other more advanced statistical analysis methods (Habeck and Stern, 2”

    From Quantitative mapping of the brain’s structural connectivity using diffusion MRI tractography: A review (2022) · cites this paper as Martí-Juan et al., 2020

    Section 4.5 (p. 16) discusses statistical methods for detecting longitudinal MRI group differences and names ANOVA as a comparator. It does not describe hypothesis-driven comparisons of tracts of interest, extraction of a summary microstructural measure, or use of Student’s t-test or p-values. (LLM, conf=0.79)

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Research works printed but not linked: 30

  1. [6][6] E. Lawrence, C. Vegvari, A. Ower, C. Hadjichrysanthou, F. De Wolf, R. M. Anderson, A Systematic Review of Longitudinal Studies Which Measure Alzheimer's Disease Biomarkers, J. Alzheimer's Dis. 59 (2017) 1359-1379. -
  2. [14][14] J. G. Ibrahim, G. Molenberghs, Missing data methods in longitudinal studies: a review., Test (Madr). 18 (2009) 1-43. -
  3. [19][19] M. Bilgel, B. Jedynak, D. F. Wong, S. M. Resnick, J. L. Prince, Temporal trajectory and progression score estimation from voxelwise longitudinal imaging measures: Application to amyloid imaging, in: Lect. Notes Comput. Sci., volume 9123, NIH Public Access, 2015, pp. 424-436. 815 doi: 10.1007/978-3-319-19992-4\_33 . - · DOI
  4. [25][25] F. Rodrigues, M. Silveira, Longitudinal FDG-PET features for the classification of Alzheimer's disease., Conf. Proc. ... Annu. Int. Conf. IEEE Eng. Med. Biol. Soc. IEEE Eng. Med. Biol. Soc. Annu. Conf. 2014 (2014) 835 1941-1944. -
  5. [28][28] J. Huang, D. Alexander, Probabilistic Event Cascades for Alzheimer's disease, Adv. Neural Inf. Process. Syst. 25 (2012) 3104-3112. -
  6. [31][31] G. Sanroma, V. Andrea, O. M. Benkarim, J. V. Manjón, P. Coupé, O. Camara, G. Piella, M. A. González Ballester, Early prediction of alzheimer's disease with non-local patch-based longitudinal descriptors, in: Lect. Notes Comput. Sci. (including Subser. Lect. Notes Artif. Intell. Lect. Notes 855 Bioinformatics), volume 10530 LNCS, Springer, Cham, 2017, pp. 74-81. doi: 10.1007/978-3-319-67434-6\_9 . 860 - · DOI
  7. [40][40] M. Aghili, S. Tabarestani, M. Adjouadi, E. Adeli, Predictive Modeling of Longitudinal Data for Alzheimer's Disease Diagnosis Using RNNs, in: Predict. Intell. Med., Springer International Publishing, 2018, pp. 112119. doi: 10.1007/978-3-030-00320-3\_14 . - · DOI
  8. [42][42] S. Minhas, A. Khanum, F. Riaz, A. Alvi, S. S. A. Khan, Minhas, Khanum, 895 Riaz, A. Alvi, Khan, S. Minhas, A. Khanum, F. Riaz, A. Alvi, S. S. A. Khan, A Non Parametric Approach for Mild Cognitive Impairment to AD Conversion Prediction: Results on Longitudinal Data., IEEE J. Biomed. Heal. Informatics 21 (2016) 1-2. -
  9. [43][43] A. L. Young, N. P. Oxtoby, J. Huang, R. V. Marinescu, P. Daga, 900 D. M. Cash, N. C. Fox, S. Ourselin, J. M. Schott, D. C. Alexander, Multiple orderings of events in disease progression, in: Lect. Notes Comput. Sci. (including Subser. Lect. Notes Artif. Intell. Lect. Notes Bioinformatics), volume 9123, Springer, Cham, 2015, pp. 711-722. doi: 10.1007/978-3-319-19992-4\_56 . 905 910 - · DOI
  10. [44][44] M. W. Weiner, D. P. Veitch, P. S. Aisen, L. A. Beckett, N. J. Cairns, R. C. Green, D. Harvey, C. R. Jack, W. Jagust, J. C. Morris, R. C. Petersen, A. J. Saykin, L. M. Shaw, A. W. Toga, J. Q. Trojanowski, Recent publications from the Alzheimer's Disease Neuroimaging Initiative: Reviewing progress toward improved AD clinical trials, 2017. doi: 10.1016/j.jalz.2016.11.007 . - · DOI
  11. [46][46] R. V. R. V. Marinescu, A. Eshaghi, M. Lorenzi, A. L. Young, N. P. Ox915 toby, S. Garbarino, T. J. Shakespeare, S. J. Crutch, D. C. Alexander, R. V. R. V. Marinescu, A. Eshaghi, M. Lorenzi, A. L. Young, N. P. Oxtoby, S. Garbarino, T. J. Shakespeare, S. J. Crutch, D. C. Alexander, A Vertex Clustering Model for Disease Progression: Application to Cortical Thickness Images, in: M. Niethammer, M. Styner, S. Aylward, 920 H. Zhu, I. Oguz, P.-T. Yap, D. Shen (Eds.), Inf. Process. Med. Imaging, volume 10265, Springer International Publishing, Cham, 2017, pp. 134-145. doi: 10.1007/978-3-319-59050-9 . - · DOI
  12. [52][52] M. Liu, H. I. Suk, D. Shen, Multi-task sparse classifier for diagnosis of 945 MCI conversion to AD with longitudinal MR images, in: Mach. Learn. Med. Imaging (MLMI). Lect. Notes Comput. Sci., volume 8184, 2013, pp. 243-250. doi: 10.1007/978-3-319-02267-3\_31 . - · DOI
  13. [54][54] J. Zhang, Q. Li, R. J. Caselli, J. Ye, Y. Wang, Multi-task Dictionary Learning based Convolutional Neural Network for Computer aided Diagnosis with Longitudinal Images, ArXiv (2017). -
  14. [59][59] L. E. Givon, L. J. Mariano, D. O'Dowd, J. M. Irvine, A. R. Schneider, Cognitive Subscore Trajectory Prediction in Alzheimer's Disease, ArXiv (2017). 975 -
  15. [60][60] A. Ortiz, J. Munilla, F. J. Martínez-Murcia, J. M. Górriz, J. Ramírez, Learning longitudinal MRI patterns by SICE and deep learning: Assessing the Alzheimer's disease progression, in: Commun. Comput. Inf. Sci., volume 723, Springer, Cham, 2017, pp. 413-424. doi: 10.1007/ 978-3-319-60964-5\_36 . -
  16. [61][61] R. Cui, M. Liu, G. Li, Longitudinal analysis for Alzheimer's disease diagnosis using RNN, Proc. - Int. Symp. Biomed. Imaging 2018-April (2018) 1398-1401. -
  17. [67][67] R. Guerrero, C. Ledig, A. Schmidt-Richberg, D. Rueckert, Groupconstrained Laplacian Eigenmaps: Longitudinal AD biomarker learning, in: Lect. Notes Comput. Sci. (including Subser. Lect. Notes Artif. Intell. Lect. Notes Bioinformatics), volume 9352, Springer International Publishing, 2015, pp. 178-185. doi: 10.1007/978-3-319-24888-2\_22 . 1005 - · DOI
  18. [76][76] A. Bône, O. Colliot, S. Durrleman, Learning distributions of shape trajectories from longitudinal datasets: a hierarchical model on a manifold of 1035 diffeomorphisms, in: CVPR 2018 - Comput. Vis. Pattern Recognit. 2018, Salt Lake City, United States, 2018, pp. 9271-9280. arXiv:1803.10119 . - · arXiv
  19. [94][94] J. Zhang, M. Liu, L. An, Y. Gao, D. Shen, Alzheimer's Disease Diagnosis Using Landmark-Based Features From Longitudinal Structural MR Images., IEEE J. Biomed. Heal. informatics 21 (2017) 1607-1616. -
  20. [95][95] Y. Zhu, X. Zhu, M. Kim, Early Diagnosis of Alzheimer's Disease by Joint Feature Selection and Classification on Temporally Structured Support Vector Machine, MICCAI 9900 (2016) 264-272. -
  21. [102][102] B. Jie, M. Liu, J. Liu, D. Zhang, D. Shen, Temporally Constrained Group Sparse Learning for Longitudinal Data Analysis in Alzheimer's Disease., IEEE Trans. Biomed. Eng. 64 (2017) 238-249. -
  22. [105][105] Y. Zhu, M. R. Sabuncu, A Probabilistic Disease Progression Model for Predicting Future Clinical Outcome, ArXiV (2018). -
  23. [107][107] M. Yang, P. Yang, A. Elazab, W. Hou, X. Li, T. Wang, W. Zou, B. Lei, Join and Deep Ensemble Regression of Clinical Scores for Alzheimer's Disease Using Longitudinal and Incomplete Data, Proc. Annu. Int. Conf. IEEE Eng. Med. Biol. Soc. EMBS 2018-July (2018) 1254-1257. -
  24. [120][120] C. Wachinger, A. Rieckmann, M. Reuter, Latent processes governing neu1185 roanatomical change in aging and dementia, in: M. Descoteaux, L. MaierHein, A. Franz, P. Jannin, D. L. Collins, S. Duchesne (Eds.), Medical Image Computing and Computer Assisted Intervention - MICCAI 2017, Springer International Publishing, Cham, 2017, pp. 30-37. -
  25. [123][123] D. Goyal, Z. Syed, J. Wiens, Clinically Meaningful Comparisons Over Time: An Approach to Measuring Patient Similarity based on Subsequence Alignment, ArXiv (2018). -
  26. [129][129] A. Schmidt-Richberg, R. Guerrero, C. Ledig, H. Molina-Abril, A. F. 1215 Frangi, D. Rueckert, Multi-stage biomarker models for progression estimation in Alzheimer's disease, in: Lect. Notes Comput. Sci. (including Subser. Lect. Notes Artif. Intell. Lect. Notes Bioinformatics), volume 9123, Springer, Cham, 2015, pp. 387-398. doi: 10.1007/978-3-319-19992-4\_ 30 . 1220 - · DOI
  27. [137][137] S. Minhas, A. Khanum, F. Riaz, S. A. Khan, A. Alvi, Predicting progression from mild cognitive impairment to Alzheimer's disease using autoregressive modelling of longitudinal and multimodal biomarkers, IEEE J. Biomed. Heal. Informatics 22 (2018) 818-825. -
  28. [143][143] X. Liu, Methods and Applications of Longitudinal Data Analysis, 2016. 1275 doi: 10.1016/c2013-0-13082-6 . - · DOI
  29. [147][147] T. Ching, D. S. Himmelstein, B. K. Beaulieu-Jones, A. A. Kalinin, 1285 B. T. Do, G. P. Way, E. Ferrero, P.-M. Agapow, M. Zietz, M. M. Hoffman, W. Xie, G. L. Rosen, B. J. Lengerich, J. Israeli, J. Lanchantin, S. Woloszynek, A. E. Carpenter, A. Shrikumar, J. Xu, E. M. Cofer, C. A. Lavender, S. C. Turaga, A. M. Alexandari, Z. Lu, D. J. Harris, D. De- 2. Caprio, Y. Qi, A. Kundaje, Y. Peng, L. K. Wiley, M. H. S. Segler, S. M. 1290 Boca, S. J. Swamidass, A. Huang, A. Gitter, C. S. Greene, Opportunities and obstacles for deep learning in biology and medicine, J. R. Soc. Interface 15 (2018). -
  30. [151][151] S. Liu, S. Liu, W. Cai, S. Pujol, R. Kikinis, D. Feng, Early diagnosis of Alzheimer's disease with deep learning, in: 2014 IEEE 11th Int. Symp. Biomed. Imaging, ISBI 2014, Institute of Electrical and Electronics Engineers Inc., 2014, pp. 1015-1018. doi: 10.1109/isbi.2014.6868045 . - · DOI

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Authors
Martí-Juan, G., Sanroma-Guell, G., & Piella, G.
Affiliations
Universitat Pompeu Fabra (ES)
Venue
Computer Methods and Programs in Biomedicine
Publisher
Elsevier BV
Published
2020-06
Volume
189
Pages
105348
ISSN
0169-2607 (ISSN-L)
OpenAlex
W3002097015
Cited by
85
References
12
Citations by year
2026: 6 · 2025: 8 · 2024: 22 · 2023: 19 · 2022: 19 · 2021: 6 · 2020: 5
FWCI
2.00
Type
journal article
Language
en
Open access
closed
Locations
  • Computer Methods and Programs in Biomedicine (publishedVersion)
  • PubMed (publishedVersion)
  • DZNE Pub (submittedVersion)
  • Repositori digital de la UPF (Universitat Pompeu Fabra) (submittedVersion)
Funders
  • Ministerio de Economía y Competitividad
  • Fundació la Marató de TV3
Topics
  • Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
  • Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Keywords
Alzheimer's disease, longitudinal neuroimaging, machine learning, statistical learning, disease progression modeling, computer-aided diagnosis, missing data, longitudinal analysis, neuroimaging data
MeSH terms
Machine Learning, Alzheimer Disease, Humans, Longitudinal Studies, Disease Progression, Neuroimaging

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