A machine-learning framework for robust and reliable prediction of short- and long-term treatment response in initially antipsychotic-naïve schizophrenia patients based on multimodal neuropsychiatric data.
Journal
Translational psychiatry
ISSN: 2158-3188
Titre abrégé: Transl Psychiatry
Pays: United States
ID NLM: 101562664
Informations de publication
Date de publication:
10 08 2020
10 08 2020
Historique:
received:
25
02
2020
accepted:
22
07
2020
revised:
14
07
2020
entrez:
12
8
2020
pubmed:
12
8
2020
medline:
22
6
2021
Statut:
epublish
Résumé
The reproducibility of machine-learning analyses in computational psychiatry is a growing concern. In a multimodal neuropsychiatric dataset of antipsychotic-naïve, first-episode schizophrenia patients, we discuss a workflow aimed at reducing bias and overfitting by invoking simulated data in the design process and analysis in two independent machine-learning approaches, one based on a single algorithm and the other incorporating an ensemble of algorithms. We aimed to (1) classify patients from controls to establish the framework, (2) predict short- and long-term treatment response, and (3) validate the methodological framework. We included 138 antipsychotic-naïve, first-episode schizophrenia patients with data on psychopathology, cognition, electrophysiology, and structural magnetic resonance imaging (MRI). Perinatal data and long-term outcome measures were obtained from Danish registers. Short-term treatment response was defined as change in Positive And Negative Syndrome Score (PANSS) after the initial antipsychotic treatment period. Baseline diagnostic classification algorithms also included data from 151 matched controls. Both approaches significantly classified patients from healthy controls with a balanced accuracy of 63.8% and 64.2%, respectively. Post-hoc analyses showed that the classification primarily was driven by the cognitive data. Neither approach predicted short- nor long-term treatment response. Validation of the framework showed that choice of algorithm and parameter settings in the real data was successfully guided by results from the simulated data. In conclusion, this novel approach holds promise as an important step to minimize bias and obtain reliable results with modest sample sizes when independent replication samples are not available.
Identifiants
pubmed: 32778656
doi: 10.1038/s41398-020-00962-8
pii: 10.1038/s41398-020-00962-8
pmc: PMC7417553
doi:
Substances chimiques
Antipsychotic Agents
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
276Subventions
Organisme : Lundbeckfonden (Lundbeck Foundation)
ID : R155-2013-16337
Pays : International
Organisme : Lundbeckfonden (Lundbeck Foundation)
ID : R25-A2701
Pays : International
Organisme : Lundbeckfonden (Lundbeck Foundation)
ID : R25-A2701
Pays : International
Organisme : Lundbeckfonden (Lundbeck Foundation)
ID : R155-2013-16337
Pays : International
Organisme : Lundbeckfonden (Lundbeck Foundation)
ID : R155-2013-16337
Pays : International
Organisme : Lundbeckfonden (Lundbeck Foundation)
ID : R25-A2701
Pays : International
Organisme : Lundbeckfonden (Lundbeck Foundation)
ID : R25-A2701
Pays : International
Organisme : Lundbeckfonden (Lundbeck Foundation)
ID : R155-2013-16337
Pays : International
Organisme : Lundbeckfonden (Lundbeck Foundation)
ID : R25-A2701
Pays : International
Organisme : Lundbeckfonden (Lundbeck Foundation)
ID : R155-2013-16337
Pays : International
Organisme : Lundbeckfonden (Lundbeck Foundation)
ID : R246-2016-3237
Pays : International
Organisme : Lundbeckfonden (Lundbeck Foundation)
ID : R25-A2701
Pays : International
Organisme : Lundbeckfonden (Lundbeck Foundation)
ID : R155-2013-16337
Pays : International
Organisme : Department of Health | National Health and Medical Research Council (NHMRC)
ID : 1105825
Pays : International
Références
Beck, K. et al. Prevalence of treatment-resistant psychoses in the community: a naturalistic study. J. Psychopharmacol. 33, 1248–1253 (2019).
pubmed: 31241396
doi: 10.1177/0269881119855995
Howes, O. D. et al. Treatment-resistant schizophrenia: Treatment Response and Resistance in psychosis (TRRIP) Working Group Consensus Guidelines on Diagnosis and Terminology. AJP 174, 216–229 (2016).
doi: 10.1176/appi.ajp.2016.16050503
Haijma, S. V. et al. Brain volumes in schizophrenia: a meta-analysis in over 18 000 subjects. Schizophr. Bull. 39, 1129–1138 (2013).
pubmed: 23042112
doi: 10.1093/schbul/sbs118
van Erp, T. G. M. et al. Subcortical brain volume abnormalities in 2028 individuals with schizophrenia and 2540 healthy controls via the ENIGMA consortium. Mol. Psychiatry 21, 547–553 (2016).
doi: 10.1038/mp.2015.63
pubmed: 26033243
Owens, E., Bachman, P., Glahn, D. C. & Bearden, C. E. Electrophysiological endophenotypes for schizophrenia. Harv. Rev. Psychiatry 24, 129–147 (2016).
pubmed: 26954597
pmcid: 4785844
doi: 10.1097/HRP.0000000000000110
Randau, M. et al. Attenuated mismatch negativity in patients with first-episode antipsychotic-naive schizophrenia using a source-resolved method. NeuroImage: Clin. 22, 101760 (2019).
doi: 10.1016/j.nicl.2019.101760
Fatouros-Bergman, H., Cervenka, S., Flyckt, L., Edman, G. & Farde, L. Meta-analysis of cognitive performance in drug-naïve patients with schizophrenia. Schizophr. Res. 158, 156–162 (2014).
pubmed: 25086658
doi: 10.1016/j.schres.2014.06.034
Olabi, B. et al. Are there progressive brain changes in schizophrenia? A meta-analysis of structural magnetic resonance imaging studies. Biol. Psychiatry 70, 88–96 (2011).
pubmed: 21457946
doi: 10.1016/j.biopsych.2011.01.032
Leung, M. et al. Gray matter in first-episode schizophrenia before and after antipsychotic drug treatment. Anatomical likelihood estimation meta-analyses with sample size weighting. Schizophr. Bull. 37, 199–211 (2011).
doi: 10.1093/schbul/sbp099
pubmed: 19759093
Arbabshirani, M. R., Plis, S., Sui, J. & Calhoun, V. D. Single subject prediction of brain disorders in neuroimaging: promises and pitfalls. NeuroImage 145, 137–165 (2017).
pubmed: 27012503
doi: 10.1016/j.neuroimage.2016.02.079
Janssen, R. J., Mourão-Miranda, J. & Schnack, H. G. Making individual prognoses in psychiatry using neuroimaging and machine learning. Biol. Psychiatry.: Cogn. Neurosci. Neuroimaging 3, 798–808 (2018).
Vieira, S. et al. Using machine learning and structural neuroimaging to detect first episode psychosis: reconsidering the evidence. Schizophr. Bull. https://doi.org/10.1093/schbul/sby189 (2019).
Winterburn, J. L. et al. Can we accurately classify schizophrenia patients from healthy controls using magnetic resonance imaging and machine learning? A multi-method and multi-dataset study. Schizophr. Res. https://doi.org/10.1016/j.schres.2017.11.038 (2017).
Cearns, M., Hahn, T. & Baune, B. T. Recommendations and future directions for supervised machine learning in psychiatry. Transl. Psychiatry 9, 1–12 (2019).
doi: 10.1038/s41398-018-0355-8
Doan, N. T. et al. Distinct multivariate brain morphological patterns and their added predictive value with cognitive and polygenic risk scores in mental disorders. NeuroImage: Clin. 15, 719–731 (2017).
doi: 10.1016/j.nicl.2017.06.014
Ebdrup, B. H. et al. Accuracy of diagnostic classification algorithms using cognitive-, electrophysiological-, and neuroanatomical data in antipsychotic-naïve schizophrenia patients. Psychol. Med. https://doi.org/10.1017/S0033291718003781 (2018).
Bak, N. et al. Two subgroups of antipsychotic-naive, first-episode schizophrenia patients identified with a Gaussian mixture model on cognition and electrophysiology. Transl. Psychiatry 7, e1087 (2017).
pubmed: 28398342
pmcid: 5416700
doi: 10.1038/tp.2017.59
Kelleher, J. D., Namee, B. M. & D’Arcy, A. Fundamentals of Machine Learning for Predictive Data Analytics: Algorithms, Worked Examples, and Case Studies (The MIT Press, 2015).
Nørbak-Emig, H. et al. Extrastriatal dopamine D 2/3 receptors and cortical grey matter volumes in antipsychotic-naïve schizophrenia patients before and after initial antipsychotic treatment. World J. Biol. Psychiatry 18, 539–549 (2017).
pubmed: 27782768
doi: 10.1080/15622975.2016.1237042
Jessen, K. et al. Patterns of cortical structures and cognition in antipsychotic-naïve patients with first-episode schizophrenia: a partial least squares correlation analysis. Biol. Psychiatry.: Cogn. Neurosci. Neuroimaging 4, 444–453 (2019).
Wing, J. K. et al. SCAN. Schedules for Clinical Assessment in Neuropsychiatry. Arch. Gen. Psychiatry 47, 589–593 (1990).
doi: 10.1001/archpsyc.1990.01810180089012
pubmed: 2190539
Kay, S. R., Fiszbein, A. & Opler, L. A. The Positive and Negative Syndrome Scale (PANSS) for schizophrenia. Schizophr. Bull. 13, 261–276 (1987).
pubmed: 3616518
doi: 10.1093/schbul/13.2.261
Wimberley, T. et al. Predictors of treatment resistance in patients with schizophrenia: a population-based cohort study. Lancet Psychiatry 3, 358–366 (2016).
pubmed: 26922475
doi: 10.1016/S2215-0366(15)00575-1
Nelson, H. E. & O’Connell, A. Dementia: the estimation of premorbid intelligence levels using the New Adult Reading Test. Cortex 14, 234–244 (1978).
pubmed: 679704
doi: 10.1016/S0010-9452(78)80049-5
Wechsler, D. Manual for the Wechsler Adult Intelligence Scale (WAIS) (The Psychological Corporation, 1955).
Wechsler, D. WAIS-III Administration and Scoring Manual (The Psychological Corporation, 1997).
Robbins, T. W. et al. Cambridge Neuropsychological Test Automated Battery (CANTAB): a factor analytic study of a large sample of normal elderly volunteers. DEM 5, 266–281 (1994).
Keefe, R. S. E. et al. The brief assessment of cognition in schizophrenia: reliability, sensitivity, and comparison with a standard neurocognitive battery. Schizophr. Res. 68, 283–297 (2004).
pubmed: 15099610
doi: 10.1016/j.schres.2003.09.011
Buschke, H. Selective reminding for analysis of memory and learning. J. Verbal Learn. Verbal Behav. 12, 543–550 (1973).
doi: 10.1016/S0022-5371(73)80034-9
Smith, A. Symbol Digit Modalities Test (Western Psychological Services, Los Angeles, CA, 1982).
Reitan, R. & Wolfson, D. The Halstead-Reitan Neuropsychological Test Battery: Theory and Clinical Interpretation. Neuropsychology Press; 2nd edition (1993).
Milner, B. Effects of different brain lesions on card sorting: the role of the frontal lobes. Arch. Neurol. 9, 90–100 (1963).
doi: 10.1001/archneur.1963.00460070100010
Baddeley, A., Emslie, H. & Nimmo-Smith, I. The Speed and Capacity of Language-Processing Test (SCOLP)—Reference Materials (Pearson Assessment, 1992).
Jessen, K. et al. Cortical structures and their clinical correlates in antipsychotic-naïve schizophrenia patients before and after 6 weeks of dopamine D2/3 receptor antagonist treatment. Psychol. Med. 49, 754–763 (2019).
pubmed: 29734953
doi: 10.1017/S0033291718001198
Reuter, M., Rosas, H. D. & Fischl, B. Highly accurate inverse consistent registration: a robust approach. NeuroImage 53, 1181–1196 (2010).
pubmed: 20637289
doi: 10.1016/j.neuroimage.2010.07.020
Reuter, M. & Fischl, B. Avoiding asymmetry-induced bias in longitudinal image processing. NeuroImage 57, 19–21 (2011).
pubmed: 21376812
doi: 10.1016/j.neuroimage.2011.02.076
Reuter, M., Schmansky, N. J., Rosas, H. D. & Fischl, B. Within-subject template estimation for unbiased longitudinal image analysis. NeuroImage 61, 1402–1418 (2012).
pubmed: 22430496
doi: 10.1016/j.neuroimage.2012.02.084
Desikan, R. S. et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage 31, 968–980 (2006).
doi: 10.1016/j.neuroimage.2006.01.021
pubmed: 16530430
Jenkinson, M., Beckmann, C. F., Behrens, T. E. J., Woolrich, M. W. & Smith, S. M. FSL. NeuroImage 62, 782–790 (2012).
pubmed: 21979382
doi: 10.1016/j.neuroimage.2011.09.015
Jensen, K. S., Oranje, B., Wienberg, M. & Glenthøj, B. Y. The effects of increased serotonergic activity on human sensory gating and its neural generators. Psychopharmacology 196, 631–641 (2008).
pubmed: 18000656
doi: 10.1007/s00213-007-1001-y
Oranje, B., Jensen, K., Wienberg, M. & Glenthøj, B. Y. Divergent effects of increased serotonergic activity on psychophysiological parameters of human attention. Int. J. Neuropsychopharmacol. 11, 453–463 (2008).
pubmed: 17971261
doi: 10.1017/S1461145707008176
Oranje, B. & Glenthøj, B. Y. Clonidine normalizes sensorimotor gating deficits in patients with schizophrenia on stable medication. Schizophrenia Bull. 39, 684–691 (2013).
doi: 10.1093/schbul/sbs071
Düring, S., Glenthøj, B. Y., Andersen, G. S. & Oranje, B. Effects of dopamine D2/D3 blockade on human sensory and sensorimotor gating in initially antipsychotic-naive, first-episode schizophrenia patients. Neuropsychopharmacology 39, 3000–3008 (2014).
pubmed: 24954063
pmcid: 4229570
doi: 10.1038/npp.2014.152
Düring, S., Glenthøj, B. Y. & Oranje, B. Effects of blocking D2/D3 receptors on mismatch negativity and P3a amplitude of initially antipsychotic naïve, first episode schizophrenia patients. Int. J. Neuropsychopharmacol. 19, 3 pyv109, https://doi.org/10.1093/ijnp/pyv109 (2015).
Donders, A. R. T., van der Heijden, G. J. M. G., Stijnen, T. & Moons, K. G. M. Review: A gentle introduction to imputation of missing values. J. Clin. Epidemiol. 59, 1087–1091 (2006).
pubmed: 16980149
doi: 10.1016/j.jclinepi.2006.01.014
Tipping, M. E. & Bishop, C. M. Mixtures of probabilistic principal component analyzers. Neural Comput. 11, 443–482 (1999).
pubmed: 9950739
doi: 10.1162/089976699300016728
Hansen, L. K. et al. Generalizable patterns in neuroimaging: how many principal components? NeuroImage 9, 534–544 (1999).
pubmed: 10329293
doi: 10.1006/nimg.1998.0425
Everitt, B. S. An Introduction to Latent Variable Models (Springer Science & Business Media, 2013).
Mouchlianitis, E., McCutcheon, R. & Howes, O. D. Brain-imaging studies of treatment-resistant schizophrenia: a systematic review. Lancet Psychiatry 3, 451–463 (2016).
pubmed: 26948188
pmcid: 5796640
doi: 10.1016/S2215-0366(15)00540-4
Feurer, M. et al. in Advances in Neural Information Processing Systems Vol. 28 (eds Cortes, C. et al.) 2962–2970 (Curran Associates, Inc., 2015).
Keefe, R. S. E., Eesley, C. E. & Poe, M. P. Defining a cognitive function decrement in schizophrenia. Biol. Psychiatry 57, 688–691 (2005).
pubmed: 15780858
doi: 10.1016/j.biopsych.2005.01.003
Woodberry, K. A. & Giuliano, A. J.,. & Seidman, L. J. Premorbid IQ in schizophrenia: a meta-analytic review. Am. J. Psychiatry 165, 579–587 (2008).
pubmed: 18413704
doi: 10.1176/appi.ajp.2008.07081242
Ipsen, N. B. & Hansen, L. K. Phase transition in PCA with missing data: Reduced signal-to-noise ratio, not sample size! In proceedings of machine learning research. Int. Machine Lean. Society (IMLS) 97, 5248–5260 (2019).
Nordentoft, M. et al. From research to practice: how OPUS treatment was accepted and implemented throughout Denmark. Early Interv. Psychiatry 9, 156–162 (2015).
pubmed: 24304658
doi: 10.1111/eip.12108
Pantelis, C. et al. Neurobiological markers of illness onset in psychosis and schizophrenia: the search for a moving target. Neuropsychol. Rev. 19, 385 (2009).
pubmed: 19728098
doi: 10.1007/s11065-009-9114-1
Doucet, G. E., Moser, D. A., Luber, M. J., Leibu, E. & Frangou, S. Baseline brain structural and functional predictors of clinical outcome in the early course of schizophrenia. Mol. Psychiatry https://doi.org/10.1038/s41380-018-0269-0 (2018).
Bak, N. & Hansen, L. K. Data driven estimation of imputation error—a strategy for imputation with a reject option. PLoS ONE 11, e0164464 (2016).
pubmed: 27723782
pmcid: 5056679
doi: 10.1371/journal.pone.0164464
Oldfield, R. C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97–113 (1971).
doi: 10.1016/0028-3932(71)90067-4
pubmed: 5146491
Crespo-Facorro, B. et al. Caudate nucleus volume and its clinical and cognitive correlations in first episode schizophrenia. Schizophr. Res. 91, 87–96 (2007).
pubmed: 17306506
doi: 10.1016/j.schres.2006.12.015