Skip to main content

Advertisement

Log in

Identifying Parkinson’s disease with mild cognitive impairment by using combined MR imaging and electroencephalogram

  • Neuro
  • Published:
European Radiology Aims and scope Submit manuscript

A Correction to this article was published on 23 July 2021

This article has been updated

Abstract

Objectives

To analyse the changes of quantitative electroencephalogram (qEEG) and cortex structural magnetic resonance (MR) imaging in Parkinson’s disease with mild cognitive impairment (PD-MCI) and to explore the “composite marker”–based machine learning model in identifying PD-MCI.

Methods

Retrospective analysis of patients with PD identified 36 PD-MCI and 35 PD with normal cognition (PD-NC). QEEG features of power spectrum and structural MR features of cortex based on surface-based morphometry (SBM) were extracted. Support vector machine (SVM) was established using combined features of structural MR and qEEG to identify PD-MCI. Feature importance evaluation algorithm of mean impact value (MIV) was established to sort the vital characteristics of qEEG and structural MR.

Results

Compared with PD-NC, PD-MCI showed a statistically significant difference in 5 leads and waves of qEEG and 7 cortical region features of structural MR. The SVM model based on these qEEG and structural MR features yielded an accuracy of 0.80 in the training set and had a high prediction accuracy of 0.80 in the test set (sensitivity was 0.78, specificity was 0.83, area under the receiver operating characteristic curve was 0.77), which was higher than the model built by the feature separately. QEEG features of theta wave in C3 had a marked impact on the model for classification according to the MIV algorithm.

Conclusions

PD-MCI is characterized by widespread structural and EEG abnormality. “Composite markers” could be valuable for the individualized diagnosis of PD-MCI by machine learning.

Key Points

• Explore the brain abnormalities in Parkinson’s disease with mild cognitive impairment by using the quantitative electroencephalogram and cortex structural MR simultaneously.

• Multimodal features based support vector machine for identifying Parkinson’s disease with mild cognitive impairment has an acceptable performance.

• Theta wave in C3 is the most influential feature of qEEG and cortex structure MR imaging in identifying Parkinson’s disease with mild cognitive impairment using support vector machine.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Change history

Abbreviations

MIV:

Mean impact value

MR:

Magnetic resonance

PD:

Parkinson’s disease

PD-MCI:

Parkinson’s disease with mild cognitive impairment

PD-NC:

Parkinson’s disease with normal cognition

QEEG:

Quantitative electroencephalogram

ROC:

Receiver operating characteristic

SBM:

Surface-based morphometry

SVM:

Support vector machine

References

  1. Duncan GW, Khoo TK, Yarnall AJ et al (2014) Health-related quality of life in early Parkinson’s disease: the impact of nonmotor symptoms. Mov Disord 29(2):195–202

    Article  Google Scholar 

  2. Savica R, Grossardt BR, Rocca WA, Bower JH (2018) Parkinson disease with and without dementia: a prevalence study and future projections. Mov Disord 33(4):537–543

    Article  Google Scholar 

  3. Winer JR, Maass A, Pressman P et al (2018) Associations between tau, beta-amyloid, and cognition in Parkinson disease. JAMA Neurol 75(2):227–235

    Article  Google Scholar 

  4. Aarsland D, Creese B, Politis M et al (2017) Cognitive decline in Parkinson disease. Nat Rev Neurol 13(4):217–231

    Article  Google Scholar 

  5. Backstrom D, Granasen G, Domellof ME et al (2018) Early predictors of mortality in parkinsonism and Parkinson disease: a population-based study. Neurology 91(22):e2045–e2056

    Article  Google Scholar 

  6. Litvan I, Kieburtz K, Troster AI, Aarsland D (2018) Strengths and challenges in conducting clinical trials in Parkinson’s disease mild cognitive impairment. Mov Disord 33(4):520–527

    Article  Google Scholar 

  7. Meyer PT, Frings L, Rücker G, Hellwig S (2017) (18)F-FDG PET in parkinsonism: differential diagnosis and cognitive impairment in Parkinson’s disease. J Nucl Med 58(12)

  8. Glaab E, Trezzi JP, Greuel A et al (2019) Integrative analysis of blood metabolomics and PET brain neuroimaging data for Parkinson’s disease. Neurobiol Dis 124:555–562

    Article  CAS  Google Scholar 

  9. Kalia LV (2018) Biomarkers for cognitive dysfunction in Parkinson’s disease. Parkinsonism Relat Disord 46(Suppl 1):S19–S23

    Article  Google Scholar 

  10. Lanskey JH, Mccolgan P, Schrag AE et al (2018) Can neuroimaging predict dementia in Parkinson’s disease? Brain 141(9):2545–2560

    PubMed  PubMed Central  Google Scholar 

  11. Svenningsson P, Westman E, Ballard C, Aarsland D (2012) Cognitive impairment in patients with Parkinson’s disease: diagnosis, biomarkers, and treatment. Lancet Neurol 11(8):697–707

    Article  Google Scholar 

  12. Delgado-Alvarado M, Gago B, Navalpotro-Gomez I, Jimenez-Urbieta H, Rodriguez-Oroz MC (2016) Biomarkers for dementia and mild cognitive impairment in Parkinson’s disease. Mov Disord 31(6):861–881

    Article  Google Scholar 

  13. Arnaldi D, De Carli F, Fama F et al (2017) Prediction of cognitive worsening in de novo Parkinson’s disease: clinical use of biomarkers. Mov Disord 32(12):1738–1747

    Article  Google Scholar 

  14. Betrouni N, Delval A, Chaton L et al (2019) Electroencephalography-based machine learning for cognitive profiling in Parkinson’s disease: preliminary results. Mov Disord 34(2):210–217

    Article  Google Scholar 

  15. Morales DA, Vives-Gilabert Y, Gomez-Anson B et al (2013) Predicting dementia development in Parkinson’s disease using Bayesian network classifiers. Psychiatry Res 213(2):92–98

    Article  Google Scholar 

  16. Gelb DJ, Oliver E, Gilman S (1999) Diagnostic criteria for Parkinson disease. Arch Neurol 56(1):33–39

    Article  CAS  Google Scholar 

  17. Emre M, Aarsland D, Brown R et al (2007) Clinical diagnostic criteria for dementia associated with Parkinson’s disease. Mov Disord 22(12):1689–1707 quiz 1837

    Article  Google Scholar 

  18. Litvan I, Goldman JG, Troster AI et al (2012) Diagnostic criteria for mild cognitive impairment in Parkinson's disease: Movement Disorder Society Task Force guidelines. Mov Disord 27(3):349–356

    Article  Google Scholar 

  19. Mckeown M (2003) Independent component analysis of functional MRI: what is signal and what is noise? Curr Opin Neurobiol 13(5):620–629

    Article  CAS  Google Scholar 

  20. Chang CC, Lin CJ (2011) LIBSVM: a library for support vector machines. ACM Trans Intell Syst Technol 2(3):1–27

    Article  Google Scholar 

  21. Gromski PS, Xu Y, Correa E et al (2014) A comparative investigation of modern feature selection and classification approaches for the analysis of mass spectrometry data. Anal Chim Acta 829:1–8

    Article  CAS  Google Scholar 

  22. Jiang JL, Su X, Zhang H, Zhang XH, Yuan YJ (2013) A novel approach to active compounds identification based on support vector regression model and mean impact value. Chem Biol Drug Des 81(5):650–657

    Article  CAS  Google Scholar 

  23. Zhang JH, Han X, Zhao HW et al (2018) Personalized prediction model for seizure-free epilepsy with levetiracetam therapy: a retrospective d ata analysis using support vector machine. Br J Clin Pharmacol 84(11):2615–2624

    Article  CAS  Google Scholar 

  24. Gao Y, Nie K, Mei M et al (2018) Changes in cortical thickness in patients with early Parkinson’s disease at different Hoehn and Yahr stages. Front Hum Neurosci 12:469

    Article  Google Scholar 

  25. Kamagata K, Motoi Y, Tomiyama H et al (2013) Relationship between cognitive impairment and white-matter alteration in Parkinson's disease with dem entia: tract-based spatial statistics and tract-specific analysis. Eur Radiol 23(7):1946–1955

    Article  Google Scholar 

  26. Caviness JN, Lue LF, Hentz JG et al (2016) Cortical phosphorylated alpha-Synuclein levels correlate with brain wave spectra in Parkinson’s disease. Mov Disord 31(7):1012–1019

    Article  CAS  Google Scholar 

  27. De Benedictis A, Duffau H (2011) Brain hodotopy: from esoteric concept to practical surgical applications. Neurosurgery 68(6):1709–1723 discussion 1723

    Article  Google Scholar 

  28. Wolters AF, van de Weijer SCF, Leentjens AFG, Duits AA, Jacobs HIL, Kuijf ML (2019) Resting-state fMRI in Parkinson's disease patients with cognitive impairment: a meta-analysis. Parkinsonism Relat Disord 62:16–27

  29. Wang W, Mei M, Gao Y et al (2020) Changes of brain structural network connection in Parkinson’s disease patients with mild cognitive dy sfunction: a study based on diffusion tensor imaging. J Neurol 267(4):933–943

    Article  Google Scholar 

  30. Bratic B, Kurbalija V, Ivanovic M, Oder I, Bosnic Z (2018) Machine learning for predicting cognitive diseases: methods, data sources and risk factors. J Med Syst 42(12):243

    Article  Google Scholar 

  31. Ma Z, Wang P, Gao Z, Wang R, Khalighi K (2018) Ensemble of machine learning algorithms using the stacked generalization approach to estimate the warfarin dose. PLoS One 13(10):e0205872

    Article  Google Scholar 

  32. Bonanni L (2019) The democratic aspect of machine learning: limitations and opportunities for Parkinson’s disease. Mov Disord 34(2):164–166

    Article  Google Scholar 

  33. Schrag A, Siddiqui UF, Anastasiou Z, Weintraub D, Schott JM (2017) Clinical variables and biomarkers in prediction of cognitive impairment in patients with newly diagnosed Parkinson’s disease: a cohort study. Lancet Neurol 16(1):66–75

    Article  CAS  Google Scholar 

  34. Liu G, Locascio JJ, Corvol JC et al (2017) Prediction of cognition in Parkinson’s disease with a clinical-genetic score: a longitudinal analysis of nine cohorts. Lancet Neurol 16(8):620–629

    Article  Google Scholar 

  35. Anang JB, Gagnon JF, Bertrand JA et al (2014) Predictors of dementia in Parkinson disease: a prospective cohort study. Neurology 83(14):1253–1260

    Article  Google Scholar 

  36. Prashanth R, Dutta RS, Mandal PK, Ghosh S (2016) High-accuracy detection of early Parkinson’s disease through multimodal features and machine learning. Int J Med Inform 90:13–21

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank the support of the patients, their families, and control subjects for the study.

Funding

This study has received funding from the National Natural Science Foundation of China (No. 81501112), Guangdong Natural Science Foundation (No. 2016A030310327), Guangdong Natural Science Foundation (No. 2019A1515110061), National Key R&D Program of China (No. 2017YFC1310200), The Fundamental Research Funds for the Central Universities (No. 2018MS27), Key Program of Natural Science Foundation of Guangdong Province, China (No. 2017B030311015), Guangzhou Municipal People’s Livelihood Science and Technology Project (No. 201803010085), and Medical Science and Technology Foundation of Guangdong Province (No. A2018137).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Kun Nie or Lijuan Wang.

Ethics declarations

Guarantor

The guarantor name of this publication is Lijuan Wang.

Conflict of interest

The authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article.

Statistics and biometry

One of the authors has significant statistical expertise.

Informed consent

Written informed consent was obtained from all subjects (patients) in this study.

Ethical approval

The study had been approved by Guangdong General Hospital for Research with Human Subjects (Ethical Approval No. GDREC2015195H).

Study subjects or cohorts overlap

Some study subjects or cohorts have been previously reported in the article (Gao, Y., K. Nie, M. Mei, et al, Changes in Cortical Thickness in Patients With Early Parkinson’s Disease at Different Hoehn and Yahr Stages. Front Hum Neurosci, 2018. 12: p. 469.)

Methodology

• retrospective

• observational

• performed at one institution

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The original online version of this article was revised: The information was missing that Jiahui Zhang and Yuyuan Gao are co-first authors and that Kun Nie and Lijuan Wang are co-corresponding authors, and the presentation of Figure 2 was incorrect.

Jiahui Zhang and Yuyuan Gao are co-first authors.

Kun Nie and Lijuan Wang are co-corresponding authors

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, J., Gao, Y., He, X. et al. Identifying Parkinson’s disease with mild cognitive impairment by using combined MR imaging and electroencephalogram. Eur Radiol 31, 7386–7394 (2021). https://doi.org/10.1007/s00330-020-07575-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-020-07575-1

Keywords

Navigation