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Combining quantitative susceptibility mapping to radiomics in diagnosing Parkinson’s disease and assessing cognitive impairment

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Abstract

Objective

To explore whether magnetic susceptibility value (MSV) and radiomics features of the nigrostriatal system could be used as imaging markers for diagnosing Parkinson’s disease (PD) and its related cognitive impairment (CI).

Methods

A total of 104 PD patients and 45 age-sex-matched healthy controls (HCs) underwent quantitative susceptibility mapping (QSM). The former completed Hoehn-Yahr Stage and Montreal Cognitive Assessment (MoCA). The patients were divided into several subgroups according to disease stages, courses, and MoCA scores. The ROI was subdivided into the substantia nigra (SN), head of caudate nucleus (HCN), and putamen. The MSVs and radiomics features were obtained from QSM. The multivariable logistic regression (MLR) and support vector machine (SVM) models were constructed to diagnose PD. The correlations between MSVs, radiomics features, and MoCA scores were evaluated.

Results

The MSVs in bilateral SN pars compacta (SNc) of PD patients were higher than those of the HCs (p < 0.001). There were differences in some radiomics features between the two groups (p < 0.05). The MSVs of the right SNc and the radiomics features of the right SN had the highest area under the curve (AUC), respectively. The comprehensive MLR model (0.90) and SVM model (0.95) revealed better classification performance than MSVs (p < 0.05) in diagnosing PD. The MSVs from the HCN were negatively correlated with MoCA scores in PD subgroups. There were correlations between radiomics features and MoCA scores in PD patients.

Conclusions

Radiomics features and MSVs of the nigrostriatal system from QSM could have crucial role in diagnosing PD and assessing CI.

Key Points

The MLR and the SVM models have excellent diagnostic performance in the diagnosis of PD.

A PD diagnostic nomogram, created based on MSV and the radiomics scores of SVM model, is very convenient for clinical use.

The radiomics features of the nigrostriatal system based on QSM help to evaluate the cognitive impairment in PD patients.

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Abbreviations

CI:

Cognitive impairment

HC:

Healthy control

HCN:

Head of caudate nucleus

H-Y:

Hoehn-Yahr

MLR:

Multivariate logistic regression

MoCA:

Montreal Cognitive Assessment

MSV:

Magnetic susceptibility value

PD:

Parkinson’s disease

PUT:

Putamen

QSM:

Quantitative susceptibility mapping

SN:

Substantia nigra

SNc:

SN pars compacta

SNr:

SN pars reticulata

SVM:

Support vector machine

References

  1. Tysnes OB, Storstein A (2017) Epidemiology of Parkinson’s disease. J Neural Transm (Vienna) 124:901–905

    Article  Google Scholar 

  2. Acosta-Cabronero J, Cardenas-Blanco A, Betts MJ et al (2017) The whole-brain pattern of magnetic susceptibility perturbations in Parkinson’s disease. Brain 140:118–131

    Article  Google Scholar 

  3. An H, Zeng X, Niu T et al (2018) Quantifying iron deposition within the substantia nigra of Parkinson’s disease by quantitative susceptibility mapping. J Neurol Sci 386:46–52

    Article  CAS  Google Scholar 

  4. Ghassaban K, He N, Sethi SK et al (2019) Regional high iron in the substantia nigra differentiates Parkinson’s disease patients from healthy controls. Front Aging Neurosci. https://doi.org/10.3389/fnagi.2019.00106

  5. Deistung A, Schweser F, Reichenbach JR et al (2017) Overview of quantitative susceptibility mapping. NMR Biomed. https://doi.org/10.1002/nbm.3569

  6. Aggarwal M, Li X, Gröhn O, Sierra A (2018) Nuclei-specific deposits of iron and calcium in the rat thalamus after status epilepticus revealed with quantitative susceptibility mapping (QSM). J Magn Reson Imaging 47:554–564

    Article  Google Scholar 

  7. Chen L, Cai C, Yang T et al (2017) Changes in brain iron concentration after exposure to high-altitude hypoxia measured by quantitative susceptibility mapping. Neuroimage 147:488–499

    Article  Google Scholar 

  8. Li H, Gao L, Ma H et al (2021) Radiomics-based features for prediction of histological subtypes in central lung cancer. Front Oncol. https://doi.org/10.3389/fonc.2021.658887

  9. Xiao B, He N, Wang Q et al (2019) Quantitative susceptibility mapping based hybrid feature extraction for diagnosis of Parkinson’s disease. Neuroimage Clin. https://doi.org/10.1016/j.nicl.2019.102070

  10. Shu ZY, Cui SJ, Wu X et al (2021) Predicting the progression of Parkinson’s disease using conventional MRI and machine learning: an application of radiomic biomarkers in whole-brain white matter. Magn Reson Med 85:1611–1624

    Article  Google Scholar 

  11. Salmanpour MR, Shamsaei M, Saberi A, Hajianfar G, Soltanian-Zadeh H, Rahmim A (2021) Robust identification of Parkinson’s disease subtypes using radiomics and hybrid machine learning. Comput Biol Med. https://doi.org/10.1016/j.compbiomed.2020.104142

  12. Monastero R, Cicero CE, Baschi R et al (2018) Mild cognitive impairment in Parkinson’s disease: the Parkinson’s disease cognitive study (PACOS). J Neurol 265:1050–1058

    Article  Google Scholar 

  13. Baschi R, Restivo V, Nicoletti A et al (2019) Mild behavioral impairment in Parkinson’s disease: data from the Parkinson’s Disease Cognitive Impairment Study (PACOS). J Alzheimers Dis 68:1603–1610

    Article  Google Scholar 

  14. Uchida Y, Kan H, Sakurai K et al (2019) Voxel-based quantitative susceptibility mapping in Parkinson’s disease with mild cognitive impairment. Mov Disord 34:1164–1173

    Article  CAS  Google Scholar 

  15. Thomas GEC, Leyland LA, Schrag AE, Lees AJ, Acosta-Cabronero J, Weil RS (2020) Brain iron deposition is linked with cognitive severity in Parkinson’s disease. J Neurol Neurosurg Psychiatry 91:418–425

    Article  Google Scholar 

  16. Li DTH, Hui ES, Chan Q et al (2018) Quantitative susceptibility mapping as an indicator of subcortical and limbic iron abnormality in Parkinson’s disease with dementia. Neuroimage Clin 20:365–373

    Article  Google Scholar 

  17. Betrouni N, Lopes R, Defebvre L, Leentjens AFG, Dujardin K (2020) Texture features of magnetic resonance images: a marker of slight cognitive deficits in Parkinson’s disease. Mov Disord 35:486–494

    Article  Google Scholar 

  18. Postuma RB, Berg D, Stern M et al (2015) MDS clinical diagnostic criteria for Parkinson’s disease. Mov Disord 30:1591–1601

    Article  Google Scholar 

  19. Smith GS, Mills KA, Pontone GM et al (2019) Effect of STN DBS on vesicular monoamine transporter 2 and glucose metabolism in Parkinson’s disease. Parkinsonism Relat Disord 64:235–241

    Article  Google Scholar 

  20. Dowling P, Klinker F, Stadelmann C et al (2011) Dopamine D3 receptor specifically modulates motor and sensory symptoms in iron-deficient mice. J Neurosci 31:70–77

    Article  CAS  Google Scholar 

  21. Verschuur CVM, Suwijn SR, Boel JA et al (2019) Randomized delayed-start trial of levodopa in Parkinson’s disease. N Engl J Med 380:315–324

    Article  CAS  Google Scholar 

  22. Dalrymple-Alford JC, MacAskill MR, Nakas CT et al (2010) The MoCA: well-suited screen for cognitive impairment in Parkinson disease. Neurology 75:1717–1725

    Article  CAS  Google Scholar 

  23. van Griethuysen JJM, Fedorov A, Parmar C et al (2017) Computational radiomics system to decode the radiographic phenotype. Cancer Res 77(21):e104–e107

    Article  Google Scholar 

  24. Ma DN, Gao XY, Dan YB et al (2020) Evaluating solid lung adenocarcinoma anaplastic lymphoma kinase gene rearrangement using noninvasive radiomics biomarkers. Onco Targets Ther 13:6927–6935

    Article  Google Scholar 

  25. Mazzucchi S, Frosini D, Costagli M et al (2019) Quantitative susceptibility mapping in atypical Parkinsonisms. Neuroimage Clin. https://doi.org/10.1016/j.nicl.2019.101999

  26. Shahmaei V, Faeghi F, Mohammdbeigi A, Hashemi H, Ashrafi F (2019) Evaluation of iron deposition in brain basal ganglia of patients with Parkinson’s disease using quantitative susceptibility mapping. Eur J Radiol Open 6:169–174

    Article  Google Scholar 

  27. Liu P, Wang H, Zheng S, Zhang F, Zhang X (2020) Parkinson’s disease diagnosis using neostriatum radiomic features based on T2-weighted magnetic resonance imaging. Front Neurol. https://doi.org/10.3389/fneur.2020.00248

  28. Cao X, Wang X, Xue C, Zhang S, Huang Q, Liu W (2020) A radiomics approach to predicting Parkinson’s disease by incorporating whole-brain functional activity and gray matter structure. Front Neurosci. https://doi.org/10.3389/fnins.2020.00751

  29. Uchida Y, Kan H, Sakurai K et al (2020) Magnetic susceptibility associates with dopaminergic deficits and cognition in Parkinson’s disease. Mov Disord 35:1396–1405

    Article  CAS  Google Scholar 

  30. Wang N, Liu XL, Li L et al (2021) Screening for early-stage Parkinson’s disease: swallow tail sign on MRI susceptibility map-weighted images compared with PET. J Magn Reson Imaging 53(3):722–730

    Article  Google Scholar 

  31. Piccardo A, Cappuccio R, Bottoni G et al (2021) The role of the deep convolutional neural network as an aid to interpreting brain [18F] DOPA PET/CT in the diagnosis of Parkinson's disease [J]. Eur Radiol 31(9):7003–7011

    Article  Google Scholar 

  32. Cheng Z, Zhang J, He N et al (2019) Radiomic features of the nigrosome-1 region of the substantia nigra: using quantitative susceptibility mapping to assist the diagnosis of idiopathic Parkinson’s disease. Front Aging Neurosci. https://doi.org/10.3389/fnagi.2019.00167

  33. Shu Z, Pang P, Wu X, Cui S, Xu Y, Zhang M (2020) An integrative nomogram for identifying early-stage Parkinson’s disease using non-motor symptoms and white matter-based radiomics biomarkers from whole-brain MRI. Front Aging Neurosci. https://doi.org/10.3389/fnagi.2020.548616

  34. Kim JS, Oh YS, Lee KS, Kim YI, Yang DW, Goldstein DS (2012) Association of cognitive dysfunction with neurocirculatory abnormalities in early Parkinson disease. Neurology 79(13):1323–1331

    Article  Google Scholar 

  35. Apostolova LG, Beyer M, Green AE et al (2010) Hippocampal, caudate, and ventricular changes in Parkinson’s disease with and without dementia. Mov Disord 25:687–695

    Article  Google Scholar 

  36. Pasquini J, Durcan R, Wiblin L et al (2019) Clinical implications of early caudate dysfunction in Parkinson’s disease. J Neurol Neurosurg Psychiatry 90:1098–1104

    Article  Google Scholar 

  37. Rahmim A, Salimpour Y, Jain S et al (2016) Application of texture analysis to DAT SPECT imaging: relationship to clinical assessments. Neuroimage Clin 12:e1–e9

    Article  Google Scholar 

  38. Jin ZJ, Wang Y, Jokar M et al (2022) Automatic detection of neuromelanin and iron in the midbrain nuclei using a magnetic resonance imaging-based brain template. Hum Brain Mapp. https://doi.org/10.1002/hbm.25770

  39. Lewis MM, Du GW, Kidacki M et al (2013) Higher iron in the red nucleus marks Parkinson’s dyskinesia. Neurobiol Aging 34:1497–1503

    Article  CAS  Google Scholar 

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Acknowledgements

We would like to thank the radiographers in Affiliated Hospital of Nantong University for their professional assistance and MRI scans.

Funding

This study has received funding by the Jiangsu Provincial Health Commission (No. H2019089) and the Nantong Science and Technology Project (No. MS12020044).

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Corresponding authors

Correspondence to Li Hua Shen or Zhong Zheng Jia.

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Guarantor

The scientific guarantor of this publication is Jin Juan Kang.

Conflict of interest

The authors declare no conflicts of interest.

Statistics and biometry

No complex statistical methods were necessary for this paper.

Informed consent

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

Ethical approval

This study was approved by the institutional review board (Ethics Committee of Affiliated Hospital of Nantong University).

Methodology

• retrospective

• diagnostic and prognostic study

• performed at one institution

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Kang, J.J., Chen, Y., Xu, G.D. et al. Combining quantitative susceptibility mapping to radiomics in diagnosing Parkinson’s disease and assessing cognitive impairment. Eur Radiol 32, 6992–7003 (2022). https://doi.org/10.1007/s00330-022-08790-8

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  • DOI: https://doi.org/10.1007/s00330-022-08790-8

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