Skip to main content
Log in

Potential usefulness of signal intensity of cerebral gyri on quantitative susceptibility mapping for discriminating corticobasal degeneration from progressive supranuclear palsy and Parkinson’s disease

  • Diagnostic Neuroradiology
  • Published:
Neuroradiology Aims and scope Submit manuscript

Abstract

Purpose

The typical MRI findings in corticobasal degeneration (CBD), which have been described in previous reports, may be non-specific. We evaluated cerebral gyri (CG) using quantitative susceptibility mapping (QSM) images of patients with CBD, progressive supranuclear palsy (PSP), and Parkinson’s disease (PD) to determine the possibility of discriminating them on an individual basis.

Methods

After reviewing the normal appearances on QSM on 16 healthy subjects, two radiologists assessed abnormal findings from 12 CBD, 14 PSP, and 30 PD patients. For conventional MRI, two radiologists independently reviewed typical CBD findings that have been previously reported. We also investigated three autopsy cases including one each of CBD, PSP, and PD to reveal the histopathological basis of MRI findings.

Results

CBD-specific findings included three layers; a higher susceptibility layer in superficial GM, a lower susceptibility layer, and a higher susceptibility layer in corticomedullary junction, with frequencies of 83% (10/12) in CBD, 21% (3/14) in PSP, and 0% (0/30) in PD patients. The typical CBD findings on conventional MRI were observed in only 42% (5/12) of CBD patients. Ferritin-positive microglia accumulated in the superficial gray matter (third cortical layer) and corticomedullary junction in CBD patients.

Conclusions

The CG findings on QSM images may be more useful than those on conventional MRI for discriminating CBD from PD on an individual basis. Based on postmortem pathological data, cortical QSM hyperintensity might be an expression of ferritin-positive microglia.

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
Fig. 4

Similar content being viewed by others

Abbreviations

CBD:

Corticobasal degeneration

CG:

Cerebral gyri

GM:

Gray matter

PD:

Parkinson’s disease

PSP:

Progressive supranuclear palsy

QSM:

Quantitative susceptibility mapping

WM:

White matter

References

  1. Hess C, Christine C, Apple A et al (2014) Changes in the thalamus in atypical parkinsonism detected using shape analysis and diffusion tensor imaging. Am J Neuroradiol 35:897–903

    Article  CAS  Google Scholar 

  2. Kakeda S, Yoneda T, Ide S, Miyata M, Hashimoto T, Futatsuya K, Watanabe K, Ogasawara A, Moriya J, Sato T, Okada K, Uozumi T, Adachi H, Korogi Y (2016) Zebra sign of precentral gyri in amyotrophic lateral sclerosis: a novel finding using phase difference enhanced (PADRE) imaging-initial results. Eur Radiol 26:4173–4183

    Article  Google Scholar 

  3. Litvan I, Grimes D, Lang A et al (1999) Clinical features differentiating patients with postmortem confirmed progressive supranuclear palsy and corticobasal degeneration. J Neurol 246:II1–II5

    Article  Google Scholar 

  4. Scaravilli T, Tolosa E, Ferrer I (2005) Progressive supranuclear palsy and corticobasal degeneration: lumping versus splitting. Mov Disord 20:S21–S28

    Article  Google Scholar 

  5. Soliveri P, Monza D, Paridi D, Radice D, Grisoli M, Testa D, Savoiardo M, Girotti F (1999) Cognitive and magnetic resonance imaging aspects of corticobasal degeneration and progressive supranuclear palsy. Neurology 53:502–507

    Article  CAS  Google Scholar 

  6. Savoiardo M (2003) Differential diagnosis of Parkinson's disease and atypical parkinsonian disorders by magnetic resonance imaging. Neurol Sci 24:s35–s37

    Article  Google Scholar 

  7. Ide S, Kakeda S, Ueda I, Watanabe K, Murakami Y, Moriya J, Ogasawara A, Futatsuya K, Sato T, Ohnari N, Okada K, Matsuyama A, Fujiwara H, Hisaoka M, Tsuji S, Liu T, Wang Y, Korogi Y (2015) Internal structures of the globus pallidus in patients with Parkinson’s disease: evaluation with quantitative susceptibility mapping (QSM). Eur Radiol 25:710–718

    Article  Google Scholar 

  8. Liu T, Surapaneni K, Lou M, Cheng L, Spincemaille P, Wang Y (2012) Cerebral microbleeds: burden assessment by using quantitative susceptibility mapping. Radiology 262:269–278

    Article  Google Scholar 

  9. Ogasawara A, Kakeda S, Watanabe K, Ide S, Ueda I, Murakami Y, Moriya J, Futatsuya K, Sato T, Nakayamada S, Saito K, Tanaka Y, Liu T, Wang Y, Korogi Y (2016) Quantitative susceptibility mapping in patients with systemic lupus erythematosus: detection of abnormalities in normal-appearing basal ganglia. Eur Radiol 26:1056–1063

    Article  Google Scholar 

  10. Schweitzer AD, Liu T, Gupta A, Zheng K, Seedial S, Shtilbans A, Shahbazi M, Lange D, Wang Y, Tsiouris AJ (2015) Quantitative susceptibility mapping of the motor cortex in amyotrophic lateral sclerosis and primary lateral sclerosis. Am J Roentgenol 204:1086–1092

    Article  Google Scholar 

  11. Sjöström H, Granberg T, Westman E, Svenningsson P (2017) Quantitative susceptibility mapping differentiates between parkinsonian disorders. Parkinsonism Relat Disord 44:51–57

    Article  Google Scholar 

  12. Ito K, Ohtsuka C, Yoshioka K, Kameda H, Yokosawa S, Sato R, Terayama Y, Sasaki M (2017) Differential diagnosis of parkinsonism by a combined use of diffusion kurtosis imaging and quantitative susceptibility mapping. Neuroradiology 59(8):759–769

    Article  Google Scholar 

  13. Murakami Y, Kakeda S, Watanabe K et al (2015) Usefulness of quantitative susceptibility mapping for the diagnosis of Parkinson disease. AJNR Am J Neuroradiol 36(6):1102–1108

    Article  CAS  Google Scholar 

  14. Barbosa JH, Santos AC, Tumas V et al (2015) Quantifying brain iron deposition in patients with Parkinson's disease using quantitative susceptibility mapping, R2 and R2. Magn Reson Imaging 33(5):559–565

    Article  CAS  Google Scholar 

  15. Azuma M, Hirai T, Yamada K, Yamashita S, Ando Y, Tateishi M, Iryo Y, Yoneda T, Kitajima M, Wang Y, Yamashita Y (2016) Lateral asymmetry and spatial difference of iron deposition in the substantia nigra of Parkinson’s disease patients measured with quantitative susceptibility mapping. AJNR Am J Neuroradio 37(5):782–788

    Article  CAS  Google Scholar 

  16. Wang Y, Spincemaille P, Liu Z, Dimov A, Deh K, Li J, Zhang Y, Yao Y, Gillen KM, Wilman AH, Gupta A, Tsiouris AJ, Kovanlikaya I, Chiang GCY, Weinsaft JW, Tanenbaum L, Chen W, Zhu W, Chang S, Lou M, Kopell BH, Kaplitt MG, Devos D, Hirai T, Huang X, Korogi Y, Shtilbans A, Jahng GH, Pelletier D, Gauthier SA, Pitt D, Bush AI, Brittenham GM, Prince MR (2017) Clinical quantitative susceptibility mapping (QSM): biometal imaging and its emerging roles in patient care. J Magn Reson Imaging 46(4):951–971

    Article  Google Scholar 

  17. Belfor N, Amici S, Boxer AL, Kramer JH, Gorno-Tempini ML, Rosen HJ, Miller BL (2006) Clinical and neuropsychological features of corticobasal degeneration. Mech Ageing Dev 127:203–207

    Article  Google Scholar 

  18. Dickson D, Bergeron C, Chin S et al (2002) Office of Rare Diseases neuropathologic criteria for corticobasal degeneration. J Neuropathol Exp Neurol 61:935–946

    Article  CAS  Google Scholar 

  19. Mizuno Y, Ozeki M, Iwata H, Takeuchi T, Ishihara R, Hashimoto N, Kobayashi H, Iwai K, Ogasawara S, Ukai K, Shibayama H (2002) A case of clinically and neuropathologically atypical corticobasal degeneration with widespread iron deposition. Acta Neuropathol 103:288–294

    Article  CAS  Google Scholar 

  20. Wallace MN, Cronin MJ, Bowtell RW et al (2016) Histological basis of laminar MRI patterns in high resolution images of fixed human auditory cortex. Front Neurosci 10:455

    Article  Google Scholar 

  21. Liu J, Liu T, de Rochefort L, Ledoux J, Khalidov I, Chen W, Tsiouris AJ, Wisnieff C, Spincemaille P, Prince MR, Wang Y (2012) Morphology enabled dipole inversion for quantitative susceptibility mapping using structural consistency between the magnitude image and the susceptibility map. Neuroimage 59:2560–2268

    Article  Google Scholar 

  22. Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55:181–184

    Article  CAS  Google Scholar 

  23. Armstrong MJ, Litvan I, Lang AE, Bak TH, Bhatia KP, Borroni B, Boxer AL, Dickson DW, Grossman M, Hallett M, Josephs KA, Kertesz A, Lee SE, Miller BL, Reich SG, Riley DE, Tolosa E, Troster AI, Vidailhet M, Weiner WJ (2013) Criteria for the diagnosis of corticobasal degeneration. Neurology 80:496–503

    Article  Google Scholar 

  24. Höglinger GU, Respondek G, Stamelou M, Kurz C, Josephs KA, Lang AE, Mollenhauer B, Müller U, Nilsson C, Whitwell JL, Arzberger T, Englund E, Gelpi E, Giese A, Irwin DJ, Meissner WG, Pantelyat A, Rajput A, van Swieten JC, Troakes C, Antonini A, Bhatia KP, Bordelon Y, Compta Y, Corvol JC, Colosimo C, Dickson DW, Dodel R, Ferguson L, Grossman M, Kassubek J, Krismer F, Levin J, Lorenzl S, Morris HR, Nestor P, Oertel WH, Poewe W, Rabinovici G, Rowe JB, Schellenberg GD, Seppi K, van Eimeren T, Wenning GK, Boxer AL, Golbe LI, Litvan I, for the Movement Disorder Society-endorsed PSP Study Group (2017) Clinical diagnosis of progressive supranuclear palsy: the movement disorder society criteria. Mov Disord 32:853–864

    Article  Google Scholar 

  25. Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174

    Article  CAS  Google Scholar 

  26. Abe K, Terakawa H, Takanashi M, Watanabe Y, Tanaka H, Fujita N, Hirabuki N, Yanagihara T (2000) Proton magnetic resonance spectroscopy of patients with parkinsonism. Brain Res Bull 52:589–595

    Article  CAS  Google Scholar 

  27. Yu F, Barron DS, Tantiwongkosi B et al (2015) Patterns of gray matter atrophy in atypical parkinsonism syndromes: a VBM meta-analysis. Brain Behav 5:e00329

    Article  Google Scholar 

  28. Ngai S, Tang Y, Du L et al (2007) Hyperintensity of the precentral gyral subcortical white matter and hypointensity of the precentral gyrus on fluid-attenuated inversion recovery: variation with age and implications for the diagnosis of amyotrophic lateral sclerosis. Am J Neuroradiol 28:250–254

    CAS  PubMed  Google Scholar 

  29. Fukunaga M, Li T-Q, van Gelderen P, de Zwart JA, Shmueli K, Yao B, Lee J, Maric D, Aronova MA, Zhang G, Leapman RD, Schenck JF, Merkle H, Duyn JH (2010) Layer-specific variation of iron content in cerebral cortex as a source of MRI contrast. Proc Natl Acad Sci 107:3834–3839

    Article  CAS  Google Scholar 

  30. Deistung A, Schäfer A, Schweser F, Biedermann U, Turner R, Reichenbach JR (2013) Toward in vivo histology: a comparison of quantitative susceptibility mapping (QSM) with magnitude-, phase-, and R2⁎-imaging at ultra-high magnetic field strength. Neuroimage 65:299–314

    Article  Google Scholar 

  31. Ide S, Kakeda S, Korogi Y, Yoneda T, Nishimura J, Sato T, Hiai Y, Ohnari N, Takahashi M, Hachisuka K, Fujiwara H, Matsuyama A (2012) Delineation of optic radiation and stria of Gennari on high-resolution phase difference enhanced imaging. Acad Radiol 19:1283–1289

    Article  Google Scholar 

  32. Boxer AL, Geschwind MD, Belfor N, Gorno-Tempini ML, Schauer GF, Miller BL, Weiner MW, Rosen HJ (2006) Patterns of brain atrophy that differentiate corticobasal degeneration syndrome from progressive supranuclear palsy. Arch Neurol 63:81–86

    Article  Google Scholar 

  33. Hauw J-J, Daniel S, Dickson D et al (1994) Preliminary NINDS neuropathologic criteria for Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy). Neurology 44:2015–2019

    Article  CAS  Google Scholar 

  34. Ling H, O’Sullivan SS, Holton JL et al (2010) Does corticobasal degeneration exist? A clinicopathological re-evaluation. Brain 133:2045–2057

    Article  Google Scholar 

  35. Boeve BF, Maraganore DM, Parisi JE, Ahlskog JE, Graff-Radford N, Caselli RJ, Dickson DW, Kokmen E, Petersen RC (1999) Pathologic heterogeneity in clinically diagnosed corticobasal degeneration. Neurology 53:795–800

    Article  CAS  Google Scholar 

  36. Tartaglia MC, Sidhu M, Laluz V, Racine C, Rabinovici GD, Creighton K, Karydas A, Rademakers R, Huang EJ, Miller BL, DeArmond SJ, Seeley WW (2010) Sporadic corticobasal syndrome due to FTLD-TDP. Acta Neuropathol 119:365–374

    Article  Google Scholar 

  37. Huey ED, Ferrari R, Moreno JH et al (2012) FUS and TDP43 genetic variability in FTD and CBS. Neurobiol Aging 33:1016 e1019–1016 e1017

    Article  Google Scholar 

Download references

Funding

No funding was received for this study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mari Miyata.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest directly relevant to the content of this article.

Ethical approval

All procedures performed in the studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed consent

Human experiments were performed in accordance with the guidelines provided and approved by the Institutional Review Board of the University of Occupational and Environmental Health School of Medicine (Kitakyushu, Fukuoka, Japan). Our institutional review board approved this retrospective study, which analyzed existing, de-identified patient data, and waived informed consent.

Additional information

Publisher’s note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Miyata, M., Kakeda, S., Toyoshima, Y. et al. Potential usefulness of signal intensity of cerebral gyri on quantitative susceptibility mapping for discriminating corticobasal degeneration from progressive supranuclear palsy and Parkinson’s disease. Neuroradiology 61, 1251–1259 (2019). https://doi.org/10.1007/s00234-019-02253-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00234-019-02253-6

Keywords

Navigation