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Using ‘swallow-tail’ sign and putaminal hypointensity as biomarkers to distinguish multiple system atrophy from idiopathic Parkinson’s disease: A susceptibility-weighted imaging study

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Abstract

Objective

To investigate the value of ‘swallow-tail’ sign and putaminal hypointensity on 3 T susceptibility-weighted imaging (SWI) for distinguishing multiple system atrophy (MSA) from idiopathic Parkinson’s disease (IPD).

Methods

Three groups – 39 MSA patients, 18 IPD patients,and 31 healthy controls (HCs) – were administered a 3 T SWI sequence to evaluate ‘swallow-tail’ sign and putaminal hypointensity using visual scales from 0 to 2 and 0 to 3 scores, respectively. The diagnostic accuracy of the two signs separately and combined was calculated using a receiver operating characteristic curve, with clinical diagnosis as the gold standard.

Results

The scores of ‘swallow-tail’ sign were lower in IPD than in MSA or in HCs, as well as for putaminal hypointensity in IPD or HCs than in MSA (p < 0.05). The sensitivity and specificity of ‘swallow-tail’ sign and putaminal hypointensity were 87.9% and 83.3%, and 35.9% and 100%, respectively, in the respective patient groups. The area under the curve of combined signs was increased from 0.85 (‘swallow tail’) or 0.68 (putaminal hypointensity) to 0.93.

Conclusion

The combination of ‘swallow-tail’ sign and putaminal hypointensity can increase the accuracy of discriminating between MSA and IPD.

Key Points

• Differential diagnosis of MSA and IPD is still challenging in clinical practice.

• Absence of ‘swallow-tail’ sign is a valuable biomarker for IPD on SWI.

• Putaminal hypointensity is a valuable biomarker for MSA on SWI.

• Combined ‘swallow- tail’ sign and putaminal hypointensity increase diagnostic accuracy.

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Abbreviations

AP:

Atypical Parkinsonism

AUC:

Area under the curve

HCs:

Healthy controls

IPD:

Idiopathic Parkinson’s disease

MRI:

Magnetic resonance imaging

MSA:

Multiple system atrophy

ROC:

Receiver operating characteristic

SN:

Substantia nigra

SWI:

Susceptibility-weighted imaging

References

  1. Stefanova N, Bücke P, Duerr S, Wenning GK (2009) Multiple system atrophy: an update. Lancet Neurol 8:1172–1178

    Article  CAS  PubMed  Google Scholar 

  2. Ramli N, Nair SR, Ramli NM, Lim SY (2015) Differentiating multiple-system atrophy from Parkinson's disease. Clin Radiol 70:555–564

    Article  CAS  PubMed  Google Scholar 

  3. Dabrowska M, Schinwelski M, Sitek EJ et al (2015) The role of neuroimaging in the diagnosis of the atypical parkinsonian syndromes in clinical practice. Neurol Neurochir Pol 49:421–431

    PubMed  Google Scholar 

  4. Mahlknecht P, Hotter A, Hussl A, Esterhammer R, Schocke M, Seppi K (2010) Significance of MRI in diagnosis and differential diagnosis of Parkinson's disease. Neurodegener Dis 7:300–318

    Article  PubMed  Google Scholar 

  5. Paviour DC, Thornton JS, Lees AJ, Jager HR (2007) Diffusion-weighted magnetic resonance imaging differentiates Parkinsonian variant of multiple-system atrophy from progressive supranuclear palsy. Mov Disord 22:68–74

    Article  PubMed  Google Scholar 

  6. Meijer FJ, van Rumund A, Tuladhar AM et al (2015) Conventional 3T brain MRI and diffusion tensor imaging in the diagnostic workup of early stage parkinsonism. Neuroradiology 57:655–669

    Article  PubMed  PubMed Central  Google Scholar 

  7. Gottlich M, Munte TF, Heldmann M, Kasten M, Hagenah J, Kramer UM (2013) Altered resting state brain networks in Parkinson’s disease. PLoS One 8, e77336

    Article  PubMed  PubMed Central  Google Scholar 

  8. You H, Wang J, Wang H et al (2011) Altered regional homogeneity in motor cortices in patients with multiple system atrophy. Neurosci Lett 502:18–23

    Article  CAS  PubMed  Google Scholar 

  9. Francesco F, Isabella LS, Vincenzo L et al (1997) Proton Magnetic Resonance Spectroscopy in Parlunson’s Disease and Atypical Parkinsonian Disorders. Mov Disord 12:903–909

    Article  Google Scholar 

  10. Eckert T, Sailer M, Kaufmann J et al (2004) Differentiation of idiopathic Parkinson's disease, multiple system atrophy, progressive supranuclear palsy, and healthy controls using magnetization transfer imaging. Neuroimage 21:229–235

    Article  PubMed  Google Scholar 

  11. Sehgal V, Delproposto Z, Haacke EM et al (2005) Clinical applications of neuroimaging with susceptibility-weighted imaging. J Magn Reson Imaging 22:439–450

    Article  PubMed  Google Scholar 

  12. Liu C, Li W, Tong KA, Yeom KW, Kuzminski S (2015) Susceptibility-weighted imaging and quantitative susceptibility mapping in the brain. J Magn Reson Imaging 42:23–41

    Article  PubMed  Google Scholar 

  13. Wang C, Fan G, Xu K, Wang S (2013) Quantitative assessment of iron deposition in the midbrain using 3D-enhanced T2 star weighted angiography (ESWAN): a preliminary cross-sectional study of 20 Parkinson's disease patients. Magn Reson Imaging 31:1068–1073

    Article  CAS  PubMed  Google Scholar 

  14. Gupta D, Saini J, Kesavadas C, Sarma PS, Kishore A (2010) Utility of susceptibility-weighted MRI in differentiating Parkinson's disease and atypical parkinsonism. Neuroradiology 52:1087–1094

    Article  PubMed  Google Scholar 

  15. Schwarz ST, Afzal M, Morgan PS, Bajaj N, Gowland PA, Auer DP (2014) The 'swallow tail' appearance of the healthy nigrosome - a new accurate test of Parkinson's disease: a case-control and retrospective cross-sectional MRI study at 3T. PLoS One 9, e93814

    Article  PubMed  PubMed Central  Google Scholar 

  16. Meijer FJ, Steens SC, van Rumund A et al (2016) Nigrosome-1 on Susceptibility Weighted Imaging to Differentiate Parkinson's Disease From Atypical Parkinsonism: An In Vivo and Ex Vivo Pilot Study. Pol J Radiol 81:363–369

    Article  PubMed  PubMed Central  Google Scholar 

  17. Wang Y, Butros SR, Shuai X et al (2012) Different iron-deposition patterns of multiple system atrophy with predominant parkinsonism and idiopathetic Parkinson diseases demonstrated by phase-corrected susceptibility-weighted imaging. AJNR Am J Neuroradiol 33:266–273

    Article  CAS  PubMed  Google Scholar 

  18. Jae-hyeok L, Seung-kug B (2011) Putaminal hypointensity in the parkinsonianvariant of multiple system atrophy: simple visual assessment using susceptibility-weighted imaging. J Mov Disord 4:60–63

    Article  Google Scholar 

  19. Meijer FJ, van Rumund A, Fasen BA et al (2015) Susceptibility-weighted imaging improves the diagnostic accuracy of 3T brain MRI in the work-up of parkinsonism. AJNR Am J Neuroradiol 36:454–460

    Article  CAS  PubMed  Google Scholar 

  20. Gilman S, Wenning GK, Low PA et al (2008) Second consensus statement on the diagnosis of multiple system atrophy. Neurology 71:670–676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Andrew JH, Susan ED, Linda K et al (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  Google Scholar 

  22. Gao P, Zhou PY, Wang PQ et al (2016) Universality analysis of the existence of substantia nigra ‘swallow tail’ appearance of non-Parkinson patients in 3T SWI. Eur Rev Med Pharmacol Sci 20:1307–1314

    CAS  PubMed  Google Scholar 

  23. Damier P, Hirsch EC, Agid Y et al (1999) The substantia nigra of the humanbrain I. Nigrosomes and the nigral matrix, a compartmental organization based on calbindin D28K immunohistochemistry. Brain 122:1421–1436

    Article  PubMed  Google Scholar 

  24. Anna IB, Stefan TS, Alain P et al (2013) Visualization of nigrosome 1 and its loss in PD: Pathoanatomical correlation and in vivo 7 T MRI. Neurology 81:534–540

    Article  Google Scholar 

  25. Fearnley JM, Lees RJ (1991) Ageing and Parkinson’s disease: substantia nigra regional selectivity. Brain 114:2283–2301

    Article  PubMed  Google Scholar 

  26. Sian-Hulsmann J, Mandel S, Youdim MB, Riederer P (2011) The relevance of iron in the pathogenesis of Parkinson's disease. J Neurochem 118:939–957

    Article  PubMed  Google Scholar 

  27. Zecca L, Casella L, Albertini A et al (2008) Neuromelanin can protect against iron-mediated oxidative damage in system modeling iron overload of brain aging and Parkinson's disease. J Neurochem 106:1866–1875

    CAS  PubMed  Google Scholar 

  28. Yoon RG, Kim SJ, Kim HS et al (2015) The utility of susceptibility-weighted imaging for differentiating Parkinsonism-predominant multiple system atrophy from Parkinson's disease: correlation with 18F-flurodeoxyglucose positron-emission tomography. Neurosci Lett 584:296–301

    Article  CAS  PubMed  Google Scholar 

  29. Han YH, Lee JH, Kang BM et al (2013) Topographical differences of brain iron deposition between progressive supranuclear palsy and parkinsonian variant multiple system atrophy. J Neurol Sci 325:29–35

    Article  CAS  PubMed  Google Scholar 

  30. Matsusue E, Fujii S, Kanasaki Y et al (2008) Putaminal lesion in multiple system atrophy: postmortem MR-pathological correlations. Neuroradiology 50:559–567

    Article  PubMed  Google Scholar 

  31. Sugiyama A, Ito S, Suichi T et al (2015) Putaminal hypointensity on T2*-weighted MR imaging is the most practically useful sign in diagnosing multiple system atrophy: A preliminary study. J Neurol Sci 349:174–178

    Article  PubMed  Google Scholar 

  32. Harder SL, Hopp KM, Ward H, Neglio H, Gitlin J, Kido D (2008) Mineralization of the deep gray matter with age: a retrospective review with susceptibility-weighted MR imaging. AJNR Am J Neuroradiol 29:176–183

    Article  CAS  PubMed  Google Scholar 

  33. Zhang J, Wei L, Hu X et al (2015) Akinetic-rigid and tremor-dominant Parkinson's disease patients show different patterns of intrinsic brain activity. Parkinsonism Relat Disord 21:23–30

    Article  PubMed  Google Scholar 

  34. Wenning GK, Tison F, Shlomo YB et al (1997) Multiple System Atrophy: A Review of 203 Pathologically Proven Cases. Mov Disord 12:133–147

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank LetPub (www.letpub.com) for its linguistic assistance during the preparation of this manuscript.

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Authors and Affiliations

  1. Department of Radiology, The First Affiliated Hospital of China Medical University, Shenyang, 110001, Liaoning, People’s Republic of China

    Na Wang, HuaGuang Yang, ChengBo Li & GuoGuang Fan

  2. Department of Neurology, The First Affiliated Hospital of China Medical University, Shenyang, 110001, Liaoning, People’s Republic of China

    XiaoGuang Luo

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  1. Na Wang
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  2. HuaGuang Yang
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Correspondence to GuoGuang Fan or XiaoGuang Luo.

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Guarantor

The scientific guarantor of this publication is Guoguang Fan.

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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

No complex statistical methods were necessary for this paper.

Informed consent

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

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Institutional Review Board approval was obtained.

Study subjects or cohorts overlap

No study subjects or cohorts have been previously reported.

Methodology

  • retrospective

  • diagnostic or prognostic study

  • performed at one institution

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Wang, N., Yang, H., Li, C. et al. Using ‘swallow-tail’ sign and putaminal hypointensity as biomarkers to distinguish multiple system atrophy from idiopathic Parkinson’s disease: A susceptibility-weighted imaging study. Eur Radiol 27, 3174–3180 (2017). https://doi.org/10.1007/s00330-017-4743-x

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  • DOI: https://doi.org/10.1007/s00330-017-4743-x

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