Top

Published in:

01-02-2019 | Head and Neck

Abnormalities of white and grey matter in early multiple system atrophy: comparison of parkinsonian and cerebellar variants

Authors: Santosh Kumar Dash, Albert Stezin, Tejashree Takalkar, Lija George, Nitish L Kamble, M Netravathi, Ravi Yadav, Keshav J. Kumar, Madhura Ingalhalikar, Jitender Saini, Pramod Kumar Pal

Published in: European Radiology | Issue 2/2019

Abstract

Objective

Multiple system atrophy (MSA) is a neurodegenerative disorder with progressive motor and autonomic dysfunction. There is a paucity of information on the early neurostructural changes in MSA, especially its subtypes, MSA-P (patients with predominant parkinsonism) and MSA-C (patients with predominant cerebellar signs). This study investigates the abnormalities of grey matter (GM) and white matter (WM) in early MSA and its subtypes using multi-modal voxel-based analysis.

Materials and methods

Twenty-six patients with MSA with duration of symptoms ≤ 2.5 years (mean duration: 1.6 ±0.9 years) were assessed clinically and with 3T MRI. Voxel-based morphometry (VBM) and diffusion tensor imaging (DTI) were performed to identify the structural changes in MSA and its subtypes. The GM changes and diffusion parameters of WM tracts were correlated with the clinical scores. The results were compared with MRI of 25 age- and gender-matched healthy controls.

Results

The early structural changes in MSA included GM loss of the cerebellum and subcallosal gyrus with widespread involvement of supratentorial and infratentorial WM fibres. In MSA-C, GM loss was limited to the cerebellum with WM changes predominantly affecting the infratentorial WM and association tracts. In contrast, MSA-P did not demonstrate any GM loss and the WM involvement was mainly supratentorial. There was no significant correlation between structural changes and clinical severity score.

Conclusion

In early MSA, WM microstructure was more affected than GM. These changes were greater in MSA-C than in MSA-P, suggesting variable deterioration in the subtypes of MSA.

Key Points

• Structural changes in early multiple system atrophy were evaluated using multi-modal neuroimaging.

• White matter was more affected than grey matter in early MSA.

• Clinical variables did not correlate with early structural changes.

Available only for authorised users

Fanciulli A, Wenning GK (2015) Multiple-System Atrophy. N Engl J Med 372:249–263. https://doi.org/10.1056/NEJMra1311488 CrossRefPubMed

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

Wenning GK, Ben-Shlomo Y, Hughes A et al (2000) What clinical features are most useful to distinguish definite multiple system atrophy from Parkinson’s disease? J Neurol Neurosurg Psychiatry 68:434–440. https://doi.org/10.1136/jnnp.68.4.434 CrossRefPubMedPubMedCentral

Gilman S, Wenning GK, Low PA et al (2008) Second consensus statement on the diagnosis of multiple system atrophy. Neurology 71:670–676. https://doi.org/10.1212/01.wnl.0000324625.00404.15 CrossRefPubMedPubMedCentral

Ubhi K, Low P, Masliah E (2011) Multiple system atrophy: A clinical and neuropathological perspective. Trends Neurosci 34:581–590. https://doi.org/10.1016/j.tins.2011.08.003 CrossRefPubMedPubMedCentral

Brooks DJ, Seppi K (2009) Proposed neuroimaging criteria for the diagnosis of multiple system atrophy. Mov Disord 24:949–964. https://doi.org/10.1002/mds.22413 CrossRefPubMed

Kim H-J, Jeon BS, Kim YE et al (2013) Clinical and imaging characteristics of dementia in multiple system atrophy. Parkinsonism Relat Disord 19:617–21. doi: https://doi.org/10.1016/j.parkreldis.2013.02.012

Brenneis C, Boesch SM, Egger KE et al (2006) Cortical atrophy in the cerebellar variant of multiple system atrophy: A voxel-based morphometry study. Mov Disord 21:159–165. https://doi.org/10.1002/mds.20656 CrossRefPubMed

Chang CC, Chang YY, Chang WN et al (2009) Cognitive deficits in multiple system atrophy correlate with frontal atrophy and disease duration. Eur J Neurol 16:1144–1150. https://doi.org/10.1111/j.1468-1331.2009.02661.x CrossRefPubMed

10.

Tzarouchi LC, Astrakas LG, Konitsiotis S et al (2010) Voxel-based morphometry and voxel-based relaxometry in parkinsonian variant of multiple system atrophy. J Neuroimaging 20:260–266. https://doi.org/10.1111/j.1552-6569.2008.00343.x CrossRefPubMed

11.

Hauser T-K, Luft A, Skalej M et al (2006) Visualization and quantification of disease progression in multiple system atrophy. Mov Disord 21:1674–1681. https://doi.org/10.1002/mds.21032 CrossRefPubMed

12.

Lee MJ, Shin J-H, Seoung J-K et al (2016) Cognitive impairments associated with morphological changes in cortical and subcortical structures in multiple system atrophy of the cerebellar type. Eur J Neurol 23:92–100. https://doi.org/10.1111/ene.12796 CrossRefPubMed

13.

Oishi K, Konishi J, Mori S et al (2009) Reduced fractional anisotropy in early-stage cerebellar variant of multiple system atrophy. J Neuroimaging 19:127–131. https://doi.org/10.1111/j.1552-6569.2008.00262.x CrossRefPubMed

14.

Zanigni S, Evangelisti S, Testa C et al (2017) White matter and cortical changes in atypical parkinsonisms: A multimodal quantitative MR study. Parkinsonism Relat Disord 39:44–51. https://doi.org/10.1016/j.parkreldis.2017.03.001 CrossRefPubMed

15.

Wang J, Wai Y, Lin W-Y et al (2010) Microstructural changes in patients with progressive supranuclear palsy: a diffusion tensor imaging study. J Magn Reson Imaging 32:69–75. https://doi.org/10.1002/jmri.22229 CrossRefPubMed

16.

Blain CRV, Barker GJ, Jarosz JM et al (2006) Measuring brain stem and cerebellar damage in parkinsonian syndromes using diffusion tensor MRI. Neurology 67:2199–2205. https://doi.org/10.1212/01.wnl.0000249307.59950.f8 CrossRefPubMed

17.

Wang PS, Wu HM, Lin CP, Soong BW (2011) Use of diffusion tensor imaging to identify similarities and differences between cerebellar and Parkinsonism forms of multiple system atrophy. Neuroradiology 53:471–481. https://doi.org/10.1007/s00234-010-0757-7 CrossRefPubMed

18.

Wang P-S, Yeh C-L, Lu C-F et al (2016) The involvement of supratentorial white matter in multiple system atrophy: a diffusion tensor imaging tractography study. Acta Neurol Belg 117:213–220. https://doi.org/10.1007/s13760-016-0724-0 CrossRefPubMed

19.

Ji L, Zhu D, Xiao C, Shi J (2014) Tract based spatial statistics in multiple system atrophy: A comparison between clinical subtypes. Parkinsonism Relat Disord 20:1050–1055. https://doi.org/10.1016/j.parkreldis.2014.06.017 CrossRefPubMed

20.

Ito S, Makino T, Shirai W, Hattori T (2008) Diffusion tensor analysis of corpus callosum in progressive supranuclear palsy. Neuroradiology 50:981–985. https://doi.org/10.1007/s00234-008-0447-x CrossRefPubMed

21.

Rulseh AM, Keller J, Rusz J et al (2016) Diffusion tensor imaging in the characterization of multiple system atrophy. Neuropsychiatr Dis Treat 12:2181–2187. https://doi.org/10.2147/NDT.S109094 CrossRefPubMedPubMedCentral

22.

Wenning GK, Geser F, Krismer F et al (2013) The natural history of multiple system atrophy: A prospective European cohort study. Lancet Neurol. 12:264–274. https://doi.org/10.1016/S1474-4422(12)70327-7 CrossRefPubMedPubMedCentral

23.

Low PA, Reich SG, Jankovic J et al (2015) Natural history of multiple system atrophy in the USA: a prospective cohort study. Lancet Neurol. 14:710–719. https://doi.org/10.1016/s1474-4422(15)00058-7 CrossRefPubMedPubMedCentral

24.

Popescu V, Battaglini M, Hoogstrate WS et al (2012) Optimizing parameter choice for FSL-Brain Extraction Tool (BET) on 3D T1 images in multiple sclerosis. Neuroimage 61:1484–1494. https://doi.org/10.1016/j.neuroimage.2012.03.074 CrossRefPubMed

25.

Tristán-Vega A, Aja-Fernández S (2010) DWI filtering using joint information for DTI and HARDI. Med Image Anal. 14:205–218. https://doi.org/10.1016/j.media.2009.11.001 CrossRefPubMed

26.

Mestre TA, Gupta A, Lang A E (2016) MRI signs of multiple system atrophy preceding the clinical diagnosis: the case for an imaging-supported probable MSA diagnostic category. J Neurol Neurosurg Psychiatry. 87 443–4.

27.

Laurens B, Vergnet S, Lopez MC et al (2017) Multiple System Atrophy - State of the Art. Curr Neurol Neurosci Rep 17. https://doi.org/10.1007/s11910-017-0751-0

28.

Roncevic D, Palma JA, Martinez J et al (2014) Cerebellar and parkinsonian phenotypes in multiple system atrophy: similarities, differences and survival. J Neural Transm (Vienna). 121:507–512CrossRefPubMed

29.

Worker A, Blain C, Jarosz J et al (2014) Diffusion Tensor Imaging of Parkinson’s Disease, Multiple System Atrophy and Progressive Supranuclear Palsy: A Tract-Based Spatial Statistics Study. PLoS One. 9:e112638. https://doi.org/10.1371/journal.pone.0112638 CrossRefPubMedPubMedCentral

30.

Tha KK, Terae S, Yabe I et al (2010) Microstructural white matter abnormalities of multiple system atrophy: in vivo topographic illustration by using diffusion-tensor MR imaging. Radiology. 255:563–569. https://doi.org/10.1148/radiol.10090988 CrossRefPubMed

31.

Tir M, Delmaire C, Le Thuc V et al (2009) Motor-related circuit dysfunction in MSA-P: Usefulness of combined whole-brain imaging analysis. Mov Disord 24:863–870CrossRefPubMed

32.

Kim JS, Yang JJ, Lee DK et al (2015) Cognitive impairment and its structural correlates in the parkinsonian subtype of multiple system atrophy. Neurodegener Dis 15:294–300. https://doi.org/10.1159/000430953 CrossRefPubMed

33.

Shigemoto Y, Matsuda H, Kamiya K et al (2013) In vivo evaluation of gray and white matter volume loss in the parkinsonian variant of multiple system atrophy using SPM8 plus DARTEL for VBM. NeuroImage Clin 2:491–496. https://doi.org/10.1016/j.nicl.2013.03.017 CrossRefPubMedPubMedCentral

34.

Minnerop M, Specht K, Ruhlmann J et al (2007) Voxel-based morphometry and voxel-based relaxometry in multiple system atrophy-A comparison between clinical subtypes and correlations with clinical parameters. Neuroimage. 36:1086–1095. https://doi.org/10.1016/j.neuroimage.2007.04.028 CrossRefPubMed

35.

Minnerop M, Lüders E, Specht K et al (2010) Callosal tissue loss in multiple system atrophy-A one-year follow-up study. Mov Disord 25:2613–2620. https://doi.org/10.1002/mds.23318 CrossRefPubMedPubMedCentral

36.

Specht K, Minnerop M, Müller-Hübenthal J et al (2005) Complementary results by combining voxel-based morphometry and voxel-based relaxometry. Neuroimage. 25:287–293. https://doi.org/10.1016/j.neuroimage.2004.11.022 CrossRefPubMed

37.

Brenneis C, Egger K, Scherfler C et al (2007) Progression of brain atrophy in multiple system atrophy: A longitudinal VBM study. J Neurol 254:191–196. https://doi.org/10.1007/s00415-006-0325-6 CrossRefPubMed

38.

Yang H, Wang X, Liao W et al (2015) Application of diffusion tensor imaging in multiple system atrophy: the involvement of pontine transverse and longitudinal fibers. Int J Neurosci 125: 18–24.

Title: Abnormalities of white and grey matter in early multiple system atrophy: comparison of parkinsonian and cerebellar variants
Authors: Santosh Kumar Dash
Albert Stezin
Tejashree Takalkar
Lija George
Nitish L Kamble
M Netravathi
Ravi Yadav
Keshav J. Kumar
Madhura Ingalhalikar
Jitender Saini
Pramod Kumar Pal
Publication date: 01-02-2019
Publisher: Springer Berlin Heidelberg
Published in: European Radiology / Issue 2/2019
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI: https://doi.org/10.1007/s00330-018-5594-9

At a glance: The STEP trials

Springer Medicine

Abnormalities of white and grey matter in early multiple system atrophy: comparison of parkinsonian and cerebellar variants

Abstract

Objective

Materials and methods

Results

Conclusion

Key Points

At a glance: The STEP trials

Springer Medicine

Abstract

Objective

Materials and methods

Results

Conclusion

Key Points

Please log in to get access to this content

Other articles of this Issue 2/2019

Endometrial Cancer MRI staging: Updated Guidelines of the European Society of Urogenital Radiology

Dynamic contrast-enhanced CT for the assessment of tumour response in malignant pleural mesothelioma: a pilot study

Follow-up infarct volume as a mediator of endovascular treatment effect on functional outcome in ischaemic stroke

Correction to: Frequency and characteristics of contralateral breast abnormalities following recall at screening mammography

Prognostic value of radiomic analysis of iodine overlay maps from dual-energy computed tomography in patients with resectable lung cancer

Magnetic resonance hysterosalpingography in diagnostic work-up of female infertility – comparison with conventional hysterosalpingography: a randomised study