Top

Published in:

01-08-2016 | Neuro

Neurite orientation dispersion and density imaging in the substantia nigra in idiopathic Parkinson disease

Authors: Koji Kamagata, Taku Hatano, Ayami Okuzumi, Yumiko Motoi, Osamu Abe, Keigo Shimoji, Kouhei Kamiya, Michimasa Suzuki, Masaaki Hori, Kanako K. Kumamaru, Nobutaka Hattori, Shigeki Aoki

Published in: European Radiology | Issue 8/2016

Abstract

Objectives

We used neurite orientation dispersion and density imaging (NODDI) to quantify changes in the substantia nigra pars compacta (SNpc) and striatum in Parkinson disease (PD).

Methods

Diffusion-weighted magnetic resonance images were acquired from 58 PD patients and 36 age- and sex-matched controls. The intracellular volume fraction (Vic), orientation dispersion index (OD), and isotropic volume fraction (Viso) of the basal ganglia were compared between groups. Multivariate logistic regression analysis determined which diffusion parameters were independent predictors of PD. Receiver operating characteristic (ROC) analysis compared the diagnostic accuracies of the evaluated indices. Pearson coefficient analysis correlated each diffusional parameter with disease severity.

Results

Vic in the contralateral SNpc and putamen were significantly lower in PD patients than in healthy controls (P < 0.00058). Vic and OD in the SNpc and putamen showed significant negative correlations (P < 0.05) with disease severity. Multivariate logistic analysis revealed that Vic (P = 0.0000046) and mean diffusivity (P = 0.019) in the contralateral SNpc were the independent predictors of PD. In the ROC analysis, Vic in the contralateral SNpc showed the best diagnostic performance (mean cutoff, 0.62; sensitivity, 0.88; specificity, 0.83).

Conclusion

NODDI is likely to be useful for diagnosing PD and assessing its progression.

Key Points

• Neurite orientation dispersion and density imaging (NODDI) is a new diffusion MRI technique

• NODDI estimates neurite microstructure more specifically than diffusion tensor imaging

• By using NODDI, nigrostriatal alterations in PD can be evaluated in vivo

• NOODI is useful for diagnosing PD and assessing its disease progression

Available only for authorised users

Schulz-Schaeffer WJ (2010) The synaptic pathology of alpha-synuclein aggregation in dementia with Lewy bodies, Parkinson's disease and Parkinson's disease dementia. Acta Neuropathol 120:131–143CrossRefPubMedPubMedCentral

Patt S, Gertz HJ, Gerhard L, Cervos-Navarro J (1991) Pathological changes in dendrites of substantia nigra neurons in Parkinson’s disease: a Golgi study. Histol Histopathol 6:373–380PubMed

Zaja-Milatovic S, Milatovic D, Schantz AM et al (2005) Dendritic degeneration in neostriatal medium spiny neurons in Parkinson disease. Neurology 64:545–547CrossRefPubMed

Deutch AY (2006) Striatal plasticity in parkinsonism: dystrophic changes in medium spiny neurons and progression in Parkinson's disease. J Neural Transm Suppl 70:67–70

Chan LL, Rumpel H, Yap K et al (2007) Case control study of diffusion tensor imaging in Parkinson's disease. J Neurol Neurosurg Psychiatry 78:1383–1386CrossRefPubMedPubMedCentral

Yoshikawa K, Nakata Y, Yamada K, Nakagawa M (2004) Early pathological changes in the parkinsonian brain demonstrated by diffusion tensor MRI. J Neurol Neurosurg Psychiatry 75:481–484CrossRefPubMedPubMedCentral

Zhan W, Kang GA, Glass GA et al (2012) Regional alterations of brain microstructure in Parkinson's disease using diffusion tensor imaging. Mov Disord 27:90–97CrossRefPubMed

Focke NK, Helms G, Pantel PM et al (2011) Differentiation of typical and atypical Parkinson syndromes by quantitative MR imaging. AJNR Am J Neuroradiol 32:2087–2092CrossRefPubMed

Menke RA, Scholz J, Miller KL et al (2009) MRI characteristics of the substantia nigra in Parkinson’s disease: a combined quantitative T1 and DTI study. Neuroimage 47:435–441CrossRefPubMed

10.

Vaillancourt DE, Spraker MB, Prodoehl J et al (2009) High-resolution diffusion tensor imaging in the substantia nigra of de novo Parkinson disease. Neurology 72:1378–1384CrossRefPubMedPubMedCentral

11.

Zhang H, Schneider T, Wheeler-Kingshott CA, Alexander DC (2012) NODDI: practical in vivo neurite orientation dispersion and density imaging of the human brain. Neuroimage 61:1000–1016CrossRefPubMed

12.

Winston GP, Micallef C, Symms MR, Alexander DC, Duncan JS, Zhang H (2014) Advanced diffusion imaging sequences could aid assessing patients with focal cortical dysplasia and epilepsy. Epilepsy Res 108:336–339CrossRefPubMedPubMedCentral

13.

Billiet T, Madler B, D'Arco F et al (2014) Characterizing the microstructural basis of “unidentified bright objects” in neurofibromatosis type 1: a combined in vivo multicomponent T2 relaxation and multi-shell diffusion MRI analysis. Neuroimage Clin 4:649–658CrossRefPubMedPubMedCentral

14.

Wilm BJ, Svensson J, Henning A, Pruessmann KP, Boesiger P, Kollias SS (2007) Reduced field-of-view MRI using outer volume suppression for spinal cord diffusion imaging. Magn Reson Med 57:625–630CrossRefPubMed

15.

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 55:181–184CrossRefPubMedPubMedCentral

16.

Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17:825–841CrossRefPubMed

17.

Basser PJ, Mattiello J, LeBihan D (1994) Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson B 103:247–254CrossRefPubMed

18.

Du G, Lewis MM, Sen S et al (2012) Imaging nigral pathology and clinical progression in Parkinson's disease. Mov Disord 27:1636–1643CrossRefPubMedPubMedCentral

19.

Prakash BD, Sitoh YY, Tan LC, Au WL (2012) Asymmetrical diffusion tensor imaging indices of the rostral substantia nigra in Parkinson's disease. Parkinsonism Relat Disord 18:1029–1033CrossRefPubMed

20.

Skorpil M, Soderlund V, Sundin A, Svenningsson P (2012) MRI diffusion in Parkinson’s disease: using the technique’s inherent directional information to study the olfactory bulb and substantia nigra. J Parkinsons Dis 2:171–180PubMed

21.

Gattellaro G, Minati L, Grisoli M et al (2009) White matter involvement in idiopathic Parkinson disease: a diffusion tensor imaging study. AJNR Am J Neuroradiol 30:1222–1226CrossRefPubMed

22.

Menke RA, Jbabdi S, Miller KL, Matthews PM, Zarei M (2010) Connectivity-based segmentation of the substantia nigra in human and its implications in Parkinson's disease. Neuroimage 52:1175–1180CrossRefPubMed

23.

Peran P, Cherubini A, Assogna F et al (2010) Magnetic resonance imaging markers of Parkinson's disease nigrostriatal signature. Brain 133:3423–3433CrossRefPubMed

24.

Rolheiser TM, Fulton HG, Good KP et al (2011) Diffusion tensor imaging and olfactory identification testing in early-stage Parkinson's disease. J Neurol 258:1254–1260CrossRefPubMed

25.

Wang JJ, Lin WY, Lu CS et al (2011) Parkinson disease: diagnostic utility of diffusion kurtosis imaging. Radiology 261:210–217CrossRefPubMed

26.

Glantz SA, Slinker BK (2001) Primer of applied regression & analysis of variance, 2nd edn. McGraw-Hill, Medical Pub. Division, New York

27.

Du G, Lewis MM, Styner M et al (2011) Combined R2* and diffusion tensor imaging changes in the substantia nigra in Parkinson's disease. Mov Disord 26:1627–1632CrossRefPubMedPubMedCentral

28.

Pierpaoli C, Basser PJ (1996) Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med 36:893–906CrossRefPubMed

29.

Braak H, Del Tredici K, Rub U, de Vos RA, Jansen Steur EN, Braak E (2003) Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging 24:197–211CrossRefPubMed

30.

Hodaie M, Neimat JS, Lozano AM (2007) The dopaminergic nigrostriatal system and Parkinson’s disease: molecular events in development, disease, and cell death, and new therapeutic strategies. Neurosurgery 60:17–28, discussion 28–30CrossRefPubMed

31.

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

32.

Peran P, Hagberg G, Luccichenti G et al (2007) Voxel-based analysis of R2* maps in the healthy human brain. J Magn Reson Imaging 26:1413–1420CrossRefPubMed

33.

Abe O, Aoki S, Hayashi N et al (2002) Normal aging in the central nervous system: quantitative MR diffusion-tensor analysis. Neurobiol Aging 23:433–441CrossRefPubMed

34.

Acosta-Cabronero J, Williams GB, Pengas G, Nestor PJ (2010) Absolute diffusivities define the landscape of white matter degeneration in Alzheimer's disease. Brain 133:529–539CrossRefPubMed

35.

Seibyl J, Russell D, Jennings D, Marek K (2012) The molecular basis of dopaminergic brain imaging in Parkinson's disease. Q J Nucl Med Mol Imaging 56:4–16PubMed

36.

Tatsch K, Schwarz J, Mozley PD et al (1997) Relationship between clinical features of Parkinson's disease and presynaptic dopamine transporter binding assessed with [123I]IPT and single-photon emission tomography. Eur J Nucl Med 24:415–421PubMed

37.

Bajaj N, Hauser RA, Grachev ID (2013) Clinical utility of dopamine transporter single photon emission CT (DaT-SPECT) with (123I) ioflupane in diagnosis of parkinsonian syndromes. J Neurol Neurosurg Psychiatry 84:1288–1295CrossRefPubMedPubMedCentral

38.

Jensen JH, Helpern JA, Ramani A, Lu H, Kaczynski K (2005) Diffusional kurtosis imaging: the quantification of non-gaussian water diffusion by means of magnetic resonance imaging. Magn Reson Med 53:1432–1440CrossRefPubMed

39.

Schwarz ST, Abaei M, Gontu V, Morgan PS, Bajaj N, Auer DP (2013) Diffusion tensor imaging of nigral degeneration in Parkinson’s disease: a region-of-interest and voxel-based study at 3 T and systematic review with meta-analysis. Neuroimage Clin 3:481–488CrossRefPubMedPubMedCentral

Title: Neurite orientation dispersion and density imaging in the substantia nigra in idiopathic Parkinson disease
Authors: Koji Kamagata
Taku Hatano
Ayami Okuzumi
Yumiko Motoi
Osamu Abe
Keigo Shimoji
Kouhei Kamiya
Michimasa Suzuki
Masaaki Hori
Kanako K. Kumamaru
Nobutaka Hattori
Shigeki Aoki
Publication date: 01-08-2016
Publisher: Springer Berlin Heidelberg
Published in: European Radiology / Issue 8/2016
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI: https://doi.org/10.1007/s00330-015-4066-8

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Neurite orientation dispersion and density imaging in the substantia nigra in idiopathic Parkinson disease

Abstract

Objectives

Methods

Results

Conclusion

Key Points

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Objectives

Methods

Results

Conclusion

Key Points

Please log in to get access to this content

Other articles of this Issue 8/2016

Prenatal MR imaging features of isolated cerebellar haemorrhagic lesions

Portrayal of radiology in a major medical television series: How does it influence the perception of radiology among patients and radiology professionals?

Computer tomography colonography participation and yield in patients under surveillance for 6-9 mm polyps in a population-based screening trial

Back to the future: sagittal CT in the evaluation of COPD

Navigated MRI-guided liver biopsies in a closed-bore scanner: experience in 52 patients

Dual-Phase Dual-Energy CT in Patients Treated with Erlotinib for Advanced Non-Small Cell Lung Cancer: Possible Benefits of Iodine Quantification in Response Assessment