Skip to main content
Erschienen in: European Radiology 8/2016

29.10.2015 | Neuro

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

verfasst von: 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

Erschienen in: European Radiology | Ausgabe 8/2016

Einloggen, um Zugang zu erhalten

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
Anhänge
Nur mit Berechtigung zugänglich
Literatur
1.
Zurück zum Zitat 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 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
2.
Zurück zum Zitat 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 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
3.
Zurück zum Zitat Zaja-Milatovic S, Milatovic D, Schantz AM et al (2005) Dendritic degeneration in neostriatal medium spiny neurons in Parkinson disease. Neurology 64:545–547CrossRefPubMed Zaja-Milatovic S, Milatovic D, Schantz AM et al (2005) Dendritic degeneration in neostriatal medium spiny neurons in Parkinson disease. Neurology 64:545–547CrossRefPubMed
4.
Zurück zum Zitat 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 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
5.
Zurück zum Zitat 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 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
6.
Zurück zum Zitat 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 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
7.
Zurück zum Zitat 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 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
8.
Zurück zum Zitat 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 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
9.
Zurück zum Zitat 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 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.
Zurück zum Zitat 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 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.
Zurück zum Zitat 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 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.
Zurück zum Zitat 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 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.
Zurück zum Zitat 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 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.
Zurück zum Zitat 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 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.
Zurück zum Zitat 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 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.
Zurück zum Zitat 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 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.
Zurück zum Zitat 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 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.
19.
Zurück zum Zitat 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 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.
Zurück zum Zitat 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 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.
Zurück zum Zitat 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 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.
Zurück zum Zitat 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 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.
Zurück zum Zitat Peran P, Cherubini A, Assogna F et al (2010) Magnetic resonance imaging markers of Parkinson's disease nigrostriatal signature. Brain 133:3423–3433CrossRefPubMed Peran P, Cherubini A, Assogna F et al (2010) Magnetic resonance imaging markers of Parkinson's disease nigrostriatal signature. Brain 133:3423–3433CrossRefPubMed
24.
Zurück zum Zitat 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 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.
Zurück zum Zitat Wang JJ, Lin WY, Lu CS et al (2011) Parkinson disease: diagnostic utility of diffusion kurtosis imaging. Radiology 261:210–217CrossRefPubMed Wang JJ, Lin WY, Lu CS et al (2011) Parkinson disease: diagnostic utility of diffusion kurtosis imaging. Radiology 261:210–217CrossRefPubMed
26.
Zurück zum Zitat Glantz SA, Slinker BK (2001) Primer of applied regression & analysis of variance, 2nd edn. McGraw-Hill, Medical Pub. Division, New York Glantz SA, Slinker BK (2001) Primer of applied regression & analysis of variance, 2nd edn. McGraw-Hill, Medical Pub. Division, New York
27.
Zurück zum Zitat 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 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.
Zurück zum Zitat Pierpaoli C, Basser PJ (1996) Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med 36:893–906CrossRefPubMed Pierpaoli C, Basser PJ (1996) Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med 36:893–906CrossRefPubMed
29.
Zurück zum Zitat 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 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.
Zurück zum Zitat 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 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.
Zurück zum Zitat Fearnley JM, Lees AJ (1991) Ageing and Parkinson’s disease: substantia nigra regional selectivity. Brain 114:2283–2301CrossRefPubMed Fearnley JM, Lees AJ (1991) Ageing and Parkinson’s disease: substantia nigra regional selectivity. Brain 114:2283–2301CrossRefPubMed
32.
Zurück zum Zitat 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 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.
Zurück zum Zitat 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 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.
Zurück zum Zitat 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 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.
Zurück zum Zitat 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 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.
Zurück zum Zitat 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 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.
Zurück zum Zitat 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 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.
Zurück zum Zitat 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 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.
Zurück zum Zitat 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 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
Metadaten
Titel
Neurite orientation dispersion and density imaging in the substantia nigra in idiopathic Parkinson disease
verfasst von
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
Publikationsdatum
29.10.2015
Verlag
Springer Berlin Heidelberg
Erschienen in
European Radiology / Ausgabe 8/2016
Print ISSN: 0938-7994
Elektronische ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-015-4066-8

Weitere Artikel der Ausgabe 8/2016

European Radiology 8/2016 Zur Ausgabe

Update Radiologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.