Changes of olfactory tract in Parkinson's disease: a DTI tractography study.
MRI
Magnetic resonance
Olfactory function
Parkinson’s disease
Smell
Journal
Neuroradiology
ISSN: 1432-1920
Titre abrégé: Neuroradiology
Pays: Germany
ID NLM: 1302751
Informations de publication
Date de publication:
Feb 2021
Feb 2021
Historique:
received:
20
05
2020
accepted:
07
09
2020
pubmed:
13
9
2020
medline:
22
9
2021
entrez:
12
9
2020
Statut:
ppublish
Résumé
Impaired olfactory function is one of the main features of Parkinson's disease. However, how peripheral olfactory structures are involved remains unclear. Using diffusion tensor imaging fiber tracking, we investigated for MRI microstructural changes in the parkinsonian peripheral olfactory system and particularly the olfactory tract, in order to seek a better understanding of the structural alternations underlying hyposmia in Parkinson's disease. All patients were assessed utilizing by the Italian Olfactory Identification Test for olfactory function and the Unified Parkinson's Disease Rating Scale-III part as well as Hoehn and Yahr rating scale for motor disability. Imaging was performed on a 3 T Clinical MR scanner. MRI data pre-processing was carried out by DTIPrep, diffusion tensor imaging reconstruction, and fiber tracking using Diffusion Toolkit and tractography analysis by TrackVis. The following parameters were used for groupwise comparison: fractional anisotropy, mean diffusivity, radial diffusivity, axial diffusivity, and tract volume. Overall 23 patients with Parkinson's disease (mean age 63.6 ± 9.3 years, UPDRS-III 24.5 ± 12.3, H&Y 1.9 ± 0.5) and 18 controls (mean age 56.3 ± 13.7 years) were recruited. All patients had been diagnosed hyposmic. Diffusion tensor imaging analysis of the olfactory tract showed significant fractional anisotropy, and tract volume decreases for the Parkinson's disease group compared with controls (P < 0.05). Fractional anisotropy and age, in the control group, were significant for multiple correlations (r = - 0.36, P < 0.05, Spearman's rank correlation). Fiber tracking diffusion tensor imaging analysis of olfactory tract was feasible, and it could be helpful for characterizing hyposmia in Parkinson's disease.
Identifiants
pubmed: 32918150
doi: 10.1007/s00234-020-02551-4
pii: 10.1007/s00234-020-02551-4
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
235-242Références
Chaudhuri KR, Healy DG, Schapira AH (2006) Non-motor symptoms of Parkinson’s disease: diagnosis and management. Lancet Neurol 5:235–245
doi: 10.1016/S1474-4422(06)70373-8
Hawkes CH, Del Tredici K, Braak H (2007) Parkinson’s disease: a dual-hit hypothesis. Neuropathol Appl Neurobiol 33:599–614
doi: 10.1111/j.1365-2990.2007.00874.x
Braak H, Del Tredici K, Rüb U, de Vos RA, Jansen Steur EN, Braak E (2003) Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24:197–211
doi: 10.1016/S0197-4580(02)00065-9
Hawkes CH (2008) The prodromal phase of sporadic Parkinson’s disease: does it exist and if so how long is it? Mov Disord 23:1799–1807
doi: 10.1002/mds.22242
Fullard ME, Morley JF, Duda JE (2017) Olfactory dysfunction as an early biomarker in Parkinson’s disease. Neurosci Bull 33:515–525
doi: 10.1007/s12264-017-0170-x
Postuma RB, Berg D (2016) Advances in markers of prodromal Parkinson disease. Nat Rev Neurol 12:622–634
doi: 10.1038/nrneurol.2016.152
Hummel T, Witt M, Reichmann H, Welge-Luessen A, Haehner A (2009) Immunohistochemical, volumetric, and functional neuroimaging studies in patients with idiopathic Parkinson’s disease. J Neurol Sci 289:119–122
doi: 10.1016/j.jns.2009.08.026
Silveira-Moriyama L, Holton JL, Kingsbury A, Ayling H, Petrie A, Sterlacci W, Poewe W, Maier H, Lees AJ, Revesz T (2009) Regional differences in the severity of Lewy body pathology across the olfactory cortex. Neurosci Lett 453:77–80
doi: 10.1016/j.neulet.2009.02.006
Del Tredici K, Ru BU, De Vos RA, Bohl JR, Braak H (2002) Where does parkinson disease pathology begin in the brain? J Neuropathol Exp Neurol 61:413–426
doi: 10.1093/jnen/61.5.413
Politis M, Wu K, Molloy SG, Bain P, Chaudhuri KR, Piccini P (2010) Parkinson’s disease symptoms: the patient’s perspective. Mov Disord 25:1646–1651
doi: 10.1002/mds.23135
Brooks DJ, Tambasco N (2016) Imaging synucleinopathies. Mov Disord 31:814–829
doi: 10.1002/mds.26547
Su M, Wang S, Fang W, Zhu Y, Li R, Sheng K, Zou D, Han Y, Wang X, Cheng O (2015) Alterations in the limbic/paralimbic cortices of Parkinson’s disease patients with hyposmia under resting-state functional MRI by regional homogeneity and functional connectivity analysis. Parkinsonism Relat Disord 21(7):698–703
doi: 10.1016/j.parkreldis.2015.04.006
Scherfler C, Schocke MF, Seppi K, Esterhammer R, Brenneis C, Jaschke W, Wenning GK, Poewe W (2006) Voxel-wise analysis of diffusion weighted imaging reveals disruption of the olfactory tract in Parkinson’s disease. Brain 129:538–542
doi: 10.1093/brain/awh674
Zhang K, Yu C, Zhang Y, Wu X, Zhu C, Chan P, Li K (2011) Voxel-based analysis of diffusion tensor indices in the brain in patients with Parkinson’s disease. Eur J Radiol 77:269–273
doi: 10.1016/j.ejrad.2009.07.032
Ibarretxe-Bilbao N, Junque C, Marti MJ, Valldeoriola F, Vendrell P, Bargallo N, Zarei M, Tolosa E (2010) Olfactory impairment in Parkinson’s disease and white matter abnormalities in central olfactory areas: a voxel-based diffusion tensor imaging study. Mov Disord 25:1888–1894
doi: 10.1002/mds.23208
Basser PJ, Mattiello J, LeBihan D (1994) MR diffusion tensor spectroscopy and imaging. Biophys J 66:259–267
doi: 10.1016/S0006-3495(94)80775-1
Alexander AL, Lee JE, Lazar M, Field AS (2007) Diffusion tensor imaging of the brain. Neurotherapeutics 4:316–329
doi: 10.1016/j.nurt.2007.05.011
Abhinav K, Yeh FC, Pathak S, Suski V, Lacomis D, Friedlander RM, Fernandez-Miranda JC (2014) Advanced diffusion MRI fiber tracking in neurosurgical and neurodegenerative disorders and neuroanatomical studies: a review. Biochim Biophys Acta 1842:2286–2297
doi: 10.1016/j.bbadis.2014.08.002
Schulte T, Sullivan EV, Müller-Oehring EM, Adalsteinsson E, Pfefferbaum A (2005) Corpus callosal microstructural integrity influences interhemispheric processing: a diffusion tensor imaging study. Cereb Cortex 15:1384–1392
doi: 10.1093/cercor/bhi020
Skorpil M, Rolheiser T, Robertson H, Sundin A, Svenningsson P (2011) Diffusion tensor fiber tractography of the olfactory tract. Magn Reson Imaging 29:289–292
doi: 10.1016/j.mri.2010.07.004
Daniel SE, Lees AJ (1993) Parkinson’s Disease Society Brain Bank, London: overview and research. J Neural Transm Suppl 39:165–172
pubmed: 8360656
Maremmani C, Rossi G, Tambasco N, Fattori B, Pieroni A, Ramat S, Napolitano A, Vanni P, Serra P, Piersanti P, Zanetti M, Coltelli M, Orsini M, Marconi R, Purcaro C, Rossi A, Calabresi P, Meco G (2012) The validity and reliability of the Italian Olfactory Identification Test (IOIT) in healthy subjects and in Parkinson’s disease patients. Parkinsonism Relat Disord 18:788–793
doi: 10.1016/j.parkreldis.2012.03.021
Rl D, Stern MB, Pfeiffer C, Gollomp SM, Hurtig HI (1992) Bilateral olfactory dysfunction in early stage treated and untreated idiopathic Parkinson’s disease. J Neurol Neurosurg Psychiatry 55:128–142 20
doi: 10.1136/jnnp.55.2.128
Scherfler C, Esterhammer R, Nocker M, Mahlknecht P, Stockner H, Warwitz B, Spielberger S, Pinter B, Donnemiller E, Decristoforo C, Virgolini I, Schocke M, Poewe W, Seppi K (2013) Correlation of dopaminergic terminal dysfunction and microstructural abnormalities of the basal ganglia and the olfactory tract in Parkinson’s disease. Brain 136:3028–3037
doi: 10.1093/brain/awt234
Oguz I, Farzinfar M, Matsui J, Budin F, Liu Z, Gerig G, Johnson HJ, Styner M (2014) DTIPrep: quality control of diffusion-weighted images. Front Neuroinform 8:4
doi: 10.3389/fninf.2014.00004
Wang R, Benner T, Sorensen AG et al (2007) Diffusion toolkit: a software package for diffusion imaging data processing and tractography. Proc Intl Soc Mag Reson Med 15:3720
Atkinson-Clement C, Pinto S, Eusebio A, Coulon O (2017) Diffusion tensor imaging in Parkinson’s disease: review and meta-analysis. NeuroImage Clin 16:98–110
doi: 10.1016/j.nicl.2017.07.011
Rolheiser TM, Fulton HG, Good KP, Fisk JD, McKelvey JR, Scherfler C, Khan NM, Leslie RA, Robertson HA (2011) Diffusion tensor imaging and olfactory identification testing in early-stage Parkinson’s disease. J Neurol 258:1254–1260
doi: 10.1007/s00415-011-5915-2
Chen NK, Chou YH, Sundman M, Hickey P, Kasoff WS, Bernstein A, Trouard TP, Lin T, Rapcsak SZ, Sherman SJ, Weingarten CP (2018) Alteration of diffusion-tensor magnetic resonance imaging measures in brain regions involved in early stages of Parkinson’s disease. Brain Connect 8:343–349
doi: 10.1089/brain.2017.0558
Nigro S, Riccelli R, Passamonti L, Arabia G, Morelli M, Nisticò R, Novellino F, Salsone M, Barbagallo G, Quattrone A (2016) Characterizing structural neural networks in de novo Parkinson disease patients using diffusion tensor imaging: altered structural brain network in drug-Naïve PD. Hum Brain Mapp 37:4500–4510
doi: 10.1002/hbm.23324
Dando SJ, Mackay-Sim A, Norton R, Currie BJ, St John JA, Ekberg JA, Batzloff M, Ulett GC, Beacham IR (2014) Pathogens penetrating the central nervous system: infection pathways and the cellular and molecular mechanisms of invasion. Clin Microbiol Rev 27:691–726
doi: 10.1128/CMR.00118-13
Doty RL (2008) The olfactory vector hypothesis of neurodegenerative disease: is it viable? Ann Neurol 63:7–15
doi: 10.1002/ana.21327
Rey NL, Wesson DW, Brundin P (2018) The olfactory bulb as the entry site for prion-like propagation in neurodegenerative diseases. Neurobiol Dis 109:226–248
doi: 10.1016/j.nbd.2016.12.013
Aguzzi A, Baumann F, Bremer J (2008) The Prion’s elusive reason for being. Annu Rev Neurosci 31:439–477
doi: 10.1146/annurev.neuro.31.060407.125620