Skip to main content
Top
Published in: Neurological Sciences 2/2019

01-02-2019 | Original Article

Association of olfaction dysfunction with brain microstructure in prodromal Parkinson disease

Authors: Hossein Sanjari Moghaddam, Mahsa Dolatshahi, Elaheh Salardini, Mohammad Hadi Aarabi

Published in: Neurological Sciences | Issue 2/2019

Login to get access

Abstract

Objective

Although olfaction dysfunction is now considered as an established clinical marker of prodromal Parkinson disease (PD), little is known about the neural underpinnings of olfaction dysfunction in the prodromal phase of PD. The aim of this study was to examine the microstructural association of olfaction in prodromal PD compared to early stage drug-naïve PD patients.

Methods

Diffusion MRI connectometry was conducted on 18 early PD and 17 prodromal PD patients to investigate the differences in group in terms of altered connectivity, i.e., integrity of white matter tracts, and subsequently to study the correlation of University of Pennsylvania Smell Identification Test (UPSIT) score to white matter integrity in each group using a multiple regression model considering age, sex, RBD, and MoCA, as covariates.

Results

Individuals with prodromal PD had significantly higher quantitative anisotropy (QA) comparing with PD patients in bilateral middle cerebellar peduncles and right arcuate fasciculus. Multiple regression analysis in prodromal PD demonstrated positive association between UPSIT score and connectivity in left and right subgenual cingulum, right inferior fronto-occipital fasciculus, left corticospinal tract, left parietopontine, left corticothalamic tract, and the body and the splenium of corpus callosum.

Conclusion

These results indicate that PD and prodromal PD patients, which were matched for sex, UPSIT, and MoCA scores, have different white matter fiber architecture. Thus, it is postulated that olfaction dysfunction in prodromal and early clinical phases of PD may involve distinct pathogenesis. Increased network connectivity in prodromal and early PD may suggest the neural compensation.
Literature
1.
3.
go back to reference Ansari M, Adib Moradi S, Ghazi Sherbaf F, Hedayatnia A, Aarabi MH (2018) Comparison of structural connectivity in Parkinson’s disease with depressive symptoms versus non-depressed: a diffusion MRI connectometry study. Int Psychogeriatr:1–8. https://doi.org/10.1017/s1041610218000170 Ansari M, Adib Moradi S, Ghazi Sherbaf F, Hedayatnia A, Aarabi MH (2018) Comparison of structural connectivity in Parkinson’s disease with depressive symptoms versus non-depressed: a diffusion MRI connectometry study. Int Psychogeriatr:1–8. https://​doi.​org/​10.​1017/​s104161021800017​0
5.
go back to reference Berg D, Postuma RB, Adler CH, Bloem BR, Chan P, Dubois B, Gasser T, Goetz CG, Halliday G, Joseph L, Lang AE, Liepelt-Scarfone I, Litvan I, Marek K, Obeso J, Oertel W, Olanow CW, Poewe W, Stern M, Deuschl G (2015) MDS research criteria for prodromal Parkinson’s disease. Mov Dis 30(12):1600–1611. https://doi.org/10.1002/mds.26431 CrossRef Berg D, Postuma RB, Adler CH, Bloem BR, Chan P, Dubois B, Gasser T, Goetz CG, Halliday G, Joseph L, Lang AE, Liepelt-Scarfone I, Litvan I, Marek K, Obeso J, Oertel W, Olanow CW, Poewe W, Stern M, Deuschl G (2015) MDS research criteria for prodromal Parkinson’s disease. Mov Dis 30(12):1600–1611. https://​doi.​org/​10.​1002/​mds.​26431 CrossRef
6.
go back to reference Berg D, Postuma RB, Bloem B, Chan P, Dubois B, Gasser T, Goetz CG, Halliday GM, Hardy J, Lang AE, Litvan I, Marek K, Obeso J, Oertel W, Olanow CW, Poewe W, Stern M, Deuschl G (2014) Time to redefine PD? Introductory statement of the MDS Task Force on the definition of Parkinson’s disease. Mov Dis 29(4):454–462. https://doi.org/10.1002/mds.25844 CrossRef Berg D, Postuma RB, Bloem B, Chan P, Dubois B, Gasser T, Goetz CG, Halliday GM, Hardy J, Lang AE, Litvan I, Marek K, Obeso J, Oertel W, Olanow CW, Poewe W, Stern M, Deuschl G (2014) Time to redefine PD? Introductory statement of the MDS Task Force on the definition of Parkinson’s disease. Mov Dis 29(4):454–462. https://​doi.​org/​10.​1002/​mds.​25844 CrossRef
8.
go back to reference Postuma RB, Aarsland D, Barone P, Burn DJ, Hawkes CH, Oertel W, Ziemssen T (2012) Identifying prodromal Parkinson’s disease: pre-motor disorders in Parkinson’s disease. Mov Disord 27(5):617–626PubMedCrossRef Postuma RB, Aarsland D, Barone P, Burn DJ, Hawkes CH, Oertel W, Ziemssen T (2012) Identifying prodromal Parkinson’s disease: pre-motor disorders in Parkinson’s disease. Mov Disord 27(5):617–626PubMedCrossRef
9.
go back to reference 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(2):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(2):197–211CrossRefPubMed
10.
go back to reference Chu S, Downes JJ (2000) Odour-evoked autobiographical memories: psychological investigations of Proustian phenomena. Chem Senses 25(1):111–116PubMedCrossRef Chu S, Downes JJ (2000) Odour-evoked autobiographical memories: psychological investigations of Proustian phenomena. Chem Senses 25(1):111–116PubMedCrossRef
12.
go back to reference Berg D, Marek K, Ross GW, Poewe W (2012) Defining at-risk populations for Parkinson’s disease: lessons from ongoing studies. Mov Disord 27(5):656–665PubMedCrossRef Berg D, Marek K, Ross GW, Poewe W (2012) Defining at-risk populations for Parkinson’s disease: lessons from ongoing studies. Mov Disord 27(5):656–665PubMedCrossRef
13.
go back to reference Haehner A, Hummel T, Hummel C, Sommer U, Junghanns S, Reichmann H (2007) Olfactory loss may be a first sign of idiopathic Parkinson’s disease. Mov Disord 22(6):839–842PubMedCrossRef Haehner A, Hummel T, Hummel C, Sommer U, Junghanns S, Reichmann H (2007) Olfactory loss may be a first sign of idiopathic Parkinson’s disease. Mov Disord 22(6):839–842PubMedCrossRef
14.
go back to reference Ross GW, Petrovitch H, Abbott RD, Tanner CM, Popper J, Masaki K, Launer L, White LR (2008) Association of olfactory dysfunction with risk for future Parkinson’s disease. Ann Neurol 63(2):167–173PubMedCrossRef Ross GW, Petrovitch H, Abbott RD, Tanner CM, Popper J, Masaki K, Launer L, White LR (2008) Association of olfactory dysfunction with risk for future Parkinson’s disease. Ann Neurol 63(2):167–173PubMedCrossRef
15.
go back to reference Ponsen MM, Stoffers D, Twisk JW, Wolters EC, Berendse HW (2009) Hyposmia and executive dysfunction as predictors of future Parkinson’s disease: a prospective study. Mov Disord 24(7):1060–1065PubMedCrossRef Ponsen MM, Stoffers D, Twisk JW, Wolters EC, Berendse HW (2009) Hyposmia and executive dysfunction as predictors of future Parkinson’s disease: a prospective study. Mov Disord 24(7):1060–1065PubMedCrossRef
16.
go back to reference Postuma RB, Gagnon JF, Vendette M, Desjardins C, Montplaisir JY (2011) Olfaction and color vision identify impending neurodegeneration in rapid eye movement sleep behavior disorder. Ann Neurol 69(5):811–818PubMedCrossRef Postuma RB, Gagnon JF, Vendette M, Desjardins C, Montplaisir JY (2011) Olfaction and color vision identify impending neurodegeneration in rapid eye movement sleep behavior disorder. Ann Neurol 69(5):811–818PubMedCrossRef
17.
go back to reference Mahlknecht P, Iranzo A, Högl B, Frauscher B, Müller C, Santamaría J, Tolosa E, Serradell M, Mitterling T, Gschliesser V (2015) Olfactory dysfunction predicts early transition to a Lewy body disease in idiopathic RBD. Neurology 84(7):654–658PubMedCrossRef Mahlknecht P, Iranzo A, Högl B, Frauscher B, Müller C, Santamaría J, Tolosa E, Serradell M, Mitterling T, Gschliesser V (2015) Olfactory dysfunction predicts early transition to a Lewy body disease in idiopathic RBD. Neurology 84(7):654–658PubMedCrossRef
18.
go back to reference Jennings D, Stern M, Siderowf A, Eberly S, Oakes D, Marek K (2015) Longitudinal imaging and phenoconversion in the PARS prodromal cohort. Mov Disord 30:S383 Jennings D, Stern M, Siderowf A, Eberly S, Oakes D, Marek K (2015) Longitudinal imaging and phenoconversion in the PARS prodromal cohort. Mov Disord 30:S383
19.
go back to reference Postuma RB, Berg D (2016) Advances in markers of prodromal Parkinson disease. Nat Rev Neurol 12(11):622–634PubMedCrossRef Postuma RB, Berg D (2016) Advances in markers of prodromal Parkinson disease. Nat Rev Neurol 12(11):622–634PubMedCrossRef
23.
go back to reference Stern MB, Doty RL, Dotti M, Corcoran P, Crawford D, McKeown DA, Adler C, Gollomp S, Hurtig H (1994) Olfactory function in Parkinson’s disease subtypes. Neurology 44(2):266–268PubMedCrossRef Stern MB, Doty RL, Dotti M, Corcoran P, Crawford D, McKeown DA, Adler C, Gollomp S, Hurtig H (1994) Olfactory function in Parkinson’s disease subtypes. Neurology 44(2):266–268PubMedCrossRef
24.
go back to reference Doty RL, Shaman P, Dann M (1984) Development of the University of Pennsylvania Smell Identification Test: a standardized microencapsulated test of olfactory function. Physiol Behav 32(3):489–502PubMedCrossRef Doty RL, Shaman P, Dann M (1984) Development of the University of Pennsylvania Smell Identification Test: a standardized microencapsulated test of olfactory function. Physiol Behav 32(3):489–502PubMedCrossRef
25.
go back to reference Baba T, Kikuchi A, Hirayama K, Nishio Y, Hosokai Y, Kanno S, Hasegawa T, Sugeno N, Konno M, Suzuki K, Takahashi S, Fukuda H, Aoki M, Itoyama Y, Mori E, Takeda A (2012) Severe olfactory dysfunction is a prodromal symptom of dementia associated with Parkinson’s disease: a 3 year longitudinal study. Brain 135(Pt 1):161–169. https://doi.org/10.1093/brain/awr321 PubMedCrossRef Baba T, Kikuchi A, Hirayama K, Nishio Y, Hosokai Y, Kanno S, Hasegawa T, Sugeno N, Konno M, Suzuki K, Takahashi S, Fukuda H, Aoki M, Itoyama Y, Mori E, Takeda A (2012) Severe olfactory dysfunction is a prodromal symptom of dementia associated with Parkinson’s disease: a 3 year longitudinal study. Brain 135(Pt 1):161–169. https://​doi.​org/​10.​1093/​brain/​awr321 PubMedCrossRef
26.
go back to reference Baba T, Takeda A, Kikuchi A, Nishio Y, Hosokai Y, Hirayama K, Hasegawa T, Sugeno N, Suzuki K, Mori E, Takahashi S, Fukuda H, Itoyama Y (2011) Association of olfactory dysfunction and brain. Metabolism in Parkinson’s disease. Mov Dis 26(4):621–628. https://doi.org/10.1002/mds.23602 CrossRef Baba T, Takeda A, Kikuchi A, Nishio Y, Hosokai Y, Hirayama K, Hasegawa T, Sugeno N, Suzuki K, Mori E, Takahashi S, Fukuda H, Itoyama Y (2011) Association of olfactory dysfunction and brain. Metabolism in Parkinson’s disease. Mov Dis 26(4):621–628. https://​doi.​org/​10.​1002/​mds.​23602 CrossRef
27.
go back to reference Berendse HW, Booij J, Francot CM, Bergmans PL, Hijman R, Stoof JC, Wolters EC (2001) Subclinical dopaminergic dysfunction in asymptomatic Parkinson’s disease patients’ relatives with a decreased sense of smell. Ann Neurol 50(1):34–41PubMedCrossRef Berendse HW, Booij J, Francot CM, Bergmans PL, Hijman R, Stoof JC, Wolters EC (2001) Subclinical dopaminergic dysfunction in asymptomatic Parkinson’s disease patients’ relatives with a decreased sense of smell. Ann Neurol 50(1):34–41PubMedCrossRef
34.
go back to reference Leemans A, Jeurissen B, Sijbers J, Jones D (2009) ExploreDTI: a graphical toolbox for processing, analyzing, and visualizing diffusion MR data. In: 17th Annual Meeting of Intl Soc Mag Reson Med. p 3537 Leemans A, Jeurissen B, Sijbers J, Jones D (2009) ExploreDTI: a graphical toolbox for processing, analyzing, and visualizing diffusion MR data. In: 17th Annual Meeting of Intl Soc Mag Reson Med. p 3537
39.
go back to reference van Uem JM, Marinus J, Canning C, van Lummel R, Dodel R, Liepelt-Scarfone I, Berg D, Morris ME, Maetzler W (2016) Health-related quality of life in patients with Parkinson’s disease—a systematic review based on the ICF model. Neurosci Biobehav Rev 61:26–34PubMedCrossRef van Uem JM, Marinus J, Canning C, van Lummel R, Dodel R, Liepelt-Scarfone I, Berg D, Morris ME, Maetzler W (2016) Health-related quality of life in patients with Parkinson’s disease—a systematic review based on the ICF model. Neurosci Biobehav Rev 61:26–34PubMedCrossRef
42.
go back to reference Marek K, Jennings D, Lasch S, Siderowf A, Tanner C, Simuni T, Coffey C, Kieburtz K, Flagg E, Chowdhury S (2011) The parkinson progression marker initiative (PPMI). Prog Neurobiol 95(4):629–635CrossRefPubMedCentral Marek K, Jennings D, Lasch S, Siderowf A, Tanner C, Simuni T, Coffey C, Kieburtz K, Flagg E, Chowdhury S (2011) The parkinson progression marker initiative (PPMI). Prog Neurobiol 95(4):629–635CrossRefPubMedCentral
46.
go back to reference Tessa C, Lucetti C, Giannelli M, Diciotti S, Poletti M, Danti S, Baldacci F, Vignali C, Bonuccelli U, Mascalchi M, Toschi N (2014) Progression of brain atrophy in the early stages of Parkinson’s disease: a longitudinal tensor-based morphometry study in de novo patients without cognitive impairment. Hum Brain Mapp 35(8):3932–3944. https://doi.org/10.1002/hbm.22449 PubMedCrossRefPubMedCentral Tessa C, Lucetti C, Giannelli M, Diciotti S, Poletti M, Danti S, Baldacci F, Vignali C, Bonuccelli U, Mascalchi M, Toschi N (2014) Progression of brain atrophy in the early stages of Parkinson’s disease: a longitudinal tensor-based morphometry study in de novo patients without cognitive impairment. Hum Brain Mapp 35(8):3932–3944. https://​doi.​org/​10.​1002/​hbm.​22449 PubMedCrossRefPubMedCentral
53.
go back to reference Scherfler C, Frauscher B, Schocke M, Iranzo A, Gschliesser V, Seppi K, Santamaria J, Tolosa E, Hogl B, Poewe W (2011) White and gray matter abnormalities in idiopathic rapid eye movement sleep behavior disorder: a diffusion-tensor imaging and voxel-based morphometry study. Ann Neurol 69(2):400–407. https://doi.org/10.1002/ana.22245 PubMedCrossRef Scherfler C, Frauscher B, Schocke M, Iranzo A, Gschliesser V, Seppi K, Santamaria J, Tolosa E, Hogl B, Poewe W (2011) White and gray matter abnormalities in idiopathic rapid eye movement sleep behavior disorder: a diffusion-tensor imaging and voxel-based morphometry study. Ann Neurol 69(2):400–407. https://​doi.​org/​10.​1002/​ana.​22245 PubMedCrossRef
57.
go back to reference 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 Dis 25(12):1888–1894. https://doi.org/10.1002/mds.23208 CrossRef 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 Dis 25(12):1888–1894. https://​doi.​org/​10.​1002/​mds.​23208 CrossRef
Metadata
Title
Association of olfaction dysfunction with brain microstructure in prodromal Parkinson disease
Authors
Hossein Sanjari Moghaddam
Mahsa Dolatshahi
Elaheh Salardini
Mohammad Hadi Aarabi
Publication date
01-02-2019
Publisher
Springer International Publishing
Published in
Neurological Sciences / Issue 2/2019
Print ISSN: 1590-1874
Electronic ISSN: 1590-3478
DOI
https://doi.org/10.1007/s10072-018-3629-2

Other articles of this Issue 2/2019

Neurological Sciences 2/2019 Go to the issue