Correlation of olfactory function factors with cardiac sympathetic denervation in Parkinson's disease.

123I-meta-iodobenzylguanidine Cardiac sympathetic denervation Factor analysis Olfactory function Parkinson’s disease Selective hyposmia Smell identification test

Journal

Journal of neurology
ISSN: 1432-1459
Titre abrégé: J Neurol
Pays: Germany
ID NLM: 0423161

Informations de publication

Date de publication:
Mar 2024
Historique:
received: 10 08 2023
accepted: 23 10 2023
revised: 19 10 2023
medline: 27 2 2024
pubmed: 9 11 2023
entrez: 8 11 2023
Statut: ppublish

Résumé

Hyposmia is a common nonmotor symptom of Parkinson's disease (PD) and reportedly associated with dysautonomia in PD. The smell identification test for measuring olfactory function consists of multiple items to discriminate specific scents. In the present study, factor analysis of the smell identification test was performed, and the correlation of extracted factors with cardiac sympathetic denervation (CSD) in patients with PD was investigated. The present study included 183 early PD patients who underwent the Cross-Cultural Smell Identification Test (CC-SIT) and The mean CC-SIT score was 6.1 ± 2.6, and 133 patients (72.7%) had CSD. The CC-SIT score and five smell factors were not associated with dopamine transporter uptake or cognitive functions. However, the CC-SIT score significantly correlated with age (P < 0.001) and late H/M ratio (P < 0.001). Factors 1 and 5 showed an increasing trend with larger H/M ratio, although it was not statistically significant (β = 0.203, P = 0.085 and β = 0.230, P = 0.085, respectively). Factor 5 significantly correlated with the H/M ratio in PD patients with CSD (β = 0.676, P = 0.036). The results showed olfactory dysfunction to be selectively associated with cardiac sympathetic burden in PD. The correlation of certain factors with CSD indicates the possibility of selective hyposmia in PD patients.

Sections du résumé

BACKGROUND BACKGROUND
Hyposmia is a common nonmotor symptom of Parkinson's disease (PD) and reportedly associated with dysautonomia in PD. The smell identification test for measuring olfactory function consists of multiple items to discriminate specific scents. In the present study, factor analysis of the smell identification test was performed, and the correlation of extracted factors with cardiac sympathetic denervation (CSD) in patients with PD was investigated.
METHODS METHODS
The present study included 183 early PD patients who underwent the Cross-Cultural Smell Identification Test (CC-SIT) and
RESULTS RESULTS
The mean CC-SIT score was 6.1 ± 2.6, and 133 patients (72.7%) had CSD. The CC-SIT score and five smell factors were not associated with dopamine transporter uptake or cognitive functions. However, the CC-SIT score significantly correlated with age (P < 0.001) and late H/M ratio (P < 0.001). Factors 1 and 5 showed an increasing trend with larger H/M ratio, although it was not statistically significant (β = 0.203, P = 0.085 and β = 0.230, P = 0.085, respectively). Factor 5 significantly correlated with the H/M ratio in PD patients with CSD (β = 0.676, P = 0.036).
DISCUSSION CONCLUSIONS
The results showed olfactory dysfunction to be selectively associated with cardiac sympathetic burden in PD. The correlation of certain factors with CSD indicates the possibility of selective hyposmia in PD patients.

Identifiants

pubmed: 37940708
doi: 10.1007/s00415-023-12080-8
pii: 10.1007/s00415-023-12080-8
doi:

Substances chimiques

3-Iodobenzylguanidine 35MRW7B4AD
Iodine-123 8YWR746RPQ
Iodine Radioisotopes 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1397-1407

Subventions

Organisme : National Research Foundation of Korea
ID : NRF-2017R1D1A1B06028086
Organisme : National Institute of Health (KR)
ID : 2021-ER1008-02

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany.

Références

Hubbard PS, Esiri MM, Reading M, McShane R, Nagy Z (2007) Alpha-synuclein pathology in the olfactory pathways of dementia patients. J Anat 211(1):117–124. https://doi.org/10.1111/j.1469-7580.2007.00748.x
doi: 10.1111/j.1469-7580.2007.00748.x pubmed: 17553102 pmcid: 2375794
Stokholm MG, Danielsen EH, Hamilton-Dutoit SJ, Borghammer P (2016) Pathological α-synuclein in gastrointestinal tissues from prodromal Parkinson disease patients. Ann Neurol 79(6):940–949. https://doi.org/10.1002/ana.24648
doi: 10.1002/ana.24648 pubmed: 27015771
Orimo S, Takahashi A, Uchihara T, Mori F, Kakita A, Wakabayashi K et al (2007) Degeneration of cardiac sympathetic nerve begins in the early disease process of Parkinson’s disease. Brain Pathol 17(1):24–30. https://doi.org/10.1111/j.1750-3639.2006.00032.x
doi: 10.1111/j.1750-3639.2006.00032.x pubmed: 17493034 pmcid: 8095543
Schapira AHV, Chaudhuri KR, Jenner P (2017) Non-motor features of Parkinson disease. Nat Rev Neurosci 18(7):435–450. https://doi.org/10.1038/nrn.2017.62
doi: 10.1038/nrn.2017.62 pubmed: 28592904
Postuma RB, Berg D (2016) Advances in markers of prodromal Parkinson disease. Nat Rev Neurol 12(11):622–634. https://doi.org/10.1038/nrneurol.2016.152
doi: 10.1038/nrneurol.2016.152 pubmed: 27786242
Bohnen NI, Studenski SA, Constantine GM, Moore RY (2008) Diagnostic performance of clinical motor and non-motor tests of Parkinson disease: a matched case-control study. Eur J Neurol 15(7):685–691. https://doi.org/10.1111/j.1468-1331.2008.02148.x
doi: 10.1111/j.1468-1331.2008.02148.x pubmed: 18435767
Mao CJ, Wang F, Chen JP, Yang YP, Chen J, Huang JY et al (2017) Odor selectivity of hyposmia and cognitive impairment in patients with Parkinson’s disease. Clin Interv Aging 12:1637–1644. https://doi.org/10.2147/CIA.S147588
doi: 10.2147/CIA.S147588 pubmed: 29070942 pmcid: 5640420
Bohnen NI, Gedela S, Herath P, Constantine GM, Moore RY (2008) Selective hyposmia in Parkinson disease: association with hippocampal dopamine activity. Neurosci Lett 447(1):12–16. https://doi.org/10.1016/j.neulet.2008.09.070
doi: 10.1016/j.neulet.2008.09.070 pubmed: 18838108 pmcid: 2634293
Double KL, Rowe DB, Hayes M, Chan DK, Blackie J, Corbett A et al (2003) Identifying the pattern of olfactory deficits in Parkinson disease using the brief smell identification test. Arch Neurol 60(4):545–549. https://doi.org/10.1001/archneur.60.4.545
doi: 10.1001/archneur.60.4.545 pubmed: 12707068
Daum RF, Sekinger B, Kobal G, Lang CJ (2000) Olfactory testing with “sniffin’ sticks” or clinical diagnosis of Parkinson disease. Nervenarzt 71(8):643–650. https://doi.org/10.1007/s001150050640
doi: 10.1007/s001150050640 pubmed: 10996914
Hawkes CH, Shephard BC (1993) Selective anosmia in Parkinson’s disease? Lancet 341(8842):435–436
doi: 10.1016/0140-6736(93)93027-X pubmed: 8094195
Hähner A, Maboshe W, Baptista RB, Storch A, Reichmann H, Hummel T (2013) Selective hyposmia in Parkinson’s disease? J Neurol 260(12):3158–3160. https://doi.org/10.1007/s00415-013-7153-2
doi: 10.1007/s00415-013-7153-2 pubmed: 24158272
Lamotte G, Holmes C, Sullivan P, Lenka A, Goldstein DS (2020) Cardioselective peripheral noradrenergic deficiency in Lewy body synucleinopathies. Ann Clin Transl Neurol 7(12):2450–2460. https://doi.org/10.1002/acn3.51243
doi: 10.1002/acn3.51243 pubmed: 33216462 pmcid: 7732242
Takahashi M, Ikemura M, Oka T, Uchihara T, Wakabayashi K, Kakita A et al (2015) Quantitative correlation between cardiac MIBG uptake and remaining axons in the cardiac sympathetic nerve in Lewy body disease. J Neurol Neurosurg Psychiatry 86(9):939–944. https://doi.org/10.1136/jnnp-2015-310686
doi: 10.1136/jnnp-2015-310686 pubmed: 25935891
Lee PH, Yeo SH, Kim HJ, Youm HY (2006) Correlation between cardiac 123I-MIBG and odor identification in patients with Parkinson’s disease and multiple system atrophy. Mov Disord 21(11):1975–1977. https://doi.org/10.1002/mds.21083
doi: 10.1002/mds.21083 pubmed: 16960860
Mizutani Y, Nakamura T, Okada A, Suzuki J, Watanabe H, Hirayama M et al (2014) Hyposmia and cardiovascular dysautonomia correlatively appear in early-stage Parkinson’s disease. Parkinsonism Relat Disord 20(5):520–524. https://doi.org/10.1016/j.parkreldis.2014.02.010
doi: 10.1016/j.parkreldis.2014.02.010 pubmed: 24637128
Wang XY, Han YY, Li G, Zhang B (2019) Association between autonomic dysfunction and olfactory dysfunction in Parkinson’s disease in southern Chinese. BMC Neurol 19(1):17. https://doi.org/10.1186/s12883-019-1243-4
doi: 10.1186/s12883-019-1243-4 pubmed: 30711006 pmcid: 6359856
Gibb WR, Lees AJ (1988) The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson’s disease. J Neurol Neurosurg Psychiatry 51(6):745–752. https://doi.org/10.1136/jnnp.51.6.745
doi: 10.1136/jnnp.51.6.745 pubmed: 2841426 pmcid: 1033142
Postuma RB, Berg D, Stern M, Poewe W, Olanow CW, Oertel W et al (2015) MDS clinical diagnostic criteria for Parkinson’s disease. Mov Disord 30(12):1591–1601. https://doi.org/10.1002/mds.26424
doi: 10.1002/mds.26424 pubmed: 26474316
Ryu HJ, Yang DW (2023) The Seoul Neuropsychological Screening Battery (SNSB) for comprehensive neuropsychological assessment. Dement Neurocogn Disord 22(1):1–15. https://doi.org/10.12779/dnd.2023.22.1.1
doi: 10.12779/dnd.2023.22.1.1 pubmed: 36814700 pmcid: 9939572
Gibbons CH, Schmidt P, Biaggioni I, Frazier-Mills C, Freeman R, Isaacson S et al (2017) The recommendations of a consensus panel for the screening, diagnosis, and treatment of neurogenic orthostatic hypotension and associated supine hypertension. J Neurol 264(8):1567–1582. https://doi.org/10.1007/s00415-016-8375-x
doi: 10.1007/s00415-016-8375-x pubmed: 28050656 pmcid: 5533816
Doty RL, Marcus A, Lee WW (1996) Development of the 12-item cross-cultural smell identification test (CC-SIT). Laryngoscope 106(3 Pt 1):353–356. https://doi.org/10.1097/00005537-199603000-00021
doi: 10.1097/00005537-199603000-00021 pubmed: 8614203
Ryu DW, Kim JS, Lee JE, Oh YS, Yoo SW, Yoo IR et al (2019) Initial versus follow-up sequential myocardial 123I-MIBG scintigraphy to discriminate Parkinson disease from atypical parkinsonian syndromes. Clin Nuclear Med 44(4):282–288. https://doi.org/10.1097/RLU.0000000000002424
doi: 10.1097/RLU.0000000000002424
Horsager J, Knudsen K, Sommerauer M (2022) Clinical and imaging evidence of brain-first and body-first Parkinson’s disease. Neurobiol Dis 164:105626. https://doi.org/10.1016/j.nbd.2022.105626
doi: 10.1016/j.nbd.2022.105626 pubmed: 35031485
Iijima M, Osawa M, Momose M, Kobayakawa T, Saito S, Iwata M et al (2010) Cardiac sympathetic degeneration correlates with olfactory function in Parkinson’s disease. Mov Disord 25(9):1143–1149. https://doi.org/10.1002/mds.23001
doi: 10.1002/mds.23001 pubmed: 20131383
Ubeda-Bañon I, Saiz-Sanchez D, de la Rosa-Prieto C, Martinez-Marcos A (2014) α-Synuclein in the olfactory system in Parkinson’s disease: role of neural connections on spreading pathology. Brain Struct Funct 219(5):1513–1526. https://doi.org/10.1007/s00429-013-0651-2
doi: 10.1007/s00429-013-0651-2 pubmed: 24135772
Horsager J, Andersen KB, Knudsen K, Skjærbæk C, Fedorova TD, Okkels N et al (2020) Brain-first versus body-first Parkinson’s disease: a multimodal imaging case-control study. Brain 143(10):3077–3088. https://doi.org/10.1093/brain/awaa238
doi: 10.1093/brain/awaa238 pubmed: 32830221
Ryu DW, Yoo SW, Oh YS, Lee KS, Ha S, Kim JS (2022) Comparison of disease progression between brain-predominant Parkinson’s disease versus Parkinson’s disease with body-involvement phenotypes. Neurobiol Dis 174:105883. https://doi.org/10.1016/j.nbd.2022.105883
doi: 10.1016/j.nbd.2022.105883 pubmed: 36208865
Knudsen K, Fedorova TD, Horsager J, Andersen KB, Skjærbæk C, Berg D et al (2021) Asymmetric dopaminergic dysfunction in brain-first versus body-first Parkinson’s disease subtypes. J Parkinsons Dis 11(4):1677–1687. https://doi.org/10.3233/JPD-212761
doi: 10.3233/JPD-212761 pubmed: 34334424
Ercoli T, Masala C, Cadeddu G, Mascia MM, Orofino G, Gigante AF et al (2022) Does olfactory dysfunction correlate with disease progression in Parkinson’s disease? A systematic review of the current literature. Brain Sci 12(5):513. https://doi.org/10.3390/brainsci12050513
doi: 10.3390/brainsci12050513 pubmed: 35624900 pmcid: 9139278
Yoo HS, Chung SJ, Lee YH, Ye BS, Sohn YH, Lee PH (2020) Association between olfactory deficit and motor and cognitive function in Parkinson’s disease. J Mov Disord 13(2):133–141. https://doi.org/10.14802/jmd.19082
doi: 10.14802/jmd.19082 pubmed: 32241078 pmcid: 7280943
Masala C, Solla P, Liscia A, Defazio G, Saba L, Cannas A et al (2018) Correlation among olfactory function, motors’ symptoms, cognitive impairment, apathy, and fatigue in patients with Parkinson’s disease. J Neurol 265(8):1764–1771. https://doi.org/10.1007/s00415-018-8913-9
doi: 10.1007/s00415-018-8913-9 pubmed: 29804147
Kim JS, Park HE, Park IS, Oh YS, Ryu DW, Song IU et al (2017) Normal ‘heart’ in Parkinson’s disease: is this a distinct clinical phenotype? Eur J Neurol 24(2):349–356. https://doi.org/10.1111/ene.13206
doi: 10.1111/ene.13206 pubmed: 27888574
Papazian EJ, Pinto JM (2021) Olfactory loss and aging: connections with health and well-being. Chem Senses 46:bjab045. https://doi.org/10.1093/chemse/bjab045
doi: 10.1093/chemse/bjab045 pubmed: 34673938
Yang Z, Xie Y, Dou K, Yang L, Xie A (2023) Associations of striatal dopamine transporter binding with motor and non-motor symptoms in early Parkinson’s disease. Clin Transl Sci 16(6):1021–1038. https://doi.org/10.1111/cts.13508
doi: 10.1111/cts.13508 pubmed: 36915231 pmcid: 10264928
Meles SK, Oertel WH, Leenders KL (2021) Circuit imaging biomarkers in preclinical and prodromal Parkinson’s disease. Mol Med 27(1):111. https://doi.org/10.1186/s10020-021-00327-x
doi: 10.1186/s10020-021-00327-x pubmed: 34530732 pmcid: 8447708
Schwarz J, Storch A, Koch W, Pogarell O, Radau PE, Tatsch K (2004) Loss of dopamine transporter binding in Parkinson’s disease follows a single exponential rather than linear decline. J Nucl Med 45(10):1694–1697
pubmed: 15471835
Bohnen NI, Müller ML (2013) In vivo neurochemical imaging of olfactory dysfunction in Parkinson’s disease. J Neural Transm (Vienna) 120(4):571–576. https://doi.org/10.1007/s00702-012-0956-y
doi: 10.1007/s00702-012-0956-y pubmed: 23263541
Solla P, Masala C, Ercoli T, Frau C, Bagella C, Pinna I et al (2023) Olfactory impairment correlates with executive functions disorders and other specific cognitive dysfunctions in Parkinson’s disease. Biology (Basel) 12(1):112. https://doi.org/10.3390/biology12010112
doi: 10.3390/biology12010112 pubmed: 36671804
Cecchini MP, Federico A, Zanini A, Mantovani E, Masala C, Tinazzi M et al (2019) Olfaction and taste in Parkinson’s disease: the association with mild cognitive impairment and the single cognitive domain dysfunction. J Neural Transm (Vienna) 126(5):585–595. https://doi.org/10.1007/s00702-019-01996-z
doi: 10.1007/s00702-019-01996-z pubmed: 30911822
Camargo CHF, Jobbins VA, Serpa RA, Berbetz FA, Sabatini JS, Teive HAG (2018) Association between olfactory loss and cognitive deficits in Parkinson’s disease. Clin Neurol Neurosurg 173:120–123. https://doi.org/10.1016/j.clineuro.2018.08.018
doi: 10.1016/j.clineuro.2018.08.018 pubmed: 30121454
Bohnen NI, Gedela S, Kuwabara H, Constantine GM, Mathis CA, Studenski SA et al (2007) Selective hyposmia and nigrostriatal dopaminergic denervation in Parkinson’s disease. J Neurol 254(1):84–90. https://doi.org/10.1007/s00415-006-0284-y
doi: 10.1007/s00415-006-0284-y pubmed: 17508142
Trentin S, Fraiman de Oliveira BS, Ferreira Felloni Borges Y, de Mello Rieder CR (2022) Systematic review and meta-analysis of Sniffin sticks test performance in Parkinson’s disease patients in different countries. Eur Arch Otorhinolaryngol 279(3):1123–1145. https://doi.org/10.1007/s00405-021-06970-8
doi: 10.1007/s00405-021-06970-8 pubmed: 34319482
Cersosimo MG, Benarroch EE, Raina GB (2021) Lewy bodies in the olfactory system and the hypothalamus. Handb Clin Neurol 182:235–244. https://doi.org/10.1016/B978-0-12-819973-2.00016-2
doi: 10.1016/B978-0-12-819973-2.00016-2 pubmed: 34266595
Bang Y, Lim J, Choi HJ (2021) Recent advances in the pathology of prodromal non-motor symptoms olfactory deficit and depression in Parkinson’s disease: clues to early diagnosis and effective treatment. Arch Pharm Res 44(6):588–604. https://doi.org/10.1007/s12272-021-01337-3
doi: 10.1007/s12272-021-01337-3 pubmed: 34145553 pmcid: 8254697
Lee YH, Bak Y, Park CH, Chung SJ, Yoo HS, Baik K et al (2020) Patterns of olfactory functional networks in Parkinson’s disease dementia and Alzheimer’s dementia. Neurobiol Aging 89:63–70. https://doi.org/10.1016/j.neurobiolaging.2019.12.021
doi: 10.1016/j.neurobiolaging.2019.12.021 pubmed: 31980278
Morley JF, Cohen A, Silveira-Moriyama L, Lees AJ, Williams DR, Katzenschlager R et al (2018) Optimizing olfactory testing for the diagnosis of Parkinson’s disease: item analysis of the university of Pennsylvania smell identification test. NPJ Parkinsons Dis 4:2. https://doi.org/10.1038/s41531-017-0039-8
doi: 10.1038/s41531-017-0039-8 pubmed: 29354684 pmcid: 5768805

Auteurs

Dong-Woo Ryu (DW)

Department of Neurology, College of Medicine, The Catholic University of Korea, 222, Banpo-Daero, Seocho-gu, Seoul, 06591, Republic of Korea.

Sang-Won Yoo (SW)

Department of Neurology, College of Medicine, The Catholic University of Korea, 222, Banpo-Daero, Seocho-gu, Seoul, 06591, Republic of Korea.

Ko-Eun Choi (KE)

Department of Neurology, College of Medicine, The Catholic University of Korea, 222, Banpo-Daero, Seocho-gu, Seoul, 06591, Republic of Korea.

Yoon-Sang Oh (YS)

Department of Neurology, College of Medicine, The Catholic University of Korea, 222, Banpo-Daero, Seocho-gu, Seoul, 06591, Republic of Korea.

Joong-Seok Kim (JS)

Department of Neurology, College of Medicine, The Catholic University of Korea, 222, Banpo-Daero, Seocho-gu, Seoul, 06591, Republic of Korea. neuronet@catholic.ac.kr.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH