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HOME > J Mov Disord > Volume 17(4); 2024 > Article
Letter to the editor
Olfactory and Gustatory Function in Early-Stage Parkinson’s Disease: Implications for Cognitive Association
Jeongjae Lee1orcid, Young Eun Kim2,3corresp_iconorcid, Joong Seob Lee4orcid, Suk Yun Kang5orcid, Min Seung Kim5orcid, In Hee Kwak2,3orcid, Jaeseol Park2orcid, Jung Yeon Nam2,3orcid, Hyeo-il Ma2,3corresp_iconorcid
Journal of Movement Disorders 2024;17(4):450-452.
DOI: https://doi.org/10.14802/jmd.23243
Published online: June 27, 2024

1Department of Neurology, Chuncheon Sacred Heart Hospital, Hallym University College of Medicine, Chuncheon, Korea

2Department of Neurology, Hallym University Sacred Heart Hospital, Hallym University College of Medicine, Anyang, Korea

3Hallym Neurological Institute, Hallym University, Anyang, Korea

4Department of Otorhinolaryngology-Head and Neck Surgery, Hallym University Sacred Heart Hospital, Hallym University College of Medicine, Anyang, Korea

5Department of Neurology, Dongtan Sacred Heart Hospital, Hallym University College of Medicine, Hwaseong, Korea

Corresponding author: Hyeo-il Ma, MD, PhD Department of Neurology, Hallym University Sacred Heart Hospital, Hallym University College of Medicine, 22 Gwanpyeong-ro 170beon-gil, Dongan-gu, Anyang 14068, Korea / Tel: +82-31-380-3740 / Fax: +82-31-380-3748 / E-mail: hima@hallym.ac.kr
Corresponding author: Young Eun Kim, MD, PhD Department of Neurology, Hallym University Sacred Heart Hospital, Hallym University College of Medicine, 22 Gwanpyeong-ro 170beon-gil, Dongan-gu, Anyang 14068, Korea / Tel: +82-31-380-3740 / Fax: +82-31-380-3748 / E-mail: yekneurology@hallym.or.kr
• Received: November 20, 2023   • Revised: January 9, 2024   • Accepted: June 27, 2024

Copyright © 2024 The Korean Movement Disorder Society

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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Dear Editor,
Cognitive impairment is a prevalent nonmotor symptom of Parkinson’s disease (PD) that significantly impacts quality of life, particularly in the later stage of PD. Hyposmia and hypogeusia are also recognized as nonmotor symptoms of PD and are often interrelated [1,2]. While hyposmia has been identified as a potential risk factor for dementia in PD patients [3], few studies have investigated the association between hyposmia and cognitive functioning in early-stage PD patients. Moreover, there is a lack of research on the relationship between gustatory function and cognition. Therefore, we conducted a study to investigate the associations between olfactory or gustatory function and cognitive functioning in early-stage PD patients without dementia.
The study included patients with newly diagnosed, drug-naïve PD and excluded individuals with nasal or oral cavity disorders and those meeting the DSM-V criteria for dementia. The Movement Disorder Society-Sponsored Revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS), modified Hoehn and Yahr (H&Y) scale, Geriatric Depression Scale (GDS), Korean version of the Montreal Cognitive Assessment (MoCA), Seoul Neuropsychological Screening Battery (SNSB), YSK olfactory function (YOF) test, and YSK gustatory function (YGF) test were administered at diagnosis. The participants were categorized on the basis of the presence of mild cognitive impairment (MCI) in accordance with criteria outlined by the MDS. The specific neuropsychological tests used to identify PD with MCI (PD-MCI) were selected from the SNSB, with impairment defined as performance falling more than 1.0 standard deviations below the normative mean. Details regarding the olfactory and gustatory function tests, as well as the statistical methods, are provided in the Supplementary Material (in the online-only Data Supplement).
Our study involved 84 consecutively enrolled PD patients, and the results revealed that the mean YOF total score indicated hyposmia (≤21), whereas the mean YGF total score indicated normal gustatory function (≤12) (Supplementary Table 1 in the online-only Data Supplement).
Multiple linear regression analysis revealed significant correlations between global cognition (MoCA score) and age (p < 0.001), sex (p < 0.001), olfactory discrimination (p = 0.015), and gustatory function test results (p = 0.021) in PD patients (Table 1 and Supplementary Figure 1 in the online-only Data Supplement). The covariates included age, sex, education, disease duration, H&Y stage, MDS-UPDRS part III score, GDS score, olfactory threshold, discrimination, YOF test score, and total YGF test score. However, when the five individual cognitive domains were analyzed, no clear associations with olfactory or gustatory functions were found. A multicollinearity assessment revealed that the variance inflation factor values were less than 2, indicating weak correlations between variables.
Additionally, no significant differences in olfactory or gustatory functions were observed between participants with normal cognition (PD-NC, n = 39) and those with MCI (PD-MCI, n = 45).
Our study suggests a link between these special sensory dysfunctions and cognitive decline in early-stage PD, as evidenced by the correlation between MoCA scores and olfactory and gustatory functions. However, no significant differences in sensory function were found between the PD-NC and PD-MCI groups. Variations in methodology, participant characteristics, and MCI criteria may account for these disparities [4,5].
Shared anatomical networks and neuropathological processes may underlie the connection between cognition and these sensory dysfunctions. The processes of smell and taste can occur independently in the periphery but share central processing networks, including the frontal cortex (especially the orbitofrontal cortex) and insula, which are associated with cognitive function [6]. Previous studies on differences in brain structure based on the presence of cognitive dysfunction in PD patients have revealed structural differences, including in the frontal cortex and insula, which constitute the olfactory or gustatory pathway [7]. Otherwise, the connection between olfaction, gustation, and cognitive functioning in PD patients could be attributed to shared neuropathological processes and the influence of common neurotransmitters such as dopamine and acetylcholine.
While our multiple linear regression analysis did not find significant associations between olfactory and gustatory function tests and individual cognitive domains, a significant association was found with the MoCA score, likely because its comprehensive nature encompasses a wide range of cognitive domains. These findings suggest that hyposmia and hypogeusia in PD may be related to the cumulative degeneration of extensive neural networks rather than damage to specific brain regions.
Despite the study’s focus on early-stage PD, limitations such as a relatively small sample size and the exclusion of dementia patients may have impacted the results. Nevertheless, our study contributes to understanding the interplay of smell, taste, and cognition in early PD. Assessing smell and taste abilities in individuals with very early PD may offer insights into predicting cognitive issues, and longitudinal research is needed to further explore these findings and the underlying mechanisms.
Overall, this study enhances our understanding of the relationships among smell, taste, and cognition in early-stage PD. In a clinical context, it is possible that evaluating smell and taste abilities in individuals with very early PD could aid in predicting potential cognitive issues.
The online-only Data Supplement is available with this article at https://doi.org/10.14802/jmd.23243.
SUPPLEMENTARY MATERIAL
jmd-23243-Supplementary-Material.pdf
Supplementary Table 1.
Clinical characteristics of all participants with PD
jmd-23243-Supplementary-Table-1.pdf
Supplementary Figure 1.
Scatter plot and regression line between MoCA and sensory function. MoCA, Montreal Cognitive Assessment.
jmd-23243-Supplementary-Fig-1.pdf

Ethics Statement

This retrospective study was conducted in accordance with the ethical principles of the Declaration of Helsinki. The study protocol was approved by the Institutional Review Board of Hallym University Medical Center (IRB 2023-05-018). Due to the retrospective nature of the study, individual informed consent from participants was not required.

Conflicts of Interest

The authors have no financial conflicts of interest.

Funding Statement

This research was supported by a grant of the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI), funded by the Ministry of Health & Welfare, Republic of Korea (grant number: RS-2023-00265159), Basic Science Research Program through the National Research Foundation of Korea (NRF) grant funded by the Ministry of Education (RS-2023-00246655), the National Research Foundation of Korea(NRF) by the Korea government (MSIT) (2022R1A2C2091254), and [Bio&Medical Technology Development Program] of the National Research Foundation (NRF) funded by the Korean government (MSIT) (No. RS-2023-00223501).

Author Contributions

Conceptualization: Young Eun Kim, Hyeo-il Ma. Data curation: Jeongjae Lee, In Hee Kwak, Suk Yun Kang, Min Seung Kim, Jaeseol Park. Formal analysis: Jeongjae Lee. Funding acquisition: Young Eun Kim. Investigation: Jeongjae Lee, Joong Seob Lee, Young Eun Kim, Hyeo-il Ma, Jaeseol Park. Methodology: Jeongjae Lee, Jung Yeon Nam, Min Seung Kim. Project administration: Young Eun Kim, Hyeo-il Ma, Suk Yun Kang, Min Seung Kim. Resources: Young Eun Kim, Hyeo-il Ma, Min Seung Kim, Suk Yun Kang. Supervision: Young Eun Kim, Hyeo-il Ma. Writing—original draft: Jeongjae Lee, In Hee Kwak. Writing—review & editing: Young Eun Kim, Hyeo-il Ma, Suk Yun Kang, Min Seung Kim.

None
Table 1.
Multiple linear regression analysis for factors predicting cognition in PD patients
Dependent variables Independent variables R2 Beta p value
MoCA Age 0.492 -0.186 <0.001
Sex, female -2.603 <0.001
YOF test, discrimination 0.313 0.015
YGF test, total -0.214 0.021
Attention - - - -
Language - - - -
Visuospatial - - - -
Memory Age 0.070 0.053 0.024
Executive - - - -

The data for each cognitive domain used as dependent variables were calculated by converting the sum of the scores for each domain from the cognitive tests into z scores on the basis of the patient’s age and education level. Covariates included age, sex, education, disease duration, H&Y stage, MDS-UPDRS part III, GDS, olfactory threshold, discrimination, identification of YOF test, and total YGF test score.

PD, Parkinson’s disease; MoCA, Montreal Cognitive Assessment; YOF, YSK olfactory function; YGF, YSK gustatory function; H&Y, Hoehn and Yahr; MDS-UPDRS, Movement Disorder Society-Sponsored Revision of the Unified Parkinson’s Disease Rating Scale; GDS, Geriatric Depression Scale.

  • 1. Casjens S, Eckert A, Woitalla D, Ellrichmann G, Turewicz M, Stephan C, et al. Diagnostic value of the impairment of olfaction in Parkinson’s disease. PLoS One 2013;8:e64735.ArticlePubMedPMC
  • 2. Jagota P, Chotechuang N, Anan C, Kitjawijit T, Boonla C, Bhidayasiri R. Umami and other taste perceptions in patients with Parkinson’s disease. J Mov Disord 2022;15:115–123.ArticlePubMedPMCPDF
  • 3. Domellöf ME, Lundin KF, Edström M, Forsgren L. Olfactory dysfunction and dementia in newly diagnosed patients with Parkinson’s disease. Parkinsonism Relat Disord 2017;38:41–47.ArticlePubMed
  • 4. Park JW, Kwon DY, Choi JH, Park MH, Yoon HK. Olfactory dysfunctions in drug-naïve Parkinson’s disease with mild cognitive impairment. Parkinsonism Relat Disord 2018;46:69–73.ArticlePubMed
  • 5. Cecchini MP, Federico A, Zanini A, Mantovani E, Masala C, Tinazzi M, et al. Olfaction and taste in Parkinson’s disease: the association with mild cognitive impairment and the single cognitive domain dysfunction. J Neural Transm (Vienna) 2019;126:585–595.ArticlePubMedPDF
  • 6. de Araujo IE, Rolls ET, Kringelbach ML, McGlone F, Phillips N. Tasteolfactory convergence, and the representation of the pleasantness of flavour, in the human brain. Eur J Neurosci 2003;18:2059–2068.ArticlePubMed
  • 7. Mihaescu AS, Masellis M, Graff-Guerrero A, Kim J, Criaud M, Cho SS, et al. Brain degeneration in Parkinson’s disease patients with cognitive decline: a coordinate-based meta-analysis. Brain Imaging Behav 2019;13:1021–1034.ArticlePubMedPDF

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      Olfactory and Gustatory Function in Early-Stage Parkinson’s Disease: Implications for Cognitive Association
      Olfactory and Gustatory Function in Early-Stage Parkinson’s Disease: Implications for Cognitive Association
      Dependent variables Independent variables R2 Beta p value
      MoCA Age 0.492 -0.186 <0.001
      Sex, female -2.603 <0.001
      YOF test, discrimination 0.313 0.015
      YGF test, total -0.214 0.021
      Attention - - - -
      Language - - - -
      Visuospatial - - - -
      Memory Age 0.070 0.053 0.024
      Executive - - - -
      Table 1. Multiple linear regression analysis for factors predicting cognition in PD patients

      The data for each cognitive domain used as dependent variables were calculated by converting the sum of the scores for each domain from the cognitive tests into z scores on the basis of the patient’s age and education level. Covariates included age, sex, education, disease duration, H&Y stage, MDS-UPDRS part III, GDS, olfactory threshold, discrimination, identification of YOF test, and total YGF test score.

      PD, Parkinson’s disease; MoCA, Montreal Cognitive Assessment; YOF, YSK olfactory function; YGF, YSK gustatory function; H&Y, Hoehn and Yahr; MDS-UPDRS, Movement Disorder Society-Sponsored Revision of the Unified Parkinson’s Disease Rating Scale; GDS, Geriatric Depression Scale.


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