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Yang Hyun Lee 2 Articles
Association between Olfactory Deficit and Motor and Cognitive Function in Parkinson’s Disease
Han Soo Yoo, Seok Jong Chung, Yang Hyun Lee, Byoung Seok Ye, Young H. Sohn, Phil Hyu Lee
J Mov Disord. 2020;13(2):133-141.   Published online April 6, 2020
  • 10,356 View
  • 282 Download
  • 22 Web of Science
  • 21 Crossref
AbstractAbstract PDFSupplementary Material
To investigate whether baseline olfactory dysfunction in Parkinson’s disease (PD) patients is associated with baseline and longitudinal motor and cognitive function.
We recruited 228 drug-naïve PD patients who were followed for a mean of 6 years. Patients underwent the Cross-Cultural Smell Identification Test (CCSIT), a neuropsychological test, and N-(3-[18F]fluoropropyl)-2β-carbomethoxy-3β-(4-iodophenyl) nortropane positron emission tomography within 6 months of the baseline evaluation. Olfactory dysfunction was categorized as normosmia (CCSIT score ≥ 9), hyposmia (CCSIT score 5–8), and anosmia (CCSIT score ≤ 4). During the follow-up period, we investigated changes in the levodopa-equivalent dose (LED) and the occurrence of wearing-off, levodopa-induced dyskinesia, and dementia.
Among the PD patients, 80.7% were hyposmic at the time of diagnosis, and 26.1% were anosmic. Baseline olfactory dysfunction was not associated with either initial parkinsonian motor symptoms or with the longitudinal LED increment and motor complications. Meanwhile, the anosmic group had lower baseline scores on the Korea version of the Boston Naming Test and Stroop color reading test than the normosmic and hyposmic groups. The anosmic group exhibited a higher rate of conversion to dementia than the normosmic [adjusted hazard ratio (HR) 3.99, 95% confidence interval (CI) 1.08–14.72] and hyposmic (adjusted HR 2.48, 95% CI 1.15–5.32) PD groups, regardless of baseline motor deficits and cognitive status.
Baseline olfactory dysfunction was not associated with motor deficits and complications, but it was associated with cognitive dysfunction and prognosis, suggesting that severe olfactory impairment may reflect early cortical involvement, probably in the frontotemporal region, and rapid spreading of Lewy body pathology.


Citations to this article as recorded by  
  • Correlation of olfactory function factors with cardiac sympathetic denervation in Parkinson’s disease
    Dong-Woo Ryu, Sang-Won Yoo, Ko-Eun Choi, Yoon-Sang Oh, Joong-Seok Kim
    Journal of Neurology.2024; 271(3): 1397.     CrossRef
  • Estimating motor progression trajectory pursuant to temporal dynamic status of cardiac denervation in Parkinson’s disease
    Sang-Won Yoo, Dong-Woo Ryu, Yoon-Sang Oh, Seunggyun Ha, Chul Hyoung Lyoo, Yuna Kim, Ji-Yeon Yoo, Joong-Seok Kim
    Journal of Neurology.2024; 271(4): 2019.     CrossRef
  • Olfactory Dysfunction in Parkinson’s Disease, Its Functional and Neuroanatomical Correlates
    Gabriel Torres-Pasillas, Donají Chi-Castañeda, Porfirio Carrillo-Castilla, Gerardo Marín, María Elena Hernández-Aguilar, Gonzalo Emiliano Aranda-Abreu, Jorge Manzo, Luis I. García
    NeuroSci.2023; 4(2): 134.     CrossRef
  • Impact of deep brain stimulation (DBS) on olfaction in Parkinson's disease: Clinical features and functional hypotheses
    G. Brand, C. Bontempi, L. Jacquot
    Revue Neurologique.2023; 179(9): 947.     CrossRef
  • Sequential change in olfaction and (non) motor symptoms: the difference between anosmia and non-anosmia in Parkinson’s disease
    Ting-Chun Fang, Yu-Shan Tsai, Ming-Hong Chang
    Frontiers in Aging Neuroscience.2023;[Epub]     CrossRef
  • Traumatic brain injury-induced inflammatory changes in the olfactory bulb disrupt neuronal networks leading to olfactory dysfunction
    Xiang Liu, Zhuofan Lei, Dylan Gilhooly, Junyun He, Yun Li, Rodney M. Ritzel, Hui Li, Long-Jun Wu, Shaolin Liu, Junfang Wu
    Brain, Behavior, and Immunity.2023; 114: 22.     CrossRef
  • Serum Biomarkers of Olfactory Identification Deficits in Patients with Parkinson’s Disease
    Fu-Jia Li, Yang-Dan-Yu Li, Xu Liu, Jie Zu, Wei Zhang, Qi-Hua Xiao, Xue-Bin Niu, Li Du, Chen-Chen Cui, Ru-Yu Zhang, Xiao-Qing He, Gui-Yun Cui, Chuan-Ying Xu, Dominic B. Fee
    Acta Neurologica Scandinavica.2023; 2023: 1.     CrossRef
  • UPSIT subitems may predict motor progression in Parkinson’s disease
    Yu-Hsuan Lin, Ting-Chun Fang, Hsin-Bei Lei, Shih-Chi Chiu, Ming-Hong Chang, Yi-Jen Guo
    Frontiers in Neurology.2023;[Epub]     CrossRef
  • Olfactory dysfunction is associated with motor function only in tremor-dominant Parkinson’s disease
    Fardin Nabizadeh, Kasra Pirahesh, Elham Khalili
    Neurological Sciences.2022; 43(7): 4193.     CrossRef
  • Novel diagnostic tools for identifying cognitive impairment using olfactory-stimulated functional near-infrared spectroscopy: patient-level, single-group, diagnostic trial
    Jaewon Kim, Dong Keon Yon, Kyu Yeong Choi, Jang Jae Lee, Namwoo Kim, Kun Ho Lee, Jae Gwan Kim
    Alzheimer's Research & Therapy.2022;[Epub]     CrossRef
  • The Role of Olfactory System in the Etiogenesis of Parkinson’s Diseases: An Overview
    Jiju Narayanan Avanipully, Dithu Thekkekkara, Sahyadri M, Vipan K. Parihar, Santhepete Nanjundaiah Manjula
    Journal of Pharmacology and Pharmacotherapeutics.2022; 13(1): 31.     CrossRef
  • International consensus statement on allergy and rhinology: Olfaction
    Zara M. Patel, Eric H. Holbrook, Justin H. Turner, Nithin D. Adappa, Mark W. Albers, Aytug Altundag, Simone Appenzeller, Richard M. Costanzo, Ilona Croy, Greg E. Davis, Puya Dehgani‐Mobaraki, Richard L. Doty, Valerie B. Duffy, Bradley J. Goldstein, David
    International Forum of Allergy & Rhinology.2022; 12(4): 327.     CrossRef
  • Does Olfactory Dysfunction Correlate with Disease Progression in Parkinson’s Disease? A Systematic Review of the Current Literature
    Tommaso Ercoli, Carla Masala, Gianluca Cadeddu, Marcello Mario Mascia, Gianni Orofino, Angelo Fabio Gigante, Paolo Solla, Giovanni Defazio, Lorenzo Rocchi
    Brain Sciences.2022; 12(5): 513.     CrossRef
  • Olfactory dysfunction and striatal dopamine transporter binding in motor subtypes of Parkinson’s disease
    Fardin Nabizadeh, Fatemeh Sodeifian, Kasra Pirahesh
    Neurological Sciences.2022; 43(8): 4745.     CrossRef
  • Olfaction and Executive Cognitive Performance: A Systematic Review
    Vasudeva Murthy Challakere Ramaswamy, Peter William Schofield
    Frontiers in Psychology.2022;[Epub]     CrossRef
  • Nasal and Parotid Blood Pool Activity Is Significantly Correlated with Metabolic Syndrome Components and Sleep Apnea
    William T. Phillips, Nasser J. Issa, Shereef B. Elhalwagi, Hilda T. Draeger, Joyce G. Schwartz, Jonathan A. Gelfond
    Metabolic Syndrome and Related Disorders.2022; 20(7): 395.     CrossRef
  • Chronic neuropsychiatric sequelae of SARS‐CoV‐2: Protocol and methods from the Alzheimer's Association Global Consortium
    Gabriel A. de Erausquin, Heather Snyder, Traolach S. Brugha, Sudha Seshadri, Maria Carrillo, Rajesh Sagar, Yueqin Huang, Charles Newton, Carmela Tartaglia, Charlotte Teunissen, Krister Håkanson, Rufus Akinyemi, Kameshwar Prasad, Giovanni D'Avossa, Gabriel
    Alzheimer's & Dementia: Translational Research & Clinical Interventions.2022;[Epub]     CrossRef
  • Machine learning-based prediction of cognitive outcomes in de novo Parkinson’s disease
    Joshua Harvey, Rick A. Reijnders, Rachel Cavill, Annelien Duits, Sebastian Köhler, Lars Eijssen, Bart P. F. Rutten, Gemma Shireby, Ali Torkamani, Byron Creese, Albert F. G. Leentjens, Katie Lunnon, Ehsan Pishva
    npj Parkinson's Disease.2022;[Epub]     CrossRef
  • Impact of Subthalamic Deep Brain Stimulation on Hyposmia in Patients With Parkinson's Disease Is Influenced by Constipation and Dysbiosis of Microbiota
    Chao Li, Ying Hou, Xu Wang, Yue-xuan Li, Feng Li, Chao Zhang, Wei-guo Li
    Frontiers in Neurology.2021;[Epub]     CrossRef
  • Hyposmia may predict development of freezing of gait in Parkinson’s disease
    Jae Jung Lee, Jin Yong Hong, Jong Sam Baik
    Journal of Neural Transmission.2021; 128(6): 763.     CrossRef
  • Clinical and Dopamine Depletion Patterns in Hyposmia- and Dysautonomia-Dominant Parkinson’s Disease
    Han Soo Yoo, Sangwon Lee, Seong Ho Jeong, Byoung Seok Ye, Young H. Sohn, Mijin Yun, Phil Hyu Lee
    Journal of Parkinson's Disease.2021; 11(4): 1703.     CrossRef
Heterogeneous Patterns of Striatal Dopamine Loss in Patients with Young- versus Old-Onset Parkinson’s Disease: Impact on Clinical Features
Seok Jong Chung, Han Soo Yoo, Yang Hyun Lee, Phil Hyu Lee, Young H. Sohn
J Mov Disord. 2019;12(2):113-119.   Published online May 30, 2019
  • 7,801 View
  • 159 Download
  • 26 Web of Science
  • 27 Crossref
AbstractAbstract PDFSupplementary Material
Ample evidence has suggested that age at onset of Parkinson’s disease (PD) is associated with heterogeneous clinical features in individuals. We hypothesized that this may be attributed to different patterns of nigrostriatal dopamine loss.
A total of 205 consecutive patients with de novo PD who underwent 18F-FP-CIT PET scans (mean follow-up duration, 6.31 years) were divided into three tertile groups according to their age at onset of parkinsonian motor symptoms. Striatal dopamine transporter (DAT) availability was compared between the old- (n = 73) and young-onset (n = 66) groups. In addition, the risk of developing freezing of gait (FOG) and longitudinal requirements for dopaminergic medications were examined.
The old-onset PD group (mean age at onset, 72.66 years) exhibited more severe parkinsonian motor signs than the young-onset group (52.58 years), despite comparable DAT availability in the posterior putamen; moreover, the old-onset group exhibited more severely decreased DAT availability in the caudate than the young-onset group. A Cox regression model revealed that the old-onset PD group had a higher risk for developing FOG than the young-onset group [hazard ratio 2.523, 95% confidence interval (1.239–5.140)]. The old-onset group required higher doses of dopaminergic medications for symptom control than the young-onset group over time.
The present study demonstrated that the old-onset PD group exhibited more severe dopamine loss in the caudate and were more likely to develop gait freezing, suggesting that age at onset may be one of the major determinants of the pattern of striatal dopamine depletion and progression of gait disturbance in PD.


Citations to this article as recorded by  
  • The Molecular Pathway of p75 Neurotrophin Receptor (p75NTR) in Parkinson’s Disease: The Way of New Inroads
    Naif H. Ali, Hayder M. Al-kuraishy, Ali I. Al-Gareeb, Saud A. Alnaaim, Hebatallah M. Saad, Gaber El-Saber Batiha
    Molecular Neurobiology.2024; 61(5): 2469.     CrossRef
  • Patterns of regional cerebral hypoperfusion in early Parkinson's disease: Clinical implications
    Seok Jong Chung, Su Hong Kim, Chan Wook Park, Hye Sun Lee, Mijin Yun, Yun Joong Kim, Young H. Sohn, Yong Jeong, Phil Hyu Lee
    Parkinsonism & Related Disorders.2024; 121: 106024.     CrossRef
  • Therapeutic Potential Effect of Glycogen Synthase Kinase 3 Beta (GSK-3β) Inhibitors in Parkinson Disease: Exploring an Overlooked Avenue
    Areej Turkistani, Hayder M. Al-kuraishy, Ali I. Al-Gareeb, Ali K. Albuhadily, Athanasios Alexiou, Marios Papadakis, Mohamed M. Elfiky, Hebatallah M. Saad, Gaber El-Saber Batiha
    Molecular Neurobiology.2024;[Epub]     CrossRef
  • Imaging Procedure and Clinical Studies of [18F]FP-CIT PET
    Changhwan Sung, Seung Jun Oh, Jae Seung Kim
    Nuclear Medicine and Molecular Imaging.2024;[Epub]     CrossRef
  • Association of Family History and Polygenic Risk Score With Longitudinal Prognosis in Parkinson Disease
    Mincheol Park, Young-gun Lee
    Neurology Genetics.2024;[Epub]     CrossRef
  • Hippocampal Perfusion Affects Motor and Cognitive Functions in Parkinson Disease: An Early Phase 18F‐FP‐CIT Positron Emission Tomography Study
    Min Young Chun, Seok Jong Chung, Su Hong Kim, Chan Wook Park, Seong Ho Jeong, Hye Sun Lee, Phil Hyu Lee, Young H. Sohn, Yong Jeong, Yun Joong Kim
    Annals of Neurology.2024; 95(2): 388.     CrossRef
  • The effects of cholesterol and statins on Parkinson’s neuropathology: a narrative review
    Hayder M. Al-kuraishy, Esraa H. Fahad, Salah Al-Windy, Suzy A. El-Sherbeni, Walaa A. Negm, Gaber El-Saber Batiha
    Inflammopharmacology.2024; 32(2): 917.     CrossRef
  • BDNF/TrkB activators in Parkinson's disease: A new therapeutic strategy
    Naif H. Ali, Hayder M. Al‐Kuraishy, Ali I. Al‐Gareeb, Athanasios Alexiou, Marios Papadakis, Ali Abdullah AlAseeri, Mubarak Alruwaili, Hebatallah M. Saad, Gaber El‐Saber Batiha
    Journal of Cellular and Molecular Medicine.2024;[Epub]     CrossRef
  • The Concept of Motor Reserve in Parkinson's Disease: New Wine in Old Bottles?
    Merle C. Hoenig, Verena Dzialas, Alexander Drzezga, Thilo van Eimeren
    Movement Disorders.2023; 38(1): 16.     CrossRef
  • Memory Phenotypes In Early, De Novo Parkinson's Disease Patients with Mild Cognitive Impairment
    Mattia Siciliano, Rosa De Micco, Andrea Gerardo Russo, Fabrizio Esposito, Valeria Sant'Elia, Lucia Ricciardi, Francesca Morgante, Antonio Russo, Jennifer G. Goldman, Carlo Chiorri, Gioacchino Tedeschi, Luigi Trojano, Alessandro Tessitore
    Movement Disorders.2023; 38(8): 1461.     CrossRef
  • A meta-analysis identifies factors predicting the future development of freezing of gait in Parkinson’s disease
    Talia Herman, Yael Barer, Michal Bitan, Shani Sobol, Nir Giladi, Jeffrey M. Hausdorff
    npj Parkinson's Disease.2023;[Epub]     CrossRef
  • Premorbid Educational Attainment and Long-Term Motor Prognosis in Parkinson’s Disease
    Seong Ho Jeong, Seok Jong Chung, Han Soo Yoo, Jin Ho Jung, Kyoungwon Baik, Yang Hyun Lee, Phil Hyu Lee, Young H. Sohn
    Journal of Parkinson's Disease.2022; 12(1): 129.     CrossRef
  • Treatment Enhances Betweenness Centrality of Fronto-Parietal Network in Parkinson’s Patients
    Qing Liu, ZhongYan Shi, Kexin Wang, Tiantian Liu, Shintaro Funahashi, Jinglong Wu, Jian Zhang
    Frontiers in Computational Neuroscience.2022;[Epub]     CrossRef
  • Identifying the white matter structural network of motor reserve in early Parkinson's disease
    Yae Ji Kim, Chan Wook Park, Hye Won Shin, Hye Sun Lee, Yun Joong Kim, Mijin Yun, Phil Hyu Lee, Young H. Sohn, Yong Jeong, Seok Jong Chung
    Parkinsonism & Related Disorders.2022; 102: 108.     CrossRef
  • Potential Link Between Cognition and Motor Reserve in Patients With Parkinson’s Disease
    Seok Jong Chung, Yae Ji Kim, Yun Joong Kim, Hye Sun Lee, Mijin Yun, Phil Hyu Lee, Yong Jeong, Young H. Sohn
    Journal of Movement Disorders.2022; 15(3): 249.     CrossRef
  • Association Between White Matter Networks and the Pattern of Striatal Dopamine Depletion in Patients With Parkinson Disease
    Seok Jong Chung, Yae Ji Kim, Yun Joong Kim, Hye Sun Lee, Seong Ho Jeong, Ji-Man Hong, Young H. Sohn, Mijin Yun, Yong Jeong, Phil Hyu Lee
    Neurology.2022;[Epub]     CrossRef
  • Gut microbiota-derived metabolite trimethylamine N-oxide as a biomarker in early Parkinson's disease
    Seok Jong Chung, John Hoon Rim, Dajeong Ji, Sangwon Lee, Han Soo Yoo, Jin Ho Jung, KyoungWon Baik, Yonghoon Choi, Byoung Seok Ye, Young H. Sohn, Mijin Yun, Sang-Guk Lee, Phil Hyu Lee
    Nutrition.2021; 83: 111090.     CrossRef
  • White Matter Hyperintensities, Dopamine Loss, and Motor Deficits in De Novo Parkinson's Disease
    Seong Ho Jeong, Hye Sun Lee, Jin Ho Jung, Kyoungwon Baik, Yang Hyun Lee, Han Soo Yoo, Young H. Sohn, Seok Jong Chung, Phil Hyu Lee
    Movement Disorders.2021; 36(6): 1411.     CrossRef
  • Temporalis Muscle Thickness as an Indicator of Sarcopenia Is Associated With Long-term Motor Outcomes in Parkinson’s Disease
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    The Journals of Gerontology: Series A.2021; 76(12): 2242.     CrossRef
  • Perivascular Spaces in the Basal Ganglia and Long-term Motor Prognosis in Newly Diagnosed Parkinson Disease
    Seok Jong Chung, Han Soo Yoo, Na-Young Shin, Yae Won Park, Hye Sun Lee, Ji-Man Hong, Yun Joong Kim, Seung-Koo Lee, Phil Hyu Lee, Young H. Sohn
    Neurology.2021;[Epub]     CrossRef
  • Diagnosis and treatment of old-onset Parkinson's disease
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    npj Parkinson's Disease.2021;[Epub]     CrossRef
  • Dopamine Transporter, Age, and Motor Complications in Parkinson's Disease: A Clinical and Single‐Photon Emission Computed Tomography Study
    Giovanni Palermo, Sara Giannoni, Daniela Frosini, Riccardo Morganti, Duccio Volterrani, Ubaldo Bonuccelli, Nicola Pavese, Roberto Ceravolo
    Movement Disorders.2020; 35(6): 1028.     CrossRef
  • Positron emission tomography/computed tomography dual imaging using 18-fluorine flurodeoxyglucose and 11C-labeled 2-β-carbomethoxy-3-β-(4-fluorophenyl) tropane for the severity assessment of Parkinson disease
    Xiaohong Li, Qizhou Zhang, Yongde Qin, Yubin Li, Nazimuguli Mutaerbieke, Xiaojia Zhao, Amina Yibulayin
    Medicine.2020; 99(14): e19662.     CrossRef
  • DaTSCAN (123I-FP-CIT SPECT) imaging in early versus mid and late onset Parkinson's disease: Longitudinal data from the PPMI study
    Christos Koros, Athina-Maria Simitsi, Andreas Prentakis, Nikolaos Papagiannakis, Anastasia Bougea, Ioanna Pachi, Dimitra Papadimitriou, Ion Beratis, Sokratis G. Papageorgiou, Maria Stamelou, Xenia Geronicola Trapali, Leonidas Stefanis
    Parkinsonism & Related Disorders.2020; 77: 36.     CrossRef
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