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Umami and Other Taste Perceptions in Patients With Parkinson’s Disease
Priya Jagota, Nattida Chotechuang, Chanawat Anan, Teeraparp Kitjawijit, Chanchai Boonla, Roongroj Bhidayasiri
J Mov Disord. 2022;15(2):115-123.   Published online March 22, 2022
DOI: https://doi.org/10.14802/jmd.21058
  • 5,476 View
  • 228 Download
  • 4 Web of Science
  • 4 Crossref
AbstractAbstract PDF
Objective
Studies of taste perceptions in Parkinson’s disease (PD) patients have been controversial, and none of these studies have assessed umami taste. This study aimed to assess umami, along with the other 4 taste functions in PD patients.
Methods
Participants were tested for gustation using the modified filter paper disc method and olfaction using the modified Sniffin’ Stick-16 (mSS-16) test (only 14 culturally suitable items were used). A questionnaire evaluated patients’ subjective olfactory and gustatory dysfunction, taste preference, appetite, and food habits.
Results
A total of 105 PD patients and 101 age- and sex-matched controls were included. The body mass index (BMI) of PD patients was lower than that of controls (PD = 22.62, controls = 23.86, p = 0.028). The mSS-16 score was 10.7 for controls and 6.4 for PD patients (p < 0.001) (normal ≥ 9). Taste recognition thresholds (RTs) for sweet, salty, sour, bitter and umami tastes were significantly higher in PD, indicating poorer gustation. All taste RTs correlated with each other, except for umami. Most patients were unaware of their dysfunction. Patients preferred sweet, salty and umami tastes more than the controls. Dysgeusia of different tastes in patients was differentially associated with poorer discrimination of tastes, an inability to identify the dish and adding extra seasoning to food. BMI and mSS-16 scores showed no correlation in either patients or controls.
Conclusion
PD patients have dysgeusia for all five tastes, including umami, which affects their appetite and diet. Patients preferred sweet, salty and umami tastes. This information can help adjust patients’ diets to improve their nutritional status.

Citations

Citations to this article as recorded by  
  • The missing piece of the puzzle – The key role of the dietitian in the management of Parkinson's disease
    Richelle Flanagan, Carley Rusch, Fiona E. Lithander, Indu Subramanian
    Parkinsonism & Related Disorders.2024; 121: 106021.     CrossRef
  • Body mass index in patients with Parkinson’s disease: a systematic review
    Yinghui Li, Yumei Liu, Chuanning Du, Jun Wang
    Journal of Neurophysiology.2024; 131(2): 311.     CrossRef
  • Apnea behavior in early- and late-stage mouse models of Parkinson's disease: Cineradiographic analysis of spontaneous breathing, acute stress, and swallowing
    Lorena Roberta de Souza Mendes Kawamura, Max Sarmet, Priscila Sales de Campos, Sachiko Takehara, Yasuhiro Kumei, Jorge Luis Lopes Zeredo
    Respiratory Physiology & Neurobiology.2024; 323: 104239.     CrossRef
  • Gustatory dysfunction is related to Parkinson's disease: A systematic review and meta‐analysis
    Il‐Youp Kwak, Kyung Soo Kim, Hyun Jin Min
    International Forum of Allergy & Rhinology.2023; 13(10): 1949.     CrossRef
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
DOI: https://doi.org/10.14802/jmd.19082
  • 10,359 View
  • 282 Download
  • 22 Web of Science
  • 21 Crossref
AbstractAbstract PDFSupplementary Material
Objective
To investigate whether baseline olfactory dysfunction in Parkinson’s disease (PD) patients is associated with baseline and longitudinal motor and cognitive function.
Methods
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.
Results
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.
Conclusion
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

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
Nonmotor and Dopamine Transporter Change in REM Sleep Behavior Disorder by Olfactory Impairment
Jee-Young Lee, Eun Jin Yoon, Yu Kyeong Kim, Chae Won Shin, Hyunwoo Nam, Jae Min Jeong, Han-Joon Kim, Beomseok Jeon
J Mov Disord. 2019;12(2):103-112.   Published online May 30, 2019
DOI: https://doi.org/10.14802/jmd.18061
  • 7,450 View
  • 207 Download
  • 18 Web of Science
  • 17 Crossref
AbstractAbstract PDFSupplementary Material
Objective
It is unclear whether the decline in dopamine transporters (DAT) differs among idiopathic rapid eye movement sleep behavior disorder (iRBD) patients with different levels of olfactory impairment. This study aimed to characterize DAT changes in relation to nonmotor features in iRBD patients by olfactory loss.
Methods
This prospective cohort study consisted of three age-matched groups: 30 polysomnography-confirmed iRBD patients, 30 drug-naïve Parkinson’s disease patients, and 19 healthy controls without olfactory impairment. The iRBD group was divided into two groups based on olfactory testing results. Participants were evaluated for reported prodromal markers and then underwent 18F-FP-CIT positron emission tomography and 3T MRI. Tracer uptakes were analyzed in the caudate, anterior and posterior putamen, substantia nigra, and raphe nuclei.
Results
Olfactory impairment was defined in 38.5% of iRBD patients. Mild parkinsonian signs and cognitive functions were not different between the two iRBD subgroups; however, additional prodromal features, constipation, and urinary and sexual dysfunctions were found in iRBD patients with olfactory impairment but not in those without. Tracer uptake showed significant group differences in all brain regions, except the raphe nuclei. The iRBD patients with olfactory impairment had uptake reductions in the anterior and posterior putamen, caudate, and substantia nigra (p < 0.016 in all, adjusted for age), which ranged from 0.6 to 0.8 of age-normative values. In contrast, those without olfactory impairment had insignificant changes in all regions ranging above 0.8.
Conclusion
There was a clear distinction in DAT loss and nonmotor profiles by olfactory status in iRBD.

Citations

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  • Neuropsychological Changes in Isolated REM Sleep Behavior Disorder: A Systematic Review and Meta-analysis of Cross-sectional and Longitudinal Studies
    Caterina Leitner, Giada D’Este, Laura Verga, Shady Rahayel, Samantha Mombelli, Marco Sforza, Francesca Casoni, Marco Zucconi, Luigi Ferini-Strambi, Andrea Galbiati
    Neuropsychology Review.2024; 34(1): 41.     CrossRef
  • Dopamine transporter positron emission tomography in patients with Alzheimer’s disease with Lewy body disease features
    Sungwoo Kang, Seun Jeon, Young-gun Lee, Byoung Seok Ye
    Neurobiology of Aging.2024; 134: 57.     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
  • Validation of the REM behaviour disorder phenoconversion-related pattern in an independent cohort
    Beatrice Orso, Pietro Mattioli, Eun-Jin Yoon, Yu Kyeong Kim, Heejung Kim, Jung Hwan Shin, Ryul Kim, Claudio Liguori, Francesco Famà, Andrea Donniaquio, Federico Massa, David Vállez García, Sanne K. Meles, Klaus L. Leenders, Agostino Chiaravalloti, Matteo
    Neurological Sciences.2023; 44(9): 3161.     CrossRef
  • Neurofilament light chain and cardiac MIBG uptake as predictors for phenoconversion in isolated REM sleep behavior disorder
    Don Gueu Park, Ju Yeong Kim, Min Seung Kim, Mi Hee Kim, Young-Sil An, Jaerak Chang, Jung Han Yoon
    Journal of Neurology.2023; 270(9): 4393.     CrossRef
  • Longitudinal evolution of cortical thickness signature reflecting Lewy body dementia in isolated REM sleep behavior disorder: a prospective cohort study
    Jung Hwan Shin, Heejung Kim, Yu Kyeong Kim, Eun Jin Yoon, Hyunwoo Nam, Beomseok Jeon, Jee-Young Lee
    Translational Neurodegeneration.2023;[Epub]     CrossRef
  • Brain olfactory‐related atrophy in isolated rapid eye movement sleep behavior disorder
    Kyung Ah Woo, Heejung Kim, Eun Jin Yoon, Jung Hwan Shin, Hyunwoo Nam, Beomseok Jeon, Yu Kyeong Kim, Jee‐Young Lee
    Annals of Clinical and Translational Neurology.2023; 10(12): 2192.     CrossRef
  • Monoaminergic Degeneration and Ocular Motor Abnormalities in De Novo Parkinson's Disease
    Kyung Ah Woo, Joo Hong Joun, Eun Jin Yoon, Chan Young Lee, Beomseok Jeon, Yu Kyeong Kim, Jee‐Young Lee
    Movement Disorders.2023; 38(12): 2291.     CrossRef
  • Altered cerebral perfusion and microstructure in advanced Parkinson’s disease and their associations with clinical features
    Zhaoxi Liu, Yiwei Zhang, Han Wang, Dan Xu, Hui You, Zhentao Zuo, Feng Feng
    Neurological Research.2022; 44(1): 47.     CrossRef
  • Brain Neuroimaging of Rapid Eye Movement Sleep Behavior Disorder in Parkinson’s Disease: A Systematic Review
    Rafail Matzaras, Kuangyu Shi, Artemios Artemiadis, Panagiotis Zis, Georgios Hadjigeorgiou, Axel Rominger, Claudio L.A. Bassetti, Panagiotis Bargiotas
    Journal of Parkinson's Disease.2022; 12(1): 69.     CrossRef
  • Odor Identification by Parkinson’s Disease Patients Tested by Using Sniffin’ Sticks versus Natural Spices
    Florence Baert, Geertrui Vlaemynck, Jarissa Maselyne, Christophe Matthys, Seyed-Mohammad Fereshtehnejad
    Parkinson's Disease.2022; 2022: 1.     CrossRef
  • Brain Metabolic Correlates of Dopaminergic Denervation in Prodromal and Early Parkinson's Disease
    Ryul Kim, Heejung Kim, Yu Kyeong Kim, Eun Jin Yoon, Hyun Woo Nam, Beomseok Jeon, Jee‐Young Lee
    Movement Disorders.2022; 37(10): 2099.     CrossRef
  • Longitudinal Changes in Isolated Rapid Eye Movement Sleep Behavior Disorder‐Related Metabolic Pattern Expression
    Ryul Kim, Jee‐Young Lee, Yu Kyeong Kim, Heejung Kim, Eun Jin Yoon, Jung Hwan Shin, Dallah Yoo, Hyunwoo Nam, Beomseok Jeon
    Movement Disorders.2021; 36(8): 1889.     CrossRef
  • Parkinson Disease-Related Brain Metabolic Patterns and Neurodegeneration in Isolated REM Sleep Behavior Disorder
    Jung Hwan Shin, Jee-Young Lee, Yu-Kyeong Kim, Eun Jin Yoon, Heejung Kim, Hyunwoo Nam, Beomseok Jeon
    Neurology.2021;[Epub]     CrossRef
  • Retina Thickness as a Marker of Neurodegeneration in Prodromal Lewy Body Disease
    Jee‐Young Lee, Jeeyun Ahn, Sohee Oh, Joo Young Shin, Yu Kyeong Kim, Hyunwoo Nam, Beomseok Jeon
    Movement Disorders.2020; 35(2): 349.     CrossRef
  • Serum TNF-α and neurodegeneration in isolated REM sleep behavior disorder
    Ryul Kim, Jee-Young Lee, Han-Joon Kim, Yu Kyeong Kim, Hyunwoo Nam, Beomseok Jeon
    Parkinsonism & Related Disorders.2020; 81: 1.     CrossRef
  • Longitudinal change in dopamine transporter availability in idiopathic REM sleep behavior disorder
    Jung Hwan Shin, Jee-Young Lee, Yu-Kyeong Kim, Sung-A Shin, Heejung Kim, Hyunwoo Nam, Beomseok Jeon
    Neurology.2020;[Epub]     CrossRef
Cognition, Olfaction and Uric Acid in Early de novo Parkinson’s Disease
Hwa Reung Lee, Joong Hyun Park, Sang Won Han, Jong Sam Baik
J Mov Disord. 2018;11(3):139-144.   Published online September 30, 2018
DOI: https://doi.org/10.14802/jmd.18037
  • 6,923 View
  • 151 Download
  • 7 Web of Science
  • 6 Crossref
AbstractAbstract PDF
Objective
Cognitive impairment is one of the nonmotor symptoms in Parkinson’s disease (PD), and olfactory dysfunction is used as a marker to detect premotor stages of PD. Serum uric acid (sUA) levels have been found to be a risk factor for PD. Our objective in this study was to examine whether sUA levels are associated with cognitive changes and olfactory dysfunction in early de novo PD patients.
Methods
The study participants included 196 de novo PD patients. We assessed cognitive function by the Korean versions of the Mini-Mental State Examination and the Montreal Cognitive Assessment and assessed olfactory function by the Korean version of the Sniffin’ Sticks test.
Results
The mean sUA level was 4.7 mg/dL and was significantly lower in women than in men. Cognitive scores were lower in women, suggesting that sUA levels were related to cognitive function. The olfactory functions were not related to sUA level but were clearly associated with cognitive scores. Olfactory threshold, odor discrimination, and odor identification were all significantly related to cognitive scores.
Conclusion
We conclude that lower sUA levels were associated with cognitive impairment, not olfactory dysfunction, in de novo PD patients. This finding suggests that UA is neuroprotective as an antioxidant in the cognitive function of PD patients.

Citations

Citations to this article as recorded by  
  • Serum uric acid and Parkinson's disease: A systematic review and meta‐analysis
    Mohammad Balabandian, Sarvenaz Salahi, Behnaz Mahmoudvand, Mahla Esmaeilzadeh, Seyedeh Melika Hashemi, Fardin Nabizadeh
    Neurology and Clinical Neuroscience.2023; 11(6): 299.     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
  • Association of serum uric acid and non-motor symptoms in Parkinson's disease: A cross-sectional study from a movement disorders clinic in Lagos, Nigeria
    OlanikeA Odeniyi, OluwadamilolaO Ojo, IfedayoAdeola Odeniyi, NjidekaUlunma Okubadejo
    Journal of Clinical Sciences.2022; 19(3): 104.     CrossRef
  • A postmortem study suggests a revision of the dual-hit hypothesis of Parkinson’s disease
    Per Borghammer, Mie Kristine Just, Jacob Horsager, Casper Skjærbæk, Anna Raunio, Eloise H. Kok, Sara Savola, Shigeo Murayama, Yuko Saito, Liisa Myllykangas, Nathalie Van Den Berge
    npj Parkinson's Disease.2022;[Epub]     CrossRef
  • What substance P might tell us about the prognosis and mechanism of Parkinson's disease?
    Paola Tirassa, Tommaso Schirinzi, Marcello Raspa, Massimo Ralli, Antonio Greco, Antonella Polimeni, Roberta Possenti, Nicola Biagio Mercuri, Cinzia Severini
    Neuroscience & Biobehavioral Reviews.2021; 131: 899.     CrossRef
  • Brain-First versus Gut-First Parkinson’s Disease: A Hypothesis
    Per Borghammer, Nathalie Van Den Berge, Teus van Laar
    Journal of Parkinson's Disease.2019; 9(s2): S281.     CrossRef

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