International multicenter pilot study of the first comprehensive self‐completed nonmotor symptoms questionnaire for Parkinson's disease: The NMSQuest study
Abstract
Nonmotor symptoms (NMS) of Parkinson's disease (PD) are not well recognized in clinical practice, either in primary or in secondary care, and are frequently missed during routine consultations. There is no single instrument (questionnaire or scale) that enables a comprehensive assessment of the range of NMS in PD both for the identification of problems and for the measurement of outcome. Against this background, a multidisciplinary group of experts, including patient group representatives, has developed an NMS screening questionnaire comprising 30 items. This instrument does not provide an overall score of disability and is not a graded or rating instrument. Instead, it is a screening tool designed to draw attention to the presence of NMS and initiate further investigation. In this article, we present the results from an international pilot study assessing feasibility, validity, and acceptability of a nonmotor questionnaire (NMSQuest). Data from 123 PD patients and 96 controls were analyzed. NMS were highly significantly more prevalent in PD compared to controls (PD NMS, median = 9.0, mean = 9.5 vs. control NMS, median = 5.5, mean = 4.0; Mann–Whitney, Kruskal–Wallis, and t test, P < 0.0001), with PD patients reporting at least 10 different NMS on average per patient. In PD, NMS were highly significantly more prevalent across all disease stages and the number of symptoms correlated significantly with advancing disease and duration of disease. Furthermore, frequently, problems such as diplopia, dribbling, apathy, blues, taste and smell problems were never previously disclosed to the health professionals. © 2006 Movement Disorder Society
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PD is strongly associated with REM sleep behaviour disorder, as well as excessive daytime sleepiness, insomnia and restless legs syndrome.
“PD, in particular, is strongly associated with rapid eye moment (reM) sleep behaviour disorder (RBD), as well as excessive daytime sleepiness, insomnia and restless legs syndrome270–273.”
From Rhythms of life: circadian disruption and brain disorders across the lifespan (2019) · cites this paper as [271]
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MethodWhy have we failed to achieve neuroprotection in Parkinson's disease?
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Self-citationConstipation in parkinson's disease: Subjective symptoms, objective markers, and new perspectives
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BackgroundNonmotor and diagnostic findings in subjects with de novo Parkinson disease of the DeNoPa cohort
Mollenhauer, B., Trautmann, E., Sixel‐Döring, F., Wicke, T., Ebentheuer, J., Schaumburg, M., Lang, E., Focke, N. K., Kumar, K. R., Lohmann, K., et al. (2013) · Neurology · doi:10.1212/wnl.0b013e3182a6cbd5 · Cited by 184 · see citing works
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“more than 6 months), (2) solid versus liquid dysphagia, (3) level with which the patients senses food or fluid “sticking” in their chest, (4) the frequency with which symptoms occur (constant (with every bite) vs.”
BackgroundGut Microbiota Differs Between Parkinson’s Disease Patients and Healthy Controls in Northeast China
Li, C., Cui, L., Yang, Y., Miao, J., Zhao, X., Zhang, J., Cui, G., & Zhang, Y. (2019) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2019.00171 · Cited by 178 · see citing works
Levodopa unresponsive symptoms in Parkinson disease
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Self-citationSupplementary motor area stimulation for Parkinson disease
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“Secondary end points were the UPDRS total score, Hamilton Rating Scale for Depression, apathy score, and nonmotor symptoms questionnaire.(19) The UPDRS part III score at time points other than the 9th and 20th weeks was also analyzed.”
MethodNon-motor outcomes depend on location of neurostimulation in Parkinson’s disease
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“…finally, non-motor disorders, cognitive disorders, sensory disturbances, anxiety and depression, which may precede Massicotte-Marquez, & Montplaisir, 2006), were evaluated et al., 2006). patients enrolled in NWg performed a 12-week exercise program, consisting of exercise sessions supervised by…”
The hidden sister of motor fluctuations in Parkinson's disease: A review on nonmotor fluctuations
Martínez‐Fernández, R., Schmitt, E., Martínez‐Martín, P., & Krack, P. (2016) · Movement Disorders · doi:10.1002/mds.26731 · Cited by 165 · see citing works
Impact of non-motor symptoms on health-related and perceived quality of life in Parkinson's disease
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“Two different instruments were used to assess QoL: 1) the 39-item Parkinson's disease Quality of Life Questionnaire Summary Index score (PDQ-39SI) [13], and 2) a subjective rating of perceived QoL (PQ-10) on a scale from 0 (worst) to 10 (best).”
BackgroundMethodResultInfluentialRotigotine and specific non-motor symptoms of Parkinson's disease: Post hoc analysis of RECOVER
Chaudhuri, К. R., Martínez‐Martín, P., Antonini, A., Brown, R. G., Friedman, J. H., ONOFRJ, M. C., Surmann, E., Ghys, L., & Trenkwalder, C. (2013) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2013.02.018 · Cited by 164 · see citing works
Self-citationThe challenge of non-motor symptoms in Parkinson’s disease
Chaudhuri, К. R., & Odin, P. (2010) · Progress in brain research · doi:10.1016/s0079-6123(10)84017-8 · Cited by 164 · see citing works
Self-citationThe importance of non-motor disturbances to quality of life in Parkinson's disease
Martinez-Martin, P. (2011) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2011.05.006 · Cited by 160 · see citing works
Mertsalmi, T. H., Aho, V. T. E., Pereira, P. A. B., Paulin, L., Pekkonen, E., Auvinen, P., & Scheperjans, F. (2017) · European Journal of Neurology · doi:10.1111/ene.13398 · Cited by 153 · see citing works
“Overall prevalence and severity of non-motor symptoms were assessed using the Non-Motor Symptoms Questionnaire (NMSQuest) [11] and Non-Motor Symptom Scale (NMSS) [12].”
MethodQuantitation of non‐motor symptoms in Parkinson’s disease
Chaudhuri, К. R., & Martínez‐Martín, P. (2008) · European Journal of Neurology · doi:10.1111/j.1468-1331.2008.02212.x · Cited by 160 · see citing works
“5% in HY stages 2 and 3 – from centres in the United Kingdom, the United States, Germany, Spain, and Italy [12].”
BackgroundMethodInfluentialThe Impact of Physical Activity on Non-Motor Symptoms in Parkinson’s Disease: A Systematic Review
Cusso, M., Donald, K. J., & Khoo, T. K. (2016) · Frontiers in Medicine · doi:10.3389/fmed.2016.00035 · Cited by 159 · see citing works
Kurtis, M. M., Rajah, T., Delgado, L. F., & Dafsari, H. S. (2017) · npj Parkinson s Disease · doi:10.1038/npjparkd.2016.24 · Cited by 158 · see citing works
Sleep-related problems of Parkinson’s disease
Dhawan, V., Healy, D. G., Pal, S., & Chaudhuri, К. R. (2006) · Age and Ageing · doi:10.1093/ageing/afj087 · Cited by 157 · see citing works
Self-citationSleep Disorders in Parkinson's Disease
Schrempf, W., Brandt, M., Storch, A., & Reichmann, H. (2014) · Journal of Parkinson s Disease · doi:10.3233/jpd-130301 · Cited by 141 · see citing works
“Patients also complain about nocturia, which is very common in PD and is responsible for sleep disruption [22, 50, 51].”
Parkinson disease phenotype in Ashkenazi jews with and without LRRK2 G2019S mutations
Alcalay, R. N., Mirelman, A., Saunders-Pullman, R. J., Tang, M., Santana, H. M., Raymond, D., Roos, E., Orbe‐Reilly, M., Gurevich, T., Shira, A. B., et al. (2013) · Movement Disorders · doi:10.1002/mds.25647 · Cited by 139 · see citing works
“All participants were evaluated using section III (the motor section) of the UPDRS (UPDRS-III)(15); the Montreal Cognitive Assessment (MoCA),(16) which was performed in either Hebrew(17) or English based on participants’ native language; the abbreviated Geriatric Depression Scale (GDS-15),(18) in which higher scores s…”
MethodNighttime sleep problems and daytime sleepiness in Parkinson's disease
Verbaan, D., van Rooden, S. M., Jeukens‐Visser, M., Marinus, J., & van Hilten, J. J. (2007) · Movement Disorders · doi:10.1002/mds.21727 · Cited by 139 · see citing works
“DOI: 10.1002/mds.21727 35 disability, and global outcomes of health using valid and reliable assessment instruments for PD. Findings obtained from the first annual evaluation of 420 patients assessed between May 2003 and March 2006 were used for analysis.”
InfluentialMoum, S. J., Price, C. C., Limotai, N., Oyama, G., Ward, H. E., Jacobson, C. E., Foote, K. D., & Okun, M. S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029768 · Cited by 136 · see citing works
“Most patients undergoing DBS are selected based on the potential for improvement of motor symptoms as well as for potential improvement in on-off medication fluctuations”
BackgroundPain in Parkinson disease: a cross-sectional survey of its prevalence, specifics, and therapy
Buhmann, C., Wrobel, N., Grashorn, W., Fründt, O., Wesemann, K., Diedrich, S., & Bingel, U. (2017) · Journal of Neurology · doi:10.1007/s00415-017-8426-y · Cited by 136 · see citing works
Neuropsychiatric symptoms, behavioural disorders, and quality of life in Parkinson's disease
Balestrino, R., & Martinez-Martin, P. (2017) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2016.12.060 · Cited by 135 · see citing works
Ethnic Variation in the Manifestation of Parkinson’s Disease: A Narrative Review
Ben-Joseph, A., Marshall, C. R., Lees, A. J., & Noyce, A. J. (2019) · Journal of Parkinson s Disease · doi:10.3233/jpd-191763 · Cited by 135 · see citing works
Stubendorff, K., Aarsland, D., Minthon, L., & Londos, E. (2012) · PLoS ONE · doi:10.1371/journal.pone.0045451 · Cited by 134 · see citing works
“In PD, the non-motor symptoms are related to advanced stages in patients with a fully developed motor phenotype [33], but are reported significantly more common in the disease across all stages than in controls [34].”
Tibar, H., Bayad, K. E., Bouhouche, A., Haddou, E. H. A. B., Benomar, A., Yahyaoui, M., Benazzouz, A., & Regragui, W. (2018) · Frontiers in Neurology · doi:10.3389/fneur.2018.00170 · Cited by 132 · see citing works
Validation of the non-motor symptoms questionnaire (NMS-Quest)
Romenets, S. R., Wolfson, C. M., Galatas, C., Pelletier, A., Altman, R., Wadup, L., & Postuma, R. B. (2011) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2011.08.013 · Cited by 131 · see citing works
Natale, G., Pasquali, L., Ruggieri, S. A., Paparelli, A., & Fornai, F. (2008) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2008.01162.x · Cited by 129 · see citing works
Unmet needs in Parkinson disease: Motor and non-motor
LeWitt, P. A., & Chaudhuri, К. R. (2020) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2020.09.024 · Cited by 127 · see citing works
Gastrointestinal barriers to levodopa transport and absorption in Parkinson's disease
Leta, V., Klingelhoefer, L., Longardner, K., Campagnolo, M., Çotur, H., Aureli, F., Metta, V., Bhidayasiri, R., Chung‐Faye, G., Falup‐Pecurariu, C., et al. (2023) · European Journal of Neurology · doi:10.1111/ene.15734 · Cited by 127 · see citing works
“Constipation has a prevalence of 20%– 89% [3,34,90] and is up to sixfold more common amongst PwP than amongst age- and sexmatched controls [90,91].”
BackgroundSelf-citationRetinal thickness in Parkinson's disease
Archibald, N. K., Clarke, M. W., Mosimann, U. P., & Burn, D. J. (2011) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2011.03.004 · Cited by 125 · see citing works
Chaudhuri, К. R., Rojo, J. M., Schapira, A. H. V., Brooks, D. J., Stocchi, F., Odin, P., Antonini, A., Brown, R. G., & Martínez‐Martín, P. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057221 · Cited by 122 · see citing works
Self-citationEarly Parkinson’s disease and non-motor issues
Chaudhuri, К. R., & Naidu, Y. (2008) · Journal of Neurology · doi:10.1007/s00415-008-5006-1 · Cited by 121 · see citing works
Swallowing disturbances in Parkinson's disease: A multivariate analysis of contributing factors
Cereda, E., Cilia, R., Klersy, C., Canesi, M., Zecchinelli, A., Mariani, C. B., Tesei, S., Sacilotto, G., Meucci, N., Zini, M., et al. (2014) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2014.09.031 · Cited by 120 · see citing works
Effects of Sleep Disorders on the Non-Motor Symptoms of Parkinson Disease
Neikrug, A. B., Maglione, J. E., Liu, L., Natarajan, L., Avanzino, J. A., Corey‐Bloom, J., Palmer, B. W., Loredo, J. S., & Ancoli‐Israel, S. (2013) · Journal of Clinical Sleep Medicine · doi:10.5664/jcsm.3148 · Cited by 120 · see citing works
Nonmotor Symptoms in Parkinson’s Disease in 2012: Relevant Clinical Aspects
Bonnet, A. M., Jutras, M., Czernecki, V., Corvol, J., & Vidailhet, M. (2012) · Parkinson s Disease · doi:10.1155/2012/198316 · Cited by 119 · see citing works
Beneficial Effects of Bilateral Subthalamic Stimulation on Non-Motor Symptoms in Parkinson's Disease
Dafsari, H. S., Reddy, P., Herchenbach, C., Wawro, S., Petry‐Schmelzer, J. N., Visser-Vandewalle, V. E. R. M., Rizos, A., Silverdale, M., Ashkan, K., Samuel, M., et al. (2015) · Brain stimulation · doi:10.1016/j.brs.2015.08.005 · Cited by 117 · see citing works
Do nonmotor symptoms in Parkinson's disease differ from normal aging?
Krishnan, S., Sarma, G., Sarma, P. S., & Kishore, A. (2011) · Movement Disorders · doi:10.1002/mds.23826 · Cited by 117 · see citing works
Knudsen, K., Fedorova, T. D., Bekker, A. C., Iversen, P., Østergaard, K., Krogh, K., & Borghammer, P. (2017) · Journal of Parkinson s Disease · doi:10.3233/jpd-161050 · Cited by 117 · see citing works
“Finally, NMS symptoms in general, including constipation, were evaluated by the non-motor symptoms questionnaire (NMSQuest), defining constipation as <3 bowel movements per week and/or straining during the past month [12].”
Prevalence and duration of non‐motor symptoms in prodromal Parkinson's disease
Durcan, R., Wiblin, L., Lawson, R. A., Khoo, T. K., Yarnall, A. J., Duncan, G. W., Brooks, D. J., Pavese, N., Burn, D. J., & the ICICLE‐PD Study Group (2019) · European Journal of Neurology · doi:10.1111/ene.13919 · Cited by 117 · see citing works
“Participant NMS burden was assessed at the initial patient screening visit using the Non-Motor Symptom Questionnaire (NMSQuest) [11].”
MethodNonmotor Symptoms in Parkinson's Disease
Sung, V., & Nicholas, A. P. (2013) · Neurologic Clinics · doi:10.1016/j.ncl.2013.04.013 · Cited by 117 · see citing works
Erro, R., Picillo, M., Vitale, C., Amboni, M., Moccia, M., Longo, K., Cozzolino, A., Giordano, F., Rosa, A. D., Michele, G. D., et al. (2012) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp-2012-303419 · Cited by 115 · see citing works
“Moreover, for detection of NMS, we used a validated tool in PD, in line with previous studies.(16) 33 Finally, we checked the presence/absence of NMS by means of NMSQuest, and we did not rate their severity, thus missing to assess an NMS severity progression.”
MethodInfluentialSelf-citationConcha‐Marambio, L., Weber, S., Farris, C. M., Dakna, M., Lang, E., Wicke, T., Ma, Y., Starke, M., Ebentheuer, J., Sixel‐Döring, F., et al. (2023) · Movement Disorders · doi:10.1002/mds.29329 · Cited by 116 · see citing works
Chaudhuri, К. R., Sauerbier, A., Rojo, J. M., Sethi, K. D., Schapira, A. H. V., Brown, R. G., Antonini, A., Stocchi, F., Odin, P., Bhattacharya, K., et al. (2015) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2014.12.031 · Cited by 113 · see citing works
Self-citationNon‐motor Parkinson disease: new concepts and personalised management
Titova, N., & Chaudhuri, К. R. (2018) · The Medical Journal of Australia · doi:10.5694/mja17.00993 · Cited by 112 · see citing works
Serotonergic Dysfunction in Parkinson's Disease and Its Relevance to Disability
Politis, M., & Loane, C. (2011) · The Scientific World JOURNAL · doi:10.1100/2011/172893 · Cited by 109 · see citing works
“The serotonergic system is thought to be involved in the modulation of various cognitive and physiological processes, such as, mood, emotion, sleep, and appetite; thus altered serotonergic neurotransmission is likely to be implicated in both motor and nonmotor disturbances observed in PD [2].”
Motor and Non-Motor Symptoms in Parkinson’s Disease: Effects on Quality of Life
Gökçal, E., Gür, V. E., Selvitop, R., Yıldız, G. B., & Asıl, T. (2016) · Nöro Psikiyatri Arşivi · doi:10.5152/npa.2016.12758 · Cited by 109 · see citing works
“The first international prevalence study reported a higher prevalence of non-motor symptoms in IPD patients compared to age-matched controls, as well as the presence of 10–12 non-motor symptoms in a typical patient (14).”
BackgroundPain in Parkinson's disease: facts and uncertainties
Antonini, A., Tinazzi, M., Abbruzzese, G., Berardelli, A., Chaudhuri, К. R., Defazio, G., Ferreira, J. J., Martínez‐Martín, P., Trenkwalder, C., & Rascol, O. (2018) · European Journal of Neurology · doi:10.1111/ene.13624 · Cited by 108 · see citing works
Lenka, A., Jhunjhunwala, K. R., Saini, J., & Pal, P. K. (2015) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2015.04.005 · Cited by 106 · see citing works
Lakshminarayana, R., Wang, D., Burn, D. J., Chaudhuri, К. R., Galtrey, C. M., Guzman, N. V., Hellman, B., James, B., Pal, S., Stamford, J., et al. (2017) · npj Parkinson s Disease · doi:10.1038/s41531-016-0003-z · Cited by 107 · see citing works
Self-citationCircadian rest‐activity rhythm is altered in Parkinson's disease patients with hallucinations
Whitehead, D. L., Davies, A. D. M., Playfer, J. R., & Turnbull, C. J. (2008) · Movement Disorders · doi:10.1002/mds.22057 · Cited by 105 · see citing works
“Individuals with Parkinson’s disease (PD) display a range of sleep disturbances; insomnias, and sleep fragmentation, and parasomnias such as REM behavior disorder, excessive daytime sleepiness, and sleep apnoea.(1,2) There is a large and growing body of literature investigating these disorders, seeking both clinical c…”
BackgroundProbable RBD and association with neurodegenerative disease markers: A population‐based study
Mahlknecht, P., Seppi, K., Frauscher, B., Kiechl, S. J., Willeit, J., Stockner, H., Djamshidian, A., Nocker, M., Rastner, V., Defrancesco, M., et al. (2015) · Movement Disorders · doi:10.1002/mds.26350 · Cited by 104 · see citing works
A panel of four decreased serum microRNAs as a novel biomarker for early Parkinson’s disease
Dong, H., Wang, C., Lu, S., Yu, C., Huang, L., Feng, W., Xu, H., Chen, X., Zen, K., Yan, Q., et al. (2015) · Biomarkers · doi:10.3109/1354750x.2015.1118544 · Cited by 103 · see citing works
“…modified Hoehn and Yahr staging of Parkinson’s disease) (Martinezmartin et al., 1994), Parkinson’s Disease Non-Motor Symptoms questionnaire (PDNMS) (Chaudhuri et al., 2006), Parkinson’s Disease Sleep Scale (PDSS), Hamilton Depression Rating Scale (HAMD), and Hamilton Anxiety Rating Scale (HAMA).”
BackgroundMethodInfluentialClinical Assessments in Parkinson's Disease
Bhidayasiri, R., & Martínez‐Martín, P. (2017) · International review of neurobiology · doi:10.1016/bs.irn.2017.01.001 · Cited by 102 · see citing works
Differences in the Presentation and Progression of Parkinson's Disease by Sex
Iwaki, H., Blauwendraat, C., Leonard, H. L., Makarious, M. B., Kim, J. J., Liu, G., Maple‐Grødem, J., Corvol, J., Pihlstrøm, L., van Nimwegen, M., et al. (2020) · Movement Disorders · doi:10.1002/mds.28312 · Cited by 103 · see citing works
- Authors
- Chaudhuri, K. R., Martinez‐Martin, P., Schapira, A. H. V., Stocchi, F., Sethi, K., Odin, P., Brown, R. G., Koller, W., Barone, P., MacPhee, G., Kelly, L., Rabey, M., MacMahon, D., Thomas, S., Ondo, W., Rye, D., Forbes, A., Tluk, S., Dhawan, V., Bowron, A., Williams, A. J., & Olanow, C. W.
- Affiliations
- The Royal Free Hospital (GB)
- Istituto Neurologico Mediterraneo (IT)
- Augusta University (US)
- Klinikum Bremerhaven-Reinkenheide (DE)
- King's College London (GB)
- University of North Carolina at Chapel Hill (US)
- Southern General Hospital (GB)
- Parkinson's UK (GB)
- Tel Aviv University (IL)
- Camborne Redruth Community Hospital (GB)
- Royal College of Nursing (GB)
- Baylor College of Medicine (US)
- Emory University (US)
- University Hospital Lewisham (GB)
- King's College Hospital (GB)
- North Tyneside General Hospital (GB)
- St Thomas' Hospital (GB)
- Icahn School of Medicine at Mount Sinai (US)
- ORCID
- Venue
- Movement Disorders
- Publisher
- Wiley
- Published
- 2006-03-17
- Volume
- 21
- Issue
- 7
- Pages
- 916-923
- ISSN
- 0885-3185 (ISSN-L)
- 1531-8257
- OpenAlex
- W2168946626
- Cited by
- 1,100
- References
- 24
- Citations by year
- 2026: 36 · 2025: 83 · 2024: 64 · 2023: 73 · 2022: 80 · 2021: 84 · 2020: 58 · 2019: 52 · 2018: 63 · 2017: 76 · 2016: 54 · 2015: 60 · 2014: 56 · 2013: 73 · 2012: 43
- FWCI
- 14.80
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Movement Disorders (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Research Portal (King's College London) (submittedVersion)
- Funders
- Pfizer Corporation
- GSK Pharmaceuticals
- U.K. Parkinson's Disease Society
- Topics
- Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
- Health Sciences › Medicine › Neurology › Neurological disorders and treatments
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Keywords
- Parkinson's disease, non-motor symptoms, screening questionnaire, feasibility, validity, acceptability, symptom prevalence, disease stage, disease duration, symptom disclosure, diplopia, dysarthria, apathy, anosmia, hyposmia, taste disorders, patient-reported outcomes
- MeSH terms
- Aged, Aged, 80 and over, Female, Health Surveys, Humans, Male, Middle Aged, Neurologic Examination, Neuropsychological Tests, Parkinson Disease, Pilot Projects, Quality of Life, Surveys and Questionnaires, Sick Role, Outcome Assessment, Health Care, Sickness Impact Profile
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