The clinical diagnosis of Parkinson's disease

Abstract

After more than 200 years since its initial description, the clinical diagnosis of Parkinson's disease (PD) remains an often-challenging endeavor, with broad implications that are fundamental for clinical management. Despite major developments in understanding it's pathogenesis, pathological landmarks, non-motor features and potential paraclinical clues, the most accepted diagnostic criteria remain solidly based on a combination of clinical signs. Here, we review this process, discussing its history, clinical criteria, differential diagnoses, ancillary diagnostic testing, and the role of non-motor and pre-motor signs and symptoms.

Resumo

Passados mais de 200 anos desde a sua descrição inicial, o diagnóstico clínico da doença de Parkinson (DP) continua a ser um processo muitas vezes desafiante, com amplas implicações que são fundamentais para o manejo clínico. Apesar dos grandes desenvolvimentos na compreensão da sua patogénese, marcadores patológicos, características não motoras e potenciais pistas paraclínicas, os critérios diagnósticos mais aceitos permanecem solidamente baseados numa combinação de sinais clínicos motores. Aqui, revisamos esse processo, discutindo sua história, critérios clínicos, diagnósticos diferenciais, testes diagnósticos complementares e o papel dos sinais e sintomas não motores e pré-motores.

Keywords

Parkinson Disease - Supranuclear Palsy, Progressive - Multiple System Atrophy - Atherosclerotic Parkinsonism - Secondary Parkinsonism

Palavras-chave

Doença de Parkinson - Paralisia Supranuclear Progressiva - Atrofia de Múltiplos Sistemas - Parkinsonismo Secundário - Parkinsonismo Aterosclerótico

Authors' Contributions

RPM: conceptualization, formal analysis, project, writing – original draft, writing – review & editing; vt - conceptualization, formal analysis, project, writing – original draft, writing – review & editing; JLP: conceptualization, formal analysis, project, writing – original draft, writing – review & editing; LSM: conceptualization, formal analysis, project, writing – original draft, writing – review & editing.

Publikationsverlauf

Eingereicht: 14. September 2023

Angenommen: 19. November 2023

Artikel online veröffentlicht:
07. Februar 2024

• References

• 1 Parkinson J. An essay on the shaking palsy. 1817. J Neuropsychiatry Clin Neurosci 2002; 14 (02) 223-236 , discussion 222
• 2 Duvoisin RC. A brief history of parkinsonism. Neurol Clin 1992; 10 (02) 301-316
• 3 Goetz CG. The history of Parkinson's disease: early clinical descriptions and neurological therapies. Cold Spring Harb Perspect Med 2011; 1 (01) a008862
• 4 Pearce JM. Aspects of the history of Parkinson's disease. J Neurol Neurosurg Psychiatry 1989; Suppl: 6-10
• 5 Hoehn MM, Yahr MD. Parkinsonism: onset, progression and mortality. Neurology 1967; 17 (05) 427-442
• 6 Quinn N. Multiple system atrophy–the nature of the beast. J Neurol Neurosurg Psychiatry 1989; Suppl: 78-89
• 7 Rebeiz JJ, Kolodny EH, Richardson Jr EP. Corticodentatonigral degeneration with neuronal achromasia: a progressive disorder of late adult life. Trans Am Neurol Assoc 1967; 92: 23-26
• 8 Steele JC, Richardson JC, Olszewski J. Progressive Supranuclear Palsy. A Heterogeneous Degeneration Involving the Brain Stem, Basal Ganglia and Cerebellum with Vertical Gaze and Pseudobulbar Palsy, Nuchal Dystonia and Dementia. Arch Neurol 1964; 10: 333-359
• 9 Forno LS. Concentric hyalin intraneuronal inclusions of Lewy type in the brains of elderly persons (50 incidental cases): relationship to parkinsonism. J Am Geriatr Soc 1969; 17 (06) 557-575
• 10 Gibb WR, Lees AJ. The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson's disease. J Neurol Neurosurg Psychiatry 1988; 51 (06) 745-752
• 11 Gibb WR, Lees AJ. Anatomy, pigmentation, ventral and dorsal subpopulations of the substantia nigra, and differential cell death in Parkinson's disease. J Neurol Neurosurg Psychiatry 1991; 54 (05) 388-396
• 12 Yahr MD, Duvoisin RC, Schear MJ, Barrett RE, Hoehn MM. Treatment of parkinsonism with levodopa. Arch Neurol 1969; 21 (04) 343-354
• 13 Koller WC. The diagnosis of Parkinson's disease. Arch Intern Med 1984; 144 (11) 2146-2147
• 14 Gibb WR. Accuracy in the clinical diagnosis of parkinsonian syndromes. Postgrad Med J 1988; 64 (751) 345-351
• 15 Gibb WR, Lees AJ. The significance of the Lewy body in the diagnosis of idiopathic Parkinson's disease. Neuropathol Appl Neurobiol 1989; 15 (01) 27-44
• 16 Shy GM, Drager GA. A neurological syndrome associated with orthostatic hypotension: a clinical-pathologic study. Arch Neurol 1960; 2: 511-527
• 17 Hughes AJ, Daniel SE, Lees AJ. Improved accuracy of clinical diagnosis of Lewy body Parkinson's disease. Neurology 2001; 57 (08) 1497-1499
• 18 Polymeropoulos MH, Lavedan C, Leroy E. et al. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 1997; 276 (5321) 2045-2047
• 19 Zimprich A, Biskup S, Leitner P. et al. Mutations in LRRK2 cause autosomal-dominant parkinsonism with pleomorphic pathology. Neuron 2004; 44 (04) 601-607
• 20 Paisán-Ruíz C, Jain S, Evans EW. et al. Cloning of the gene containing mutations that cause PARK8-linked Parkinson's disease. Neuron 2004; 44 (04) 595-600
• 21 Ross GW, Abbott RD, Petrovitch H. et al. Association of olfactory dysfunction with incidental Lewy bodies. Mov Disord 2006; 21 (12) 2062-2067
• 22 Ward CD, Hess WA, Calne DB. Olfactory impairment in Parkinson's disease. Neurology 1983; 33 (07) 943-946
• 23 Hakusui S, Yasuda T, Yanagi T. et al. A radiological analysis of heart sympathetic functions with meta-[123I]iodobenzylguanidine in neurological patients with autonomic failure. J Auton Nerv Syst 1994; 49 (01) 81-84
• 24 Benamer TS, Patterson J, Grosset DG. et al. Accurate differentiation of parkinsonism and essential tremor using visual assessment of [123I]-FP-CIT SPECT imaging: the [123I]-FP-CIT study group. Mov Disord 2000; 15 (03) 503-510
• 25 Postuma RB, Berg D, Stern M. et al. MDS clinical diagnostic criteria for Parkinson's disease. Mov Disord 2015; 30 (12) 1591-1601
• 26 Berg D, Adler CH, Bloem BR. et al. Movement disorder society criteria for clinically established early Parkinson's disease. Mov Disord 2018; 33 (10) 1643-1646
• 27 Munhoz RP, Werneck LC, Teive HA. The differential diagnoses of parkinsonism: findings from a cohort of 1528 patients and a 10 years comparison in tertiary movement disorders clinics. Clin Neurol Neurosurg 2010; 112 (05) 431-435
• 28 Munhoz RP, Bertucci Filho D, Teive HA. Not all drug-induced parkinsonism are the same: the effect of drug class on motor phenotype. Neurol Sci 2017; 38 (02) 319-324
• 29 Höglinger GU, Respondek G, Stamelou M. et al; Movement Disorder Society-endorsed PSP Study Group. Clinical diagnosis of progressive supranuclear palsy: The movement disorder society criteria. Mov Disord 2017; 32 (06) 853-864
• 30 Wenning GK, Stankovic I, Vignatelli L. et al. The Movement Disorder Society Criteria for the Diagnosis of Multiple System Atrophy. Mov Disord 2022; 37 (06) 1131-1148
• 31 Yamada M, Komatsu J, Nakamura K. et al. Diagnostic Criteria for Dementia with Lewy Bodies: Updates and Future Directions. J Mov Disord 2020; 13 (01) 1-10
• 32 Armstrong MJ, Litvan I, Lang AE. et al. Criteria for the diagnosis of corticobasal degeneration. Neurology 2013; 80 (05) 496-503
• 33 Braak H, Del Tredici K, Rüb U, de Vos RA, Jansen Steur EN, Braak E. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging 2003; 24 (02) 197-211
• 34 Postuma RB, Aarsland D, Barone P. et al. Identifying prodromal Parkinson's disease: pre-motor disorders in Parkinson's disease. Mov Disord 2012; 27 (05) 617-626
• 35 Munhoz RP, Moro A, Silveira-Moriyama L, Teive HA. Non-motor signs in Parkinson's disease: a review. Arq Neuropsiquiatr 2015; 73 (05) 454-462
• 36 Doty RL, Stern MB, Pfeiffer C, Gollomp SM, Hurtig HI. Bilateral olfactory dysfunction in early stage treated and untreated idiopathic Parkinson's disease. J Neurol Neurosurg Psychiatry 1992; 55 (02) 138-142
• 37 Saifee T, Lees AJ, Silveira-Moriyama L. Olfactory function in Parkinson's disease in ON versus OFF states. J Neurol Neurosurg Psychiatry 2010; 81 (11) 1293-1295
• 38 Bohnen NI, Müller ML, Kotagal V. et al. Olfactory dysfunction, central cholinergic integrity and cognitive impairment in Parkinson's disease. Brain 2010; 133 (Pt 6): 1747-1754
• 39 Noyce AJ, Bestwick JP, Silveira-Moriyama L. et al. Meta-analysis of early nonmotor features and risk factors for Parkinson disease. Ann Neurol 2012; 72 (06) 893-901
• 40 Schenck CH, Mahowald MW. REM sleep behavior disorder: clinical, developmental, and neuroscience perspectives 16 years after its formal identification in SLEEP. Sleep 2002; 25 (02) 120-138
• 41 Postuma RB, Montplaisir J. Predicting Parkinson's disease - why, when, and how?. Parkinsonism Relat Disord 2009; 15 (Suppl. 03) S105-S109
• 42 American Academy of Sleep Medicine. ICSD - International classification of sleep disorders: diagnostic and coding manual. Westchester: American Sleep Disorders Association;; 1990
• 43 Postuma RB, Arnulf I, Hogl B. et al. A single-question screen for rapid eye movement sleep behavior disorder: a multicenter validation study. Mov Disord 2012; 27 (07) 913-916
• 44 Postuma RB, Gagnon JF, Montplaisir J. Rapid eye movement sleep behavior disorder as a biomarker for neurodegeneration: the past 10 years. Sleep Med 2013; 14 (08) 763-767
• 45 Postuma RB, Iranzo A, Hu M. et al. Risk and predictors of dementia and parkinsonism in idiopathic REM sleep behaviour disorder: a multicentre study. Brain 2019; 142 (03) 744-759
• 46 Munhoz RP, Teive HA. REM sleep behaviour disorder: how useful is it for the differential diagnosis of parkinsonism?. Clin Neurol Neurosurg 2014; 127: 71-74
• 47 Starkstein SE, Brockman S, Hayhow BD. Psychiatric syndromes in Parkinson's disease. Curr Opin Psychiatry 2012; 25 (06) 468-472
• 48 Leentjens AF, Van den Akker M, Metsemakers JF, Lousberg R, Verhey FR. Higher incidence of depression preceding the onset of Parkinson's disease: a register study. Mov Disord 2003; 18 (04) 414-418
• 49 Ishihara L, Brayne C. A systematic review of depression and mental illness preceding Parkinson's disease. Acta Neurol Scand 2006; 113 (04) 211-220
• 50 Abbott RD, Petrovitch H, White LR. et al. Frequency of bowel movements and the future risk of Parkinson's disease. Neurology 2001; 57 (03) 456-462
• 51 Cersosimo MG, Benarroch EE. Autonomic involvement in Parkinson's disease: pathology, pathophysiology, clinical features and possible peripheral biomarkers. J Neurol Sci 2012; 313 (1-2): 57-63
• 52 Munhoz RP, Ribas CB. Body mass index in Parkinson's disease. Parkinsonism Relat Disord 2005; 11 (06) 407 , author reply 409
• 53 Cheshire Jr WP, Wszolek ZK. Body mass index is reduced early in Parkinson's disease. Parkinsonism Relat Disord 2005; 11 (01) 35-38
• 54 Chen H, Zhang SM, Hernán MA, Willett WC, Ascherio A. Weight loss in Parkinson's disease. Ann Neurol 2003; 53 (05) 676-679
• 55 Goldman JG, Postuma R. Premotor and nonmotor features of Parkinson's disease. Curr Opin Neurol 2014; 27 (04) 434-441
• 56 Pagano G, Niccolini F, Politis M. Imaging in Parkinson's disease. Clin Med (Lond) 2016; 16 (04) 371-375
• 57 Meijer FJA, Goraj B, Bloem BR, Esselink RAJ. Clinical Application of Brain MRI in the Diagnostic Work-up of Parkinsonism. J Parkinsons Dis 2017; 7 (02) 211-217
• 58 Weng YH, Yen TC, Chen MC. et al. Sensitivity and specificity of 99mTc-TRODAT-1 SPECT imaging in differentiating patients with idiopathic Parkinson's disease from healthy subjects. J Nucl Med 2004; 45 (03) 393-401
• 59 Arjona M, Toldo JMP, Queiroz NC. et al. A Real-World Study of Cerebral 99mTc-TRODAT-1 Single-Photon Emission Computed Tomography (SPECT) Imaging of the Dopamine Transporter in Patients with Parkinson Disease from a Tertiary Hospital in Brazil. Med Sci Monit 2020; 26: e925130
• 60 Pavese N, Tai YF. Nigrosome Imaging and Neuromelanin Sensitive MRI in Diagnostic Evaluation of Parkinsonism. Mov Disord Clin Pract (Hoboken) 2018; 5 (02) 131-140
• 61 Belezia AB, Marussi VH, Yared J. et al. PET-CT imaging in a patient with progressive supranuclear palsy. Arq Neuropsiquiatr 2015; 73 (04) 364-365
• 62 Bor-Seng-Shu E, Pedroso JL, Felicio AC. et al. Substantia nigra echogenicity and imaging of striatal dopamine transporters in Parkinson's disease: a cross-sectional study. Parkinsonism Relat Disord 2014; 20 (05) 477-481
• 63 Gasser T. Genetic testing for Parkinson's disease in clinical practice. J Neural Transm (Vienna) 2023; 130 (06) 777-782
• 64 Saunders-Pullman R, Raymond D, Ortega RA. et al. International Genetic Testing and Counseling Practices for Parkinson's Disease. Mov Disord 2023; 38 (08) 1527-1535
• 65 Aguiar Pde C, Lessa PS, Godeiro Jr C. et al. Genetic and environmental findings in early-onset Parkinson's disease Brazilian patients. Mov Disord 2008; 23 (09) 1228-1233
• 66 Munhoz RP, Wakutani Y, Marras C. et al. The G2019S LRRK2 mutation in Brazilian patients with Parkinson's disease: phenotype in monozygotic twins. Mov Disord 2008; 23 (02) 290-294
• 67 Parnetti L, Gaetani L, Eusebi P. et al. CSF and blood biomarkers for Parkinson's disease. Lancet Neurol 2019; 18 (06) 573-586