Subscribe to RSS

DOI: 10.1590/0004-282X-ANP-2022-S130
Magnetic resonance and dopamine transporter imaging for the diagnosis of Parkinson’s disease: a narrative review
Ressonância magnética e neuroimagem do transportador de dopamina no diagnóstico da doença de Parkinson: uma revisão narrativa
ABSTRACT
Background: the diagnosis of Parkinson's disease (PD) can be challenging, especially in the early stages, albeit its updated and validated clinical criteria. Recent developments on neuroimaging in PD, altogether with its consolidated role of excluding secondary and other neurodegenerative causes of parkinsonism, provide more confidence in the diagnosis across the different stages of the disease. This review highlights current knowledge and major recent advances in magnetic resonance and dopamine transporter imaging in aiding PD diagnosis. Objective: This study aims to review current knowledge about the role of magnetic resonance imaging and neuroimaging of the dopamine transporter in diagnosing Parkinson's disease. Methods: We performed a non-systematic literature review through the PubMed database, using the keywords "Parkinson", “magnetic resonance imaging”, “diffusion tensor”, “diffusion-weighted”, “neuromelanin”, “nigrosome-1”, “single-photon emission computed tomography”, “dopamine transporter imaging”. The search was restricted to articles written in English, published between January 2010 and February 2022. Results: The diagnosis of Parkinson's disease remains a clinical diagnosis. However, new neuroimaging biomarkers hold promise for increased diagnostic accuracy, especially in earlier stages of the disease. Conclusion: Future validation of new imaging biomarkers bring the expectation of an increased neuroimaging role in the diagnosis of PD in the following years.
RESUMO
Antecedentes: O diagnóstico da doença de Parkinson (DP) pode ser desafiador, principalmente nas fases iniciais da doença, embora tenha critérios clínicos atualizados e validados. Os avanços recentes em neuroimagem na DP, além do seu papel já consolidado de excluir causas secundárias e outras causas neurodegenerativas de parkinsonismo, tem contribuído para uma maior confiabilidade no diagnóstico em diferentes estágios da doença. Nesta revisão, nós destacamos os principais avanços de ressonância magnética e imagem do transportador de dopamina em auxiliar o diagnóstico de DP. Objetivo: realizar uma revisão acerca do conhecimento atual sobre o papel da ressonância magnética e imagem do transportador de dopamina no diagnóstico de doença de Parkinson. Método: Realizamos uma revisão não sistemática da literatura através da base de dados PubMed, utilizando as palavras-chave "Parkinson", “magnetic resonance imaging”, “diffusion tensor”, “diffusion-weighted”, “neuromelanin”, “nigrosome-1”, “single-photon emission computed tomography”, “dopamine transporter imaging”. A busca foi restrita a artigos escritos em inglês, publicados entre janeiro de 2010 e fevereiro de 2022. Resultados: O diagnóstico de doença de Parkinson continua sendo um diagnóstico clínico, contudo, novos biomarcadores de neuroimagem são promissores para o aumento da acurácia diagnóstica, especialmente em fases mais precoces da doença. Conclusão: A validação futura de novos biomarcadores de imagem traz a expectativa de um maior papel da neuroimagem no diagnóstico de doença de Parkinson nos próximos anos.
Keywords:
Parkinson Disease - Parkinsonian Disorders - Diffusion Tensor Imaging - Single Photon Emission Computed Tomography Computed Tomography - Melanins - Magnetic Resonance Imaging - Diffusion Magnetic Resonance ImagingPalavras-chave:
Doença de Parkinson - Transtornos Parkinsonianos - Imagem de Tensor de Difusão - Melaninas - Imageamento por Ressonância Magnética - Imagem de Difusão por Ressonância MagnéticaAuthors’s contributions:
RTVO: designed the study and drafted the manuscript; JYSY: drafted and revised the manuscript; DMN: drafted and revised the manuscript; MSH: supervised and revised the manuscript; JBP: designed the study, supervised, and revised the manuscript.
Publication History
Received: 28 March 2022
Accepted: 29 April 2022
Article published online:
06 February 2023
© 2022. Academia Brasileira de Neurologia. This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commecial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/)
Thieme Revinter Publicações Ltda.
Rua do Matoso 170, Rio de Janeiro, RJ, CEP 20270-135, Brazil
-
References
- 1 Armstrong MJ, Okun MS. Diagnosis and treatment of Parkinson Disease: A review. JAMA 2020; 323 (06) 548-560 https://doi.org/10.1001/jama.2019.22360
- 2 Tolosa E, Garrido A, Scholz SW, Poewe W. Challenges in the diagnosis of Parkinson's disease. Lancet Neurol 2021; 20 (05) 385-397
- 3 Maserejian N, Vinikoor-Imler L, Dilley A. Estimation of the 2020 Global Population of Parkinson’s Disease (PD) [abstract]. Mov Disord. 2020 ; 35 (suppl 1) https://www.mdsabstracts.org/abstract/estimation-of-the-2020-global-population-of-parkinsons-disease-pd/
- 4 Dorsey ER, Sherer T, Okun MS, Bloem BR. The emerging evidence of the Parkinson pandemic. J Parkinsons Dis 2018; 8 s1 S3-S8 https://doi.org/10.3233/jpd-181474
- 5 Postuma RB, Berg D, Stern M, Poewe W, Olanow CW, Oertel W. et al. MDS clinical diagnostic criteria for Parkinson’s disease. Mov Disord 2015; 30 (12) 1591-1601 https://doi.org/10.1002/mds.26424
- 6 Berg D, Postuma RB, Adler CH. et al. MDS research criteria for prodromal Parkinson’s disease. Mov Disord 2015; 30 (12) 1600-1611 https://doi.org/10.1002/mds.26431
- 7 Rizzo G, Copetti M, Arcuti S, Martino D, Fontana A, Logroscino G. Accuracy of clinical diagnosis of Parkinson disease. Neurology 2016; 86 (06) 566-576 https://doi.org/10.1212/wnl.2022s1302022s1302350
- 8 Adler CH, Beach TG, Hentz JG, Shill HA, Caviness JN, Driver-Dunckley E. et al. Low clinical diagnostic accuracy of early vs advanced Parkinson disease: Clinicopathologic study. Neurology 2014; 83 (05) 406-412 https://doi.org/10.1212/WNL.2022s1302022s1300641
- 9 Peralta C, Strafella AP, van Eimeren T, Ceravolo R, Seppi K, Kaasinen V. et al. Pragmatic approach on neuroimaging techniques for the differential diagnosis of Parkinsonisms. Mov Disord Clin Pract 2021; 9 (01) 6-19 https://doi.org/10.1002/mdc3.13354
- 10 Hughes AJ, Daniel SE, Lees AJ. Improved accuracy of clinical diagnosis of Lewy body Parkinson’s disease. Neurology 2001; 57 (08) 1497-1499 https://doi.org/10.1212/wnl.57.8.1497
- 11 Reimão S, Guerreiro C, Seppi K, Ferreira JJ, Poewe W. A standardized MR imaging protocol for Parkinsonism. Mov Disord 2020; 35 (10) 1745-1750 https://doi.org/10.1002/mds.28204
- 12 Saeed U, Compagnone J, Aviv RI, Strafella AP, Black SE, Lang AE. et al. Imaging biomarkers in Parkinson’s disease and Parkinsonian syndromes: Current and emerging concepts. Transl Neurodegener 2017; 6: 8-8 https://doi.org/10.1186/s40035-017-0076-6
- 13 Greene P. Progressive supranuclear palsy, corticobasal degeneration, and multiple system atrophy. Continuum (Minneap Minn) 2019; 25 (04) 919-935 https://doi.org/10.1212/con.2022s1302022s1300751
- 14 Whitwell JL, Höglinger GU, Antonini A, Bordelon Y, Boxer AL, Colosimo C. et al. Radiological biomarkers for diagnosis in PSP: Where are we and where do we need to be?. Mov Disord 2017; 32 (07) 955-971 https://doi.org/10.1002/mds.27038
- 15 Mueller C, Hussl A, Krismer F, Heim B, Mahlknecht P, Nocker M. et al. The diagnostic accuracy of the hummingbird and morning glory sign in patients with neurodegenerative parkinsonism. Parkinsonism Relat Disord 2018; 54: 90-94 https://doi.org/10.1016/j.parkreldis.2018.04.005
- 16 Quattrone A, Nicoletti G, Messina D, Fera F, Condino F, Pugliese P. et al. MR imaging index for differentiation of progressive supranuclear palsy from Parkinson disease and the Parkinson variant of multiple system atrophy. Radiology 2008; 246 (01) 214-221 https://doi.org/10.1148/radiol.2453061703
- 17 Saeed U, Lang AE, Masellis M. Neuroimaging advances in Parkinson’s Disease and atypical Parkinsonian syndromes. Front Neurol 2020; 11 https://doi.org/10.3389/fneur.2020.572976
- 18 Boxer AL, Geschwind MD, Belfor N, Gorno-Tempini ML, Schauer GF, Miller BL. et al. Patterns of brain atrophy that differentiate corticobasal degeneration syndrome from progressive supranuclear palsy. Arch Neurol 2006; 63 (01) 81-86 https://doi.org/10.1001/archneur.63.1.81
- 19 Fanciulli A, Wenning GK. Multiple-System Atrophy. N Engl J Med 2015; 372 (03) 249-263 https://doi.org/10.1056/nejmra1311488
- 20 Massey LA, Micallef C, Paviour DC, O'Sullivan SS, Ling H, Williams DR. et al. Conventional magnetic resonance imaging in confirmed progressive supranuclear palsy and multiple system atrophy. Mov Disord 2012; 27 (14) 1754-1762 https://doi.org/10.1002/mds.24968
- 21 Kalia LV, Lang AE. Parkinson’s disease. Lancet 2015; 386 9996 896-912 https://doi.org/10.1016/s0140-6736(14)61393-3
- 22 Damier P, Hirsch EC, Agid Y, Graybiel AM. The substantia nigra of the human brain. II. Patterns of loss of dopamine-containing neurons in Parkinson's disease. Brain 1999; 122 (08) 1437-1448 https://doi.org/10.1093/brain/122.8.1437
- 23 Schwarz ST, Afzal M, Morgan PS, Bajaj N, Gowland PA, Auer DP. The “swallow tail” appearance of the healthy nigrosome - A new accurate test of Parkinson’s disease: A case-control and retrospective cross-sectional MRI study at 3T. PLoS One 2014; 9 (04) e93814 https://doi.org/10.1371/journal.pone.0093814
- 24 Liu X, Wang N, Chen C, Wu P-Y, Piao S, Geng D. et al. Swallow tail sign on susceptibility map-weighted imaging (SMWI) for disease diagnosing and severity evaluating in parkinsonism. Acta Radiol 2021; 62 (02) 234-242 https://doi.org/10.1177/0284185120920793
- 25 Mochizuki H, Choong CJ, Baba K. Parkinson’s disease and iron. J Neural Transm (Vienna) 2020; 127 (02) 181-187 https://doi.org/10.1007/s00702-020-02149-3
- 26 Dexter DT, Wells FR, Lees AJ, Agid F, Agid Y, Jenner P. et al. Increased nigral iron content and alterations in other metal ions occurring in brain in Parkinson's disease. J Neurochem 1989; 52 (06) 1830-1836 https://doi.org/10.1111/j.1471-4159.1989.tb07264.x
- 27 Mitchell T, Lehéricy S, Chiu SY, Strafella AP, Stoessl AJ, Vaillancourt DE. Emerging neuroimaging biomarkers across disease stage in Parkinson Disease: A review. JAMA Neurol 2021; 78 (10) 1262-1272 https://doi.org/10.1001/jamaneurol.2021.1312
- 28 Mahlknecht P, Krismer F, Poewe W, Seppi K. Meta-analysis of dorsolateral nigral hyperintensity on magnetic resonance imaging as a marker for Parkinson’s disease. Mov Disord 2017; 32 (04) 619-623 https://doi.org/10.1002/mds.26932
- 29 Reiter E, Mueller C, Pinter B, Krismer F, Scherfler C, Esterhammer R. et al. Dorsolateral nigral hyperintensity on 3.0T susceptibility-weighted imaging in neurodegenerative Parkinsonism. Mov Disord 2015; 30 (08) 1068-1076
- 30 Oh SW, Shin N-Y, Lee JJ, Lee S-K, Lee PH, Lim SM. et al. Correlation of 3D FLAIR and dopamine transporter imaging in patients with parkinsonism. AJR Am J Roentgenol 2016; 207 (05) 1089-1094 https://doi.org/10.2214/ajr.16.16092
- 31 Bae YJ, Kim JM, Kim E, Lee KM, Kang SY, Park HS. et al. Loss of Nigral Hyperintensity on 3 Tesla MRI of Parkinsonism: Comparison with 123I-FP-CIT SPECT. Mov Disord 2016; 31 (05) 684-692 https://doi.org/10.1002/mds.26584
- 32 Du G, Lewis MM, Sica C, He L, Connor JR, Kong L. et al. Distinct progression pattern of susceptibility MRI in the substantia nigra of Parkinson’s patients. Mov Disord 2018; 33 (09) 1423-1431 https://doi.org/10.1002/mds.27318
- 33 Sun J, Lai Z, Ma J, Gao L, Chen M, Chen J. et al. Quantitative evaluation of iron content in idiopathic rapid eye movement sleep behavior disorder. Mov Disord 2020; 35 (03) 478-485 https://doi.org/10.1002/mds.27929
- 34 Du G, Lewis MM, Sica C, He L, Connor JR, Kong L. et al. Distinct progression pattern of susceptibility MRI in the substantia nigra of Parkinson’s patients. Mov Disord 2018; 33 (09) 1423-1431 https://doi.org/10.1002/mds.27318
- 35 Martin-Bastida A, Pietracupa S, Piccini P. Neuromelanin in parkinsonian disorders: An update. Int J Neurosci 2017; 127 (12) 1116-1123 https://doi.org/10.1080/00207454.2017.1325883
- 36 Zucca FA, Segura-Aguilar J, Ferrari E, Muñoz P, Paris I, Sulzer D. et al. Interactions of iron, dopamine and neuromelanin pathways in brain aging and Parkinson’s disease. Prog Neurobiol 2017; 155: 96-119 https://doi.org/10.1016/j.pneurobio.2015.09.012
- 37 Nakamura K, Sugaya K. Neuromelanin-sensitive magnetic resonance imaging: A promising technique for depicting tissue characteristics containing neuromelanin. Neural Regen Res 2014; 9 (07) 759-760 https://doi.org/10.4103/1673-5374.131583
- 38 Gaurav R, Yahia-Cherif L, Pyatigorskaya N, Mangone G, Biondetti E, Valabrègue R. et al. Longitudinal changes in Neuromelanin MRI Signal in Parkinson’s Disease: A progression marker. Mov Disord 2021; 36 (07) 1592-1602 https://doi.org/10.1002/mds.28531
- 39 Pavese N, Tai YF. Nigrosome imaging and neuromelanin sensitive MRI in diagnostic evaluation of Parkinsonism. Mov Disord Clin Pract 2018; 5 (02) 131-140 https://doi.org/10.1002/mdc3.12590
- 40 Vila M. Neuromelanin, aging, and neuronal vulnerability in Parkinson’s disease. Mov Disord 2019; 34 (10) 1440-1451 https://doi.org/10.1002/mds.27776
- 41 Ohtsuka C, Sasaki M, Konno K, Koide M, Kato K, Takahashi J. et al. Changes in substantia nigra and locus coeruleus in patients with early-stage Parkinson’s disease using neuromelanin-sensitive MR imaging. Neurosci Lett 2013; 541: 93-98 https://doi.org/10.1016/j.neulet.2013.02.012
- 42 Ohtsuka C, Sasaki M, Konno K, Kato K, Takahashi J, Yamashita F. et al. Differentiation of early-stage parkinsonisms using neuromelanin-sensitive magnetic resonance imaging. Parkinsonism Relat Disord 2014; 20 (07) 755-760 https://doi.org/10.1016/j.parkreldis.2014.04.005
- 43 Taniguchi D, Hatano T, Kamagata K, Okuzumi A, Oji Y, Mori A. et al. Neuromelanin imaging and midbrain volumetry in progressive supranuclear palsy and Parkinson’s disease. Mov Disord 2018; 33 (09) 1488-1492 https://doi.org/10.1002/mds.27365
- 44 Isaias IU, Trujillo P, Summers P, Marotta G, Mainardi L, Pezzoli G. et al. Neuromelanin imaging and dopaminergic loss in parkinson’s disease. Front Aging Neurosci 2016; 8: 196-196 https://doi.org/10.3389/fnagi.2016.00196
- 45 Vaillancourt DE, Spraker MB, Prodoehl J, Abraham I, Corcos DM, Zhou XJ. et al. High-resolution diffusion tensor imaging in the substantia nigra of de novo Parkinson disease. Neurology 2009; 72 (16) 1378-1384 https://doi.org/10.1212/01.wnl.0000340982.01727.6e
- 46 Cochrane CJ, Ebmeier KP. Diffusion tensor imaging in parkinsonian syndromes: A systematic review and meta-analysis. Neurology 2013; 80 (09) 857-864 https://doi.org/10.1212/wnl.0b013e318284070c
- 47 Rolheiser TM, Fulton HG, Good KP, Fisk JD, McKelvey JR, Scherfler C. et al. Diffusion tensor imaging and olfactory identification testing in early-stage Parkinson’s disease. J Neurol 2011; 258 (07) 1254-1260 https://doi.org/10.1007/s00415-011-5915-2
- 48 Boelmans K, Bodammer NC, Suchorska B, Kaufmann J, Ebersbach G, Heinze H-J. et al. Diffusion tensor imaging of the corpus callosum differentiates corticobasal syndrome from Parkinson’s disease. Parkinsonism Relat Disord 2010; 16 (08) 498-502 https://doi.org/10.1016/j.parkreldis.2010.05.006
- 49 Loane C, Politis M, Kefalopoulou Z, Valle-Guzman N, Paul G, Widner H. et al. Aberrant nigral diffusion in Parkinson’s disease: A longitudinal diffusion tensor imaging study. Mov Disord 2016; 31 (07) 1020-1026 https://doi.org/10.1002/mds.26606
- 50 Burciu RG, Ofori E, Archer DB, Wu SS, Pasternak O, McFarland NR. et al. Progression marker of Parkinson’s disease: A 4-year multi-site imaging study. Brain 2017; 140 (08) 2183-2192 https://doi.org/10.1093/brain/awx146
- 51 Bajaj S, Krismer F, Palma JA, Wenning GK, Kaufmann H, Poewe W. et al. Diffusion-weighted MRI distinguishes Parkinson disease from the parkinsonian variant of multiple system atrophy: A systematic review and meta-analysis. PLoS One 2017; 12 (12) e0189897 https://doi.org/10.1371/journal.pone.0189897
- 52 Archer DB, Bricker JT, Chu WT, Burciu RG, McCracken JL, Lai S. et al. Development and validation of the automated imaging differentiation in parkinsonism (AID-P): A multicentre machine learning study. Lancet Digit Health 2019; 1 (05) 222-231 https://doi.org/10.1016/s2589-7500(19)30105-0
- 53 Palermo G, Ceravolo R. Molecular imaging of the dopamine transporter. Cells 2019; 8 (08) 872 https://doi.org/10.3390/cells8080872
- 54 Mulvihill KG. Presynaptic regulation of dopamine release: Role of the DAT and VMAT2 transporters. Neurochem Int 2019; 122: 94-105 https://doi.org/10.1016/j.neuint.2018.11.004
- 55 Tatsch K, Poepperl G. Nigrostriatal dopamine terminal imaging with dopamine transporter SPECT: An update. J Nucl Med 2013; 54 (08) 1331-1338 https://doi.org/10.2967/jnumed.112.105379
- 56 Thobois S, Prange S, Scheiber C, Broussolle E. What a neurologist should know about PET and SPECT functional imaging for parkinsonism: A practical perspective. Parkinsonism Relat Disord 2019; 59: 93-100 https://doi.org/10.1016/j.parkreldis.2018.08.016
- 57 Bajaj N, Hauser RA, Grachev ID. Clinical utility of dopamine transporter single photon emission CT (DaT-SPECT) with (123I) ioflupane in diagnosis of parkinsonian syndromes. J Neurol Neurosurg Psychiatry 2013; 84 (11) 1288-1295 https://doi.org/10.1136/jnnp-2012-304436
- 58 Tatsch K, Poepperl G. Nigrostriatal dopamine terminal imaging with dopamine transporter SPECT: An update. J Nucl Med 2013; 54 (08) 1331-1338 https://doi.org/10.2967/jnumed.112.105379
- 59 Oh M, Kim JS, Kim JY, Shin K-H, Park SH, Kim HO. et al. Subregional patterns of preferential striatal dopamine transporter loss differ in Parkinson disease, progressive supranuclear palsy, and multiple-system atrophy. J Nucl Med 2012; 53 (03) 399-406 https://doi.org/10.2967/jnumed.111.095224
- 60 Tatsch K, Poepperl G. Nigrostriatal dopamine terminal imaging with dopamine transporter SPECT: An update. J Nucl Med 2013; 54 (08) 1331-1338 https://doi.org/10.2967/jnumed.112.105379
- 61 Utiumi MA, Felício AC, Borges CR, Braatz VL, Rezende SAS, Munhoz RP. et al. Dopamine transporter imaging in clinically unclear cases of parkinsonism and the importance of scans without evidence of dopaminergic deficit (SWEDDs). Arq Neuropsiquiatr 2012; 70 (09) 667-673 https://doi.org/10.1590/s0004-282x2012000900004
- 62 Erro R, Schneider SA, Stamelou M, Quinn NP, Bathia KP. What do patients with scans without evidence of dopaminergic deficit (SWEDD) have? New evidence and continuing controversies. J Neurol Neurosurg Psychiatry 2016; 87 (03) 319-323 https://doi.org/10.1136/jnnp-2014-310256
- 63 Iranzo A, Santamaría J, Valldeoriola F, Sarradell M, Salamero M, Gaig C. et al. Dopamine transporter imaging deficit predicts early transition to synucleinopathy in idiopathic rapid eye movement sleep behavior disorder. Ann Neurol 2017; 82 (03) 419-428 https://doi.org/10.1002/ana.25026
- 64 Jennings D, Siderowf A, Stern M, Seibyl J, Eberly S, Oakes D. et al. Conversion to Parkinson disease in the PARS hyposmic and dopamine transporter-deficit prodromal cohort. JAMA Neurol 2017; 74 (08) 933-940 https://doi.org/10.1001/jamaneurol.2017.0985
- 65 Horsager J, Andersen KB, Knudsen K, Fedorova TD, Okklels N. et al. Brain-first versus body-first Parkinson’s disease: A multimodal imaging case-control study. Brain 2020; 143 (10) 3077-3088 https://doi.org/10.1093/brain/awaa238
- 66 Berg D, Borghammer P, Fereshtehnejad SM, Heinzel S, Horsager J, Schaeffer E. et al. Prodromal Parkinson disease subtypes - key to understanding heterogeneity. Nat Rev Neurol 2021; 17 (06) 349-361 https://doi.org/10.1038/s41582-021-00486-9