The role of magnetic resonance imaging in the diff erential diagnosis of Parkinson’s disease
https://doi.org/10.30629/26587947-2023-28-1-5-12
Abstract
Parkinson’s disease (PD) is one of the most common neurodegenerative diseases in the world. While until recently MRI was used exclusively for the diagnosis of symptomatic forms of parkinsonism, recent advances in neuroimaging allow the detection of signs of nigral degeneration (MR biomarkers of PD). The article discusses the possibilities of modern MRI modes sensitive to iron (SWI, T2*) and neuromelanin (neuromelanin-sensitive MRI); emphasis is placed on identifying false-negative and false-positive results of the study. The imaging of nigrosome-1 in the dorsal substantia nigra (SN) in MRI-SWI has been discussed since 2013. In the absence of nigral degeneration, this area is defi ned as a hyperintense ovoid area within the dorsolateral border of the hypointense SN (“swallow’s tail” sign). If the optimistic results of the fi rst studies testifi ed to the high sensitivity and specifi city of this technique in PD (the absence of the “swallow’s tail” sign), then in subsequent studies, similar changes were detected in patients with other neurodegenerations with parkinsonism. In addition, the diagnostic value of this technique occurs when using tomographs with a magnetic fi eld strength of at least 3 Tc. Similar conclusions can be drawn about the use of neuromelanin-sensitive MRI, since it is necessary to use high-fi eld magnetic tomographs of 3 Tc or more to detect nigral degeneration, and results similar to PD can also be found in atypical forms of parkinsonism. However, the search for signs of nigral degeneration may be useful in the diff erential diagnosis of PD and non-neurodegenerative disorders. In addition to MRI in the diagnosis of PD, the article discusses neuroimaging in various types of multisystem atrophy, progressive supranuclear palsy, and dementia with Lewy bodies. The article is illustrated with own MRI scans of the brains of patients with PD and other forms of parkinsonism.
About the Authors
A. A. TappakhovRussian Federation
Tаppakhov Alexey A.
Yakutsk
T. E. Popova
Russian Federation
Yakutsk
References
1. Pringsheim T., Jette N., Frolkis A., Steeves T. The prevalence of Parkinson’s disease: a systematic review and meta-analysis. Mov Disord. 2014;29(13):1583–1590. https://www.doi.org/10.1002/mds.25945
2. Levin O.S., Dokadina L.V. Epidemiology of parkinsonism and Parkinson’s disease. Neurological journal (Nevrologicheskiy zhurnal). 2005;(5):41–49. (In Russ.)].
3. Sapronova M.R., Shnayder N.A. Epidemiological and clinical-genetic characteristics of Parkinson’s disease (on the example of Zheleznogorsk). Neurology, neuropsychiatry, psychosomatics (Nevrologiya, neiropsikhiatriya, psikhosomatika). 2014;4(4):59–64. (In Russ.)].
4. Balestrino R., Schapira A.H.V. Parkinson disease. Eur J Neurol. 2020;27(1):27–42. https://www.doi.org/10.1111/ene.14108
5. Tolosa E., Garrido A., Scholz S.W., Poewe W. Challenges in the diagnosis of Parkinson’s disease. Lancet Neurol. 2021;20(5):385–397. https://www.doi.org/10.1016/S1474-4422(21)00030-2
6. Hughes A.J., Daniel S.E., Ben-Shlomo Y., Lees A.J. The accuracy of diagnosis of parkinsonian syndromes in a specialist movement disorder service. Brain. 2002;125(Pt 4):861–870. http://www.ncbi.nlm.nih.gov/pubmed/11912118
7. Dickson D.W. Neuropathology of Parkinson disease. Parkinsonism Relat Disord. 2018;46:S30–S33. https://www.doi.org/10.1016/j.parkreldis.2017.07.033
8. Nemmi F., Sabatini U., Rascol O., Péran P. Neurobiology of Aging Parkinson’s disease and local atrophy in subcortical nuclei: insight from shape analysis. Neurobiol Aging. 2015;36(1):424–433. https://www.doi.org/10.1016/j.neurobiolaging.2014.07.010
9. Lehéricy S., Bardinet E., Poupon C., Vidailhet M., François C. 7 tesla magnetic resonance imaging: A closer look at substantia nigra anatomy in Parkinson’s disease. Mov Disord. 2014;29(13):1574–1581. https://www.doi.org/10.1002/mds.26043
10. Yi S.Y., Barnett B.R., Yu J.J. Advances in neurodegenerative and psychiatric imaging special feature: Review Article Preclinical neuroimaging of gene — environment interactions in psychiatric disease. Br J Radiol. 2019;92(20180885):1–10.
11. Damier P., Hirsch E.C., Agid Y., Graybiel A.M. The substantia nigra of the human brain. Brain. 1999;122(8):1437–1448. https://www.doi.org/10.1093/brain/122.8.1437
12. Blazejewska A.I., Schwarz S.T., Pitiot A., Stephenson M., Lowe J., Bajaj N., Bowrell R., Auer D., Gowland P. Visualization of nigrosome 1 and its loss in PD: Pathoanatomical correlation and in vivo 7 T MRI. Neurology. 2013;81(6):534–540. https://www.doi.org/10.1212/WNL.0b013e31829e6fd2
13. Schwarz S.T., Afzal M., Morgan P.S., Bajaj N., Gowland P.A., Auer D.P. 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(4). https://www.doi.org/10.1371/journal.pone.0093814
14. Bae Y.J., Kim J.M., Kim E., Lee K., Kang S., Park H., Kim K. Loss of Nigral Hyperintensity on 3 Tesla MRI of Parkinsonism: Comparison With 123I-FP-CIT SPECT. Mov Disord. 2016;31(5):684–692. https://www.doi.org/10.1002/mds.26584
15. Reiter E., Mueller C., Pinter B. Dorsolateral nigral hyperintensity on 3.0T susceptibility-weighted imaging in neurodegenerative Parkinsonism. Mov Disord. 2015;30(8):1068–1076. https://www.doi.org/10.1002/mds.26171
16. 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(4):619–623. https://www.doi.org/10.1002/mds.26932
17. De Marzi R., Seppi K., Högl B., Müller C., Scherfl er C., Stefani A. Loss of dorsolateral nigral hyperintensity on 3.0 tesla susceptibility-weighted imaging in idiopathic rapid eye movement sleep behavior disorder. Ann Neurol. 2016;79(6):1026–1030. https://www.doi.org/10.1002/ana.24646
18. Martin-Bastida A., Pietracupa S., Piccini P. Neuromelanin in parkinsonian disorders: an update. Int J Neurosci. 2017;127(12):1116–1123. https://www.doi.org/10.1080/00207454.2017.1325883
19. Zecca L., Swartz H.M. Total and paramagnetic metals in human substantia nigra and its neuromelanin. J Neural Transm — Park Dis Dement Sect. 1993;5(3):203–213. https://www.doi.org/10.1007/BF02257675
20. Zecca L., Tampellini D., Gerlach M., Riederer P., Fariello R.G., Sulzer D. Substantia nigra neuromelanin: structure, synthesis, and molecular behaviour. Mol Pathol. 2001;54(6):414–418. http://www.ncbi.nlm.nih.gov/pubmed/11724917
21. Kubis N., Faucheux B.A., Ransmayr G. Preservation of midbrain catecholaminergic neurons in very old human subjects. Brain. 2000;123(2):366–373. https://www.doi.org/10.1093/ brain/123.2.366
22. Pakkenberg B., Moller A., Gundersen H.J., Mouritzen Dam A., Pakkenberg H. The absolute number of nerve cells in substantia nigra in normal subjects and in patients with Parkinson’s disease estimated with an unbiased stereological method. J Neurol Neurosurg Psychiatry. 1991;54(1):30–33. https://www.doi.org/10.1136/jnnp.54.1.30
23. Sasaki M., Shibata E., Tohyama K. Neuromelanin magnetic resonance imaging of locus ceruleus and substantia nigra in Parkinson’s disease. Neuroreport. 2006;17(11):1215–1218. https://www.doi.org/10.1097/01.wnr.0000227984.84927.a7
24. Schwarz S.T., Rittman T., Gontu V., Morgan P.S., Bajaj N., Auer D.P. T1-weighted MRI shows stage-dependent substantia nigra signal loss in Parkinson’s disease. Mov Disord. 2011;26(9):1633–1638. https://www.doi.org/10.1002/mds.23722
25. Vitali P., Pan M.I., Palesi F. Substantia Nigra Volumetry with 3-T MRI in de Novo and Advanced Parkinson Disease. Radiology. 2020;296(2):401–410. https://www.doi.org/10.1148/radiol.2020191235
26. Kashihara K., Shinya T., Higaki F. Reduction of neuromelanin-positive nigral volume in patients with MSA, PSP and CBD. Intern Med. 2011;50(16):1683–1687. https://www.doi.org/10.2169/internalmedicine.50.5101
27. Matsuura K., Maeda M., Yata K. Ichiba Y., Yamaguchi T., Kanamary K., Tomimoto H. Neuromelanin magnetic resonance imaging in Parkinson’s disease and multiple system atrophy. Eur Neurol. 2013;70(1–2):70–77. https://www.doi.org/10.1159/000350291
28. Ohtsuka C., Sasaki M., Konno K., Kato K., Takahashi J., Yamashita F., Terayama Y. Diff erentiation of early-stage parkinsonisms using neuromelanin-sensitive magnetic resonance imaging. Parkinsonism Relat Disord. 2014;20(7):755–760. https://www.doi.org/10.1016/j.parkreldis.2014.04.005
29. Reimão S., Pita Lobo P., Neutel D. Substantia nigra neuromelanin-MR imaging diff erentiates essential tremor from Parkinson’s disease. Mov Disord. 2015;30(7):953–959. https://www.doi.org/10.1002/mds.26182
30. Illarioshkin S.N., Konovalov R.N., Fedotova E.Yu., Moskalenko A.N. New MRI techniques in the diagnosis of Parkinson’s disease: assessment of nigral degeneration. Annals of clinical and experimental neurology (Annaly klinicheskoy i eksperimental’noy nevrologii). 2019;13(4):77–84. (In Russ.)]. https://www.doi.org/10.25692/ACEN.2019.4.10
31. Postuma R.B., Berg D., Stern M., Poewe W., Olanow C., Oertel W., et al. MDS clinical diagnostic criteria for Parkinson’s disease. Mov Disord. 2015;30(12):1591–1601. https://www.doi.org/10.1002/mds.26424
32. Andreev M.N., Fedotova E.Yu., Illarioshkin S.N. Instrumental diagnostics of vegetative disorders in multisystem atrophy. Bulletin of the National Society for the Study of Parkinson’s Disease (Byulleten’ Natsional’nogo obshchestva po izucheniyu bolezni Parkinsona). 2022;2:8–12. (In Russ.)]. https://www.doi.org/10.24412/2226-079X-2022-12423
33. Fanciulli A., Wenning G.K. Multiple-System Atrophy. N Engl J Med. 2015;372(3):249–263. https://www.doi.org/10.1056/NEJMra1311488
34. Doronina O.B., Aftanas L.I., Doronina K.S. Heterogeneity of clinical manifestations and biomarkers of atypical parkinsonism. Nervous diseases (Nervnye bolezni). 2017;2:35–39. (In Russ.)].
35. Wenning G.K., Stankovic I., Vignatelli L., Fanciulli A., Calandra-Buonaura G., Seppi K. et al. The Movement Disorder Society Criteria for the Diagnosis of Multiple System Atrophy. Mov Disord. 2022;37(6):1131–1148. https://www.doi.org/10.1002/ mds.29005
36. Carré G., Dietemann J.L., Gebus O. Brain MRI of multiple system atrophy of cerebellar type: a prospective study with implications for diagnosis criteria. J Neurol. 2020;267(5):1269–1277. https://www.doi.org/10.1007/s00415-020-09702-w
37. Lee E.A., Cho H.I., Kim S.S., Lee W.Y. Comparison of magnetic resonance imaging in subtypes of multiple system atrophy. Parkinsonism Relat Disord. 2004;10(6):363–368. https://www.doi.org/10.1016/j.parkreldis.2004.04.008
38. Chelban V., Bocchetta M., Hassanein S., Haridy N.A., Houlden H., Rohrer J.D. An update on advances in magnetic resonance imaging of multiple system atrophy. J Neurol. 2019;266(4):1036–1045. https://www.doi.org/10.1007/s00415-018-9121-3
39. Aludin S., Schmill L.P.A. MRI Signs of Parkinson’s Disease and Atypical Parkinsonism. RoFo Fortschritte auf dem Gebiet der Rontgenstrahlen und der Bildgeb Verfahren. 2021;193(12):1403–1409. https://www.doi.org/10.1055/a-1460-8795
40. Saeed U., Compagnone J., Aviv R.I. Imaging biomarkers in Parkinson’s disease and Parkinsonian syndromes: Current and emerging concepts. Transl Neurodegener. 2017;6(1):1–25. https://www.doi.org/10.1186/s40035-017-0076-6
41. Deguchi K., Ikeda K., Kume K. Signifi cance of the hot-cross bun sign on T2*-weighted MRI for the diagnosis of multiple system atrophy. J Neurol. 2015;262(6):1433–1439. https://www.doi.org/10.1007/s00415-015-7728-1
42. Bogdanov R.R. Diff erential diagnosis of parkinsonism syndrome in clinical practice. Doctor.ru. 2014;6– 1(94):15–19. (In Russ.)].
43. Sako W., Murakami N., Izumi Y., Kaji R. The diff erence in putamen volume between MSA and PD: Evidence from a metaanalysis. Park Relat Disord. 2014;20(8):873–877. https://www.doi.org/10.1016/j.parkreldis.2014.04.028
44. Irwin D.J. Tauopathies as clinicopathological entities. Parkinsonism Relat Disord. 2016;22(01):S29–S33. https://www.doi.org/10.1016/j.parkreldis.2015.09.020
45. Höglinger G.U., Respondek G., Stamelou M. Clinical diagnosis of progressive supranuclear palsy: The movement disorder society criteria. Mov Disord. 2017;32(6):853–864. https://www.doi.org/10.1002/mds.26987
46. Respondek G., Stamelou M., Kurz C. The phenotypic spectrum of progressive supranuclear palsy: A retrospective multicenter study of 100 defi nite cases. Mov Disord. 2014;29(14):1758–1766. https://www.doi.org/10.1002/mds.26054
47. Ling H. Clinical Approach to Progressive Supranuclear Palsy. J Mov Disord. 2016;9(1):3–13. https://www.doi.org/10.14802/jmd.15060
48. Boxer A.L., Yu J.T., Golbe L.I., Litvan I., Lang A.E., Höglinger G.U. Advances in progressive supranuclear palsy: new diagnostic criteria, biomarkers, and therapeutic approaches. Lancet Neurol. 2017;16(7):552–563. https://www.doi.org/10.1016/S1474-4422(17)30157-6
49. Magzhanov R.V., Davletova A.I., Ibatullin R.A., Tunik V.F., Idrisova R.F., Bakhitiyarova K.Z. Diffi culties in the diff erential diagnosis of progressive supranuclear palsy and Parkinson’s disease. Annals of clinical and experimental neurology (Annaly klinicheskoy i eksperimental’noy nevrologii). 2016;10(4):58–61. (In Russ.)].
50. Gröschel K., Hauser T-K., Luft A. Magnetic resonance imagingbased volumetry diff erentiates progressive supranuclear palsy from corticobasal degeneration. Neuroimage. 2004;21(2):714–724. https://www.doi.org/10.1016/j.neuroimage.2003.09.070
51. Kurata T., Kametaka S., Ohta Y. PSP as distinguished from CBD, MSA-P and PD by clinical and imaging diff erences at an early stage. Intern Med. 2011;50(22):2775–2781. https://www.doi.org/10.2169/internalmedicine.50.5954
52. Mueller C., Hussl A., Krismer F. The diagnostic accuracy of the hummingbird and morning glory sign in patients with neurodegenerative parkinsonism. Parkinsonism Relat Disord. 2018;54:90–94. https://www.doi.org/10.1016/j.parkreldis.2018.04.005
53. Quattrone A, Morelli M, Nigro S,Quattrone An., Vescio B. Arabia G. et al. A new MR imaging index for diff erentiation of progressive supranuclear palsy-parkinsonism from Parkinson’s disease. Park Relat Disord. 2018;54:3–8. https://www.doi.org/10.1016/j.parkreldis.2018.07.016
54. Levin O.S., Vasenina E.E., Chimagomedova A.Sh., Dudchenko N.G. Dementia with Lewy bodies. Review of psychiatry and medical psychology (Obozrenie psikhiatrii i meditsinskoy psikhologii). 2018;(2):11– 21. (In Russ.)]. https://www.doi.org/10.31363/2313-7053-20182-11-21
55. Peraza L.R., Colloby S.J., Firbank M.J. Resting state in Parkinson’s disease dementia and dementia with Lewy bodies: commonalities and diff erences. Int J Geriatr Psychiatry. 2015;30:1135–1146. https://www.doi.org/10.1002/gps.4342
56. Bonanni L., Franciotti R., Pizzi S.D., Thomas A., Onofrj M. Lewy body dementia. Neurodegener Dis Clin Asp Mol Genet Biomarkers. 2018:297–312. https://www.doi.org/10.1007/978-3-319-72938-1_14
57. Barber R., Gholkar A., Scheltens P., Ballard C., McKeith I.G., O’Brien J.T. MRI volumetric correlates of white matter lesions in dementia with Lewy bodies and Alzheimer’s disease. Int J Geriatr Psychiatry. 2000;15(10):911–916. https://www.doi.org/10.1002/1099-1166(200010)15:10<911::aidgps217>3.0.co;2-t
58. Mak E., Su L., Williams G.B. Progressive cortical thinning and subcortical atrophy in dementia with Lewy bodies and Alzheimer’s disease. Neurobiol Aging. 2015;36(4):1743–1750. https://www.doi.org/10.1016/j.neurobiolaging.2014.12.038
59. Ballard C., O’Brien J., Barber B. Neurocardiovascular instability, hypotensive episodes, and MRI lesions in neurodegenerative dementia. Ann N Y Acad Sci. 2000;903:442–445. https://www.doi.org/10.1111/j.1749-6632.2000.tb06396.x
60. Shams S., Fällmar D., Schwarz S. MRI of the swallow tail sign: A useful marker in the diagnosis of lewy body dementia? Am J Neuroradiol. 2017;38(9):1737–1741. https://www.doi.org/10.3174/ajnr.A5274
Review
For citations:
Tappakhov A.A., Popova T.E. The role of magnetic resonance imaging in the diff erential diagnosis of Parkinson’s disease. Russian neurological journal. 2023;28(1):5-12. (In Russ.) https://doi.org/10.30629/26587947-2023-28-1-5-12