Magnetic Resonance Imaging in the Neuroimaging of Progressive Supranuclear Palsy—Parkinsonism Predominant: Limitations and Strengths in Clinical Evaluation
Abstract
:1. Introduction
2. Magnetic Resonance Imaging (MRI)
3. Discussion
4. Conclusions and Future Perspectives
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Badihian, N.; Tosakulwong, N.; Weigand, S.D.; Ali, F.; Clark, H.M.; Stierwalt, J.; Botha, H.; Savica, R.; Dickson, D.W.; Whitwell, J.L.; et al. Relationships between regional burden of tau pathology and age at death and disease duration in PSP. Parkinsonism Relat. Disord. 2024, 127, 107109. [Google Scholar] [CrossRef]
- Höglinger, G.U.; Respondek, G.; Stamelou, M.; Kurz, C.; Josephs, K.A.; Lang, A.E.; Mollenhauer, B.; Müller, U.; Nilsson, C.; Whitwell, J.L.; et al. Clinical diagnosis of progressive supranuclear palsy: The movement disorder society criteria. Mov. Disord. 2017, 32, 853–864. [Google Scholar] [CrossRef]
- Koziorowski, D.; Figura, M.; Milanowski, Ł.M.; Szlufik, S.; Alster, P.; Madetko, N.; Friedman, A. Mechanisms of Neurodegeneration in Various Forms of Parkinsonism-Similarities and Differences. Cells 2021, 10, 656. [Google Scholar] [CrossRef] [PubMed]
- Madetko-Alster, N.; Otto-Ślusarczyk, D.; Wiercińska-Drapało, A.; Koziorowski, D.; Szlufik, S.; Samborska-Ćwik, J.; Struga, M.; Friedman, A.; Alster, P. Clinical Phenotypes of Progressive Supranuclear Palsy-The Differences in Interleukin Patterns. Int. J. Mol. Sci. 2023, 24, 15135. [Google Scholar] [CrossRef] [PubMed]
- Alster, P.; Otto-Ślusarczyk, D.; Kutyłowski, M.; Migda, B.; Wiercińska-Drapało, A.; Jabłońska, J.; Struga, M.; Madetko-Alster, N. The associations between common neuroimaging parameters of Progressive Supranuclear Palsy in magnetic resonance imaging and non-specific inflammatory factors—Pilot study. Front. Immunol. 2024, 15, 1458713. [Google Scholar] [CrossRef] [PubMed]
- Couto, B.; Di Luca, D.G.; Antwi, J.; Bhakta, P.; Fox, S.; Tartaglia, M.C.; Kovacs, G.G.; Lang, A.E. Ethnic background and distribution of clinical phenotypes in patients with probable progressive supranuclear palsy. Parkinsonism Relat. Disord. 2024, 123, 106955. [Google Scholar] [CrossRef]
- Inci, I.; Kusbeci, O.Y.; Eskut, N. The neutrophil-to-lymphocyte ratio as a marker of peripheral inflammation in progressive supranuclear palsy: A retrospective study. Neurol. Sci. 2020, 41, 1233–1237. [Google Scholar] [CrossRef]
- Greten, S.; Wegner, F.; Jensen, I.; Krey, L.; Rogozinski, S.; Fehring, M.; Heine, J.; Doll-Lee, J.; Pötter-Nerger, M.; Zeitzschel, M.; et al. The comorbidity and co-medication profile of patients with progressive supranuclear palsy. J. Neurol. 2024, 271, 782–793. [Google Scholar] [CrossRef]
- Colosimo, C.; Osaki, Y.; Vanacore, N.; Lees, A.J. Lack of association between progressive supranuclear palsy and arterial hypertension: A clinicopathological study. Mov. Disord. 2003, 18, 694–697. [Google Scholar] [CrossRef]
- Koga, S.; Roemer, S.F.; Kasanuki, K.; Dickson, D.W. Cerebrovascular pathology presenting as corticobasal syndrome: An autopsy case series of “vascular CBS”. Parkinsonism Relat. Disord. 2019, 68, 79–84. [Google Scholar] [CrossRef]
- Wang, H.; Chang, T.S.; Dombroski, B.A.; Cheng, P.L.; Patil, V.; Valiente-Banuet, L.; Farrell, K.; Mclean, C.; Molina-Porcel, L.; Rajput, A.; et al. Whole-genome sequencing analysis reveals new susceptibility loci and structural variants associated with progressive supranuclear palsy. Mol. Neurodegener. 2024, 19, 61. [Google Scholar] [CrossRef]
- Jackson, R.J.; Melloni, A.; Fykstra, D.P.; Serrano-Pozo, A.; Shinobu, L.; Hyman, B.T. Astrocyte tau deposition in progressive supranuclear palsy is associated with dysregulation of MAPT transcription. Acta Neuropathol. Commun. 2024, 12, 132. [Google Scholar] [CrossRef] [PubMed]
- Kovacs, G.G.; Lukic, M.J.; Irwin, D.J.; Arzberger, T.; Respondek, G.; Lee, E.B.; Coughlin, D.; Giese, A.; Grossman, M.; Kurz, C.; et al. Distribution patterns of tau pathology in progressive supranuclear palsy. Acta Neuropathol. 2020, 140, 99–119. [Google Scholar] [CrossRef]
- Planche, V.; Mansencal, B.; Manjon, J.V.; Meissner, W.G.; Tourdias, T.; Coupé, P. Staging of progressive supranuclear palsy-Richardson syndrome using MRI brain charts for the human lifespan. Brain Commun. 2024, 6, fcae055. [Google Scholar] [CrossRef] [PubMed]
- Necpál, J.; Borsek, M.; Jeleňová, B. “Parkinson’s disease” on the way to progressive supranuclear palsy: A review on PSP-parkinsonism. Neurol. Sci. 2021, 42, 4927–4936. [Google Scholar] [CrossRef] [PubMed]
- Wen, Y.; Yang, Q.; Jiao, B.; Zhang, W.; Lin, J.; Zhu, Y.; Xu, Q.; Zhou, H.; Weng, L.; Liao, X.; et al. Clinical features of progressive supranuclear palsy. Front. Aging Neurosci. 2023, 15, 1229491. [Google Scholar] [CrossRef]
- Campagnolo, M.; Weis, L.; Fogliano, C.; Cianci, V.; Garon, M.; Fiorenzato, E.; Carecchio, M.; Ferreri, F.; Bisiacchi, P.; Antonini, A.; et al. Clinical, cognitive, and morphometric profiles of progressive supranuclear palsy phenotypes. J. Neural Transm. 2023, 130, 97–109. [Google Scholar] [CrossRef]
- Ebentheuer, J.; Canelo, M.; Trautmann, E.; Trenkwalder, C. Substantia nigra echogenicity in progressive supranuclear palsy. Mov. Disord. 2010, 25, 773–777. [Google Scholar] [CrossRef]
- Spiegel, C.; Marotta, C.; Bertram, K.; Vivash, L.; Harding, I.H. Brainstem and cerebellar radiological findings in progressive supranuclear palsy. Brain Commun. 2025, 7, fcaf051. [Google Scholar] [CrossRef]
- Watanabe, H.; Yoshida, M.; Naganawa, S.; Sobue, G. The diagnosis of neurodegenerative disorders based on clinical and pathological findings using an MRI approach. Rinsho Shinkeigaku 2011, 51, 863–864. [Google Scholar] [CrossRef]
- Longoni, G.; Agosta, F.; Kostić, V.S.; Stojković, T.; Pagani, E.; Stošić-Opinćal, T.; Filippi, M. MRI measurements of brainstem structures in patients with Richardson’s syndrome, progressive supranuclear palsy-parkinsonism, and Parkinson’s disease. Mov. Disord. 2011, 26, 247–255. [Google Scholar] [CrossRef] [PubMed]
- Hwang, M.; Yang, H.; Kim, Y.; Youn, J.; Park, J.; Huh, Y.E.; Kim, H.T.; Cho, J.W. Differential Progression of Midbrain Atrophy in Parkinsonism: Longitudinal MRI Study. Neurodegener. Dis. 2017, 17, 31–37. [Google Scholar] [CrossRef] [PubMed]
- Pasha, S.A.; Yadav, R.; Ganeshan, M.; Saini, J.; Gupta, A.; Sandhya, M.; Pal, P.K. Correlation between qualitative balance indices, dynamic posturography and structural brain imaging in patients with progressive supranuclear palsy and its subtypes. Neurol. India 2016, 64, 633–639. [Google Scholar] [CrossRef]
- Agosta, F.; Pievani, M.; Svetel, M.; Ječmenica Lukić, M.; Copetti, M.; Tomić, A.; Scarale, A.; Longoni, G.; Comi, G.; Kostić, V.S. Diffusion tensor MRI contributes to differentiate Richardson’s syndrome from PSP-parkinsonism. Neurobiol. Aging 2012, 33, 2817–2826. [Google Scholar] [CrossRef]
- Liscic, R.M.; Srulijes, K.; Gröger, A.; Maetzler, W.; Berg, D. Differentiation of progressive supranuclear palsy: Clinical, imaging and laboratory tools. Acta Neurol. Scand. 2013, 127, 362–370. [Google Scholar] [CrossRef]
- Quattrone, A.; Morelli, M.; Williams, D.R.; Vescio, B.; Arabia, G.; Nigro, S.; Nicoletti, G.; Salsone, M.; Novellino, F.; Nisticò, R.; et al. MR parkinsonism index predicts vertical supranuclear gaze palsy in patients with PSP-parkinsonism. Neurology 2016, 87, 1266–1273. [Google Scholar] [CrossRef]
- Yamawaki, T. Diagnosis of MSA-P and PSP-P in Early Stage. Brain Nerve 2020, 72, 331–343. [Google Scholar] [CrossRef]
- Picillo, M.; Tepedino, M.F.; Abate, F.; Erro, R.; Ponticorvo, S.; Tartaglione, S.; Volpe, G.; Frosini, D.; Cecchi, P.; Cosottini, M.; et al. Midbrain MRI assessments in progressive supranuclear palsy subtypes. J. Neurol. Neurosurg. Psychiatry 2020, 91, 98–103. [Google Scholar] [CrossRef] [PubMed]
- Quattrone, A.; Sarica, A.; Buonocore, J.; Morelli, M.; Bianco, M.G.; Calomino, C.; Aracri, F.; De Maria, M.; Vescio, B.; Vaccaro, M.G.; et al. Differentiating between common PSP phenotypes using structural MRI: A machine learning study. J. Neurol. 2023, 270, 5502–5515. [Google Scholar] [CrossRef]
- Quattrone, A.; Caligiuri, M.E.; Morelli, M.; Nigro, S.; Vescio, B.; Arabia, G.; Nicoletti, G.; Nisticò, R.; Salsone, M.; Novellino, F.; et al. Imaging counterpart of postural instability and vertical ocular dysfunction in patients with PSP: A multimodal MRI study. Parkinsonism Relat. Disord. 2019, 63, 124–130. [Google Scholar] [CrossRef]
- Whitwell, J.L.; Tosakulwong, N.; Clark, H.M.; Ali, F.; Botha, H.; Weigand, S.D.; Sintini, I.; Machulda, M.M.; Schwarz, C.G.; Reid, R.I.; et al. Diffusion tensor imaging analysis in three progressive supranuclear palsy variants. J. Neurol. 2021, 268, 3409–3420. [Google Scholar] [CrossRef]
- Quattrone, A.; Morelli, M.; Nigro, S.; Quattrone, A.; Vescio, B.; Arabia, G.; Nicoletti, G.; Nisticò, R.; Salsone, M.; Novellino, F.; et al. A new MR imaging index for differentiation of progressive supranuclear palsy-parkinsonism from Parkinson’s disease. Parkinsonism Relat. Disord. 2018, 54, 3–8. [Google Scholar] [CrossRef]
- Quattrone, A.; Bianco, M.G.; Antonini, A.; Vaillancourt, D.E.; Seppi, K.; Ceravolo, R.; Strafella, A.P.; Tedeschi, G.; Tessitore, A.; Cilia, R.; et al. Development and Validation of Automated Magnetic Resonance Parkinsonism Index 2.0 to Distinguish Progressive Supranuclear Palsy-Parkinsonism from Parkinson’s Disease. Mov. Disord. 2022, 37, 1272–1281. [Google Scholar] [CrossRef]
- Madetko, N.; Alster, P.; Kutyłowski, M.; Migda, B.; Nieciecki, M.; Koziorowski, D.; Królicki, L. Is MRPI 2.0 More Useful than MRPI and M/P Ratio in Differential Diagnosis of PSP-P with Other Atypical Parkinsonisms? J. Clin. Med. 2022, 11, 2701. [Google Scholar] [CrossRef] [PubMed]
- Alster, P.; Nieciecki, M.; Migda, B.; Kutyłowski, M.; Madetko, N.; Duszyńska-Wąs, K.; Charzyńska, I.; Koziorowski, D.; Królicki, L.; Friedman, A. The Strengths and Obstacles in the Differential Diagnosis of Progressive Supranuclear Palsy-Parkinsonism Predominant (PSP-P) and Multiple System Atrophy (MSA) Using Magnetic Resonance Imaging (MRI) and Perfusion Single Photon Emission Computed Tomography (SPECT). Diagnostics 2022, 12, 385. [Google Scholar] [CrossRef] [PubMed]
- Whitwell, J.L.; Tosakulwong, N.; Botha, H.; Ali, F.; Clark, H.M.; Duffy, J.R.; Utianski, R.L.; Stevens, C.A.; Weigand, S.D.; Schwarz, C.G.; et al. Brain volume and flortaucipir analysis of progressive supranuclear palsy clinical variants. Neuroimage Clin. 2020, 25, 102152. [Google Scholar] [CrossRef] [PubMed]
- Amrami, A.; Singh, N.A.; Ali, F.; Pham, N.T.T.; Stephens, Y.C.; Josephs, K.A.; Whitwell, J.L. Clinical Utility of Tectal Plate Measurements on Magnetic Resonance Imaging in Progressive Supranuclear Palsy. Mov. Disord. 2024, 39, 1402–1407. [Google Scholar] [CrossRef]
- Picillo, M.; Tepedino, M.F.; Abate, F.; Ponticorvo, S.; Erro, R.; Cuoco, S.; Oksuz, N.; Di Salle, G.; Di Salle, F.; Esposito, F.; et al. Uncovering clinical and radiological asymmetry in progressive supranuclear palsy-Richardson’s syndrome. Neurol. Sci. 2022, 43, 3677–3682. [Google Scholar] [CrossRef]
- Lenka, A.; Pasha, S.A.; Mangalore, S.; George, L.; Jhunjhunwala, K.R.; Bagepally, B.S.; Naduthota, R.M.; Saini, J.; Yadav, R.; Pal, P.K. Role of Corpus Callosum Volumetry in Differentiating the Subtypes of Progressive Supranuclear Palsy and Early Parkinson’s Disease. Mov. Disord. Clin. Pract. 2017, 4, 552–558. [Google Scholar] [CrossRef]
- Grijalva, R.M.; Pham, N.T.T.; Huang, Q.; Martin, P.R.; Ali, F.; Clark, H.M.; Duffy, J.R.; Utianski, R.L.; Botha, H.; Machulda, M.M.; et al. Brainstem Biomarkers of Clinical Variant and Pathology in Progressive Supranuclear Palsy. Mov. Disord. 2022, 37, 702–712. [Google Scholar] [CrossRef]
- Agosta, F.; Kostić, V.S.; Galantucci, S.; Mesaros, S.; Svetel, M.; Pagani, E.; Stefanova, E.; Filippi, M. The in vivo distribution of brain tissue loss in Richardson’s syndrome and PSP-parkinsonism: A VBM-DARTEL study. Eur. J. Neurosci. 2010, 32, 640–647. [Google Scholar] [CrossRef]
- Seki, M.; Seppi, K.; Mueller, C.; Potrusil, T.; Goebel, G.; Reiter, E.; Nocker, M.; Steiger, R.; Wildauer, M.; Gizewski, E.R.; et al. Diagnostic potential of dentatorubrothalamic tract analysis in progressive supranuclear palsy. Parkinsonism Relat. Disord. 2018, 49, 81–87. [Google Scholar] [CrossRef] [PubMed]
- Caso, F.; Agosta, F.; Ječmenica-Lukić, M.; Petrović, I.; Meani, A.; Kostic, V.S.; Filippi, M. Progression of white matter damage in progressive supranuclear palsy with predominant parkinsonism. Parkinsonism Relat. Disord. 2018, 49, 95–99. [Google Scholar] [CrossRef] [PubMed]
- Nigro, S.; Barbagallo, G.; Bianco, M.G.; Morelli, M.; Arabia, G.; Quattrone, A.; Gasparini, S.; Cascini, G.L.; Quattrone, A. Track density imaging: A reliable method to assess white matter changes in Progressive Supranuclear Palsy with predominant parkinsonism. Parkinsonism Relat. Disord. 2019, 69, 23–29. [Google Scholar] [CrossRef] [PubMed]
- Potrusil, T.; Krismer, F.; Beliveau, V.; Seppi, K.; Müller, C.; Troger, F.; Göbel, G.; Steiger, R.; Gizewski, E.R.; Poewe, W.; et al. Diagnostic potential of automated tractography in progressive supranuclear palsy variants. Parkinsonism Relat. Disord. 2020, 72, 65–71. [Google Scholar] [CrossRef]
- Beliveau, V.; Müller, C.; Steiger, R.; Gizewski, E.R.; Poewe, W.; Seppi, K.; Scherfler, C. Characterization and diagnostic potential of R2* in early-stage progressive supranuclear palsy variants. Parkinsonism Relat. Disord. 2022, 101, 43–48. [Google Scholar] [CrossRef]
- Mangalore, S.; Kumar, M.; Pal, P.; Saini, J.; Pasha, S.; Yadav, R. Role of Multivoxel MR Spectroscopy Progressive Supranuclear Palsy—A Preliminary Study. Neurol. India 2022, 70, 2388–2391. [Google Scholar] [CrossRef]
- Satoh, R.; Weigand, S.D.; Pham, N.T.T.; Ali, F.; Arani, A.; Senjem, M.L.; Jack, C.R., Jr.; Whitwell, J.L.; Josephs, K.A. Magnetic Susceptibility in Progressive Supranuclear Palsy Variants, Parkinson’s Disease, and Corticobasal Syndrome. Mov. Disord. 2023, 38, 2282–2290. [Google Scholar] [CrossRef]
- Kawazoe, M.; Koga, S.; Sekiya, H.; Josephs, K.A.; Graff-Radford, N.R.; Dickson, D.W. Disproportionately Enlarged Subarachnoid-Space Hydrocephalus on MRI in Pathologically Confirmed Progressive Supranuclear Palsy. Neurol. Clin. Pract. 2025, 15, e200431. [Google Scholar] [CrossRef]
- Georgiopoulos, C.; Papadimitriou, S.; Nyholm, D.; Kilander, L.; Löwenmark, M.; Fällmar, D.; Virhammar, J. Quantitative brain stem assessment in discriminating neurodegenerative disorders from normal pressure hydrocephalus. J. Neuroimaging 2024, 34, 612–618. [Google Scholar] [CrossRef]
- Alster, P.; Otto-Ślusarczyk, D.; Szlufik, S.; Duszyńska-Wąs, K.; Drzewińska, A.; Wiercińska-Drapało, A.; Struga, M.; Kutyłowski, M.; Friedman, A.; Madetko-Alster, N. The significance of glial cell line-derived neurotrophic factor analysis in Progressive Supranuclear Palsy. Sci. Rep. 2024, 14, 2805. [Google Scholar] [CrossRef]
- Bianco, M.G.; Cristiani, C.M.; Scaramuzzino, L.; Sarica, A.; Augimeri, A.; Chimento, I.; Buonocore, J.; Parrotta, E.I.; Quattrone, A.; Cuda, G.; et al. Combined blood Neurofilament light chain and third ventricle width to differentiate Progressive Supranuclear Palsy from Parkinson’s Disease: A machine learning study. Parkinsonism Relat. Disord. 2024, 123, 106978. [Google Scholar] [CrossRef] [PubMed]
- Messerschmidt, K.; Barthel, H.; Brendel, M.; Scherlach, C.; Hoffmann, K.T.; Rauchmann, B.S.; Rullmann, M.; Marek, K.; Villemagne, V.L.; Rumpf, J.J.; et al. 18F-PI-2620 Tau PET Improves the Imaging Diagnosis of Progressive Supranuclear Palsy. J. Nucl. Med. 2022, 63, 1754–1760. [Google Scholar] [CrossRef]
- Gerhard, A.; Trender-Gerhard, I.; Turkheimer, F.; Quinn, N.P.; Bhatia, K.P.; Brooks, D.J. In vivo imaging of microglial activation with [11C](R)-PK11195 PET in progressive supranuclear palsy. Mov. Disord. 2006, 21, 89–93. [Google Scholar] [CrossRef] [PubMed]
- Choi, J.H.; Kim, H.; Shin, J.H.; Lee, J.Y.; Kim, H.J.; Kim, J.M.; Jeon, B. Eye movements and association with regional brain atrophy in clinical subtypes of progressive supranuclear palsy. J. Neurol. 2021, 268, 967–977. [Google Scholar] [CrossRef]
Entity Differentiated with PSP-P | Significance in MRI |
---|---|
PD |
|
PSP-RS |
|
MSA-P | Midbrain to pons ratio MRPI |
Other | Spectroscopy with PSP-C |
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Alster, P.; Kutyłowski, M.; Madetko-Alster, N. Magnetic Resonance Imaging in the Neuroimaging of Progressive Supranuclear Palsy—Parkinsonism Predominant: Limitations and Strengths in Clinical Evaluation. Diagnostics 2025, 15, 945. https://doi.org/10.3390/diagnostics15080945
Alster P, Kutyłowski M, Madetko-Alster N. Magnetic Resonance Imaging in the Neuroimaging of Progressive Supranuclear Palsy—Parkinsonism Predominant: Limitations and Strengths in Clinical Evaluation. Diagnostics. 2025; 15(8):945. https://doi.org/10.3390/diagnostics15080945
Chicago/Turabian StyleAlster, Piotr, Michał Kutyłowski, and Natalia Madetko-Alster. 2025. "Magnetic Resonance Imaging in the Neuroimaging of Progressive Supranuclear Palsy—Parkinsonism Predominant: Limitations and Strengths in Clinical Evaluation" Diagnostics 15, no. 8: 945. https://doi.org/10.3390/diagnostics15080945
APA StyleAlster, P., Kutyłowski, M., & Madetko-Alster, N. (2025). Magnetic Resonance Imaging in the Neuroimaging of Progressive Supranuclear Palsy—Parkinsonism Predominant: Limitations and Strengths in Clinical Evaluation. Diagnostics, 15(8), 945. https://doi.org/10.3390/diagnostics15080945