Progressive supranuclear palsy: clinicopathological concepts and diagnostic challenges

Williams, David R; Lees, Andrew J

doi:10.1016/s1474-4422(09)70042-0

Cited by 650Parkinson's Disease Mechanisms and TreatmentsDementia and Cognitive Impairment ResearchAlzheimer's disease research and treatments

Progressive supranuclear palsy: clinicopathological concepts and diagnostic challenges

Williams, David R, Lees, Andrew J·2009·The Lancet Neurology

DOI 10.1016/s1474-4422(09)70042-0

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Abstract

Progressive supranuclear palsy (PSP) is a clinical syndrome comprising supranuclear palsy, postural instability, and mild dementia. Neuropathologically, PSP is defined by the accumulation of neurofibrillary tangles. Since the first description of PSP in 1963, several distinct clinical syndromes have been described that are associated with PSP; this discovery challenges the traditional clinicopathological definition and complicates diagnosis in the absence of a reliable, disease-specific biomarker. We review the emerging nosology in this field and contrast the clinical and pathological characteristics of the different disease subgroups. These new insights emphasise that the pathological events and processes that lead to the accumulation of phosphorylated tau protein in the brain are best considered as dynamic processes that can develop at different rates, leading to different clinical phenomena. Moreover, for patients for whom the diagnosis is unclear, clinicians must continue to describe accurately the clinical picture of each individual, rather than label them with inaccurate diagnostic categories, such as atypical parkinsonism or PSP mimics. In this way, the development of the clinical features can be informative in assigning less common nosological categories that give clues to the underlying pathology and an understanding of the expected clinical course.

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This association occurs in motor-related regions involved in the neuropathology and symptomatology of PSP.
“This association occurs in motor-related regions that are involved in the neuropathology and symptomatology of PSP (i.e. functional deficits, postural instability, and supranuclear gaze palsy) associated with PSP Richardson’s syndrome44.”
From Neuroinflammation and Tau Colocalize in vivo in Progressive Supranuclear Palsy (2020) · cites this paper as [44]

Frontotemporal lobar degeneration: A consensus on clinical diagnostic criteria
Neary, D., Snowden, J. S., Gustafson, L., Passant, U., Stuss, D., Black, S., Freedman, M., Kertesz, A., Robert, P. H., Albert, M., et al. (1998) · Neurology · doi:10.1212/wnl.51.6.1546 · Cited by 5,047 · see citing works
The Neurology of Eye Movements
Leigh, R. J., & Zee, D. S. (2015) · Oxford University Press eBooks · doi:10.1093/med/9780199969289.001.0001 · Cited by 3,829 · see citing works
Mutations in LRRK2 Cause Autosomal-Dominant Parkinsonism with Pleomorphic Pathology
Zimprich, A. A., Biskup, S., Leitner, P., Lichtner, P., Farrer, M. J., Lincoln, S., Kachergus, J. M., Hulihan, M., Uitti, R. J., Calne, D. B., et al. (2004) · Neuron · doi:10.1016/j.neuron.2004.11.005 · Cited by 3,024 · see citing works
Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome): Report of the NINDS-SPSP International Workshop*
Litvan, I., Agid, Y., Calne, D., Campbell, G., Dubois, B., Duvoisin, R. C., Goetz, C. G., Golbe, L. I., Grafman, J., Growdon, J. H., et al. (1996) · Neurology · doi:10.1212/wnl.47.1.1 · Cited by 2,538 · see citing works
Progressive Supranuclear Palsy
Steele, J. C. (1964) · Archives of Neurology · doi:10.1001/archneur.1964.00460160003001 · Cited by 1,930 · see citing works
Motor Speech Disorders: Substrates, Differential Diagnosis, and Management
Duffy, J. R. (1995) · Cited by 1,892 · see citing works
The accuracy of diagnosis of parkinsonian syndromes in a specialist movement disorder service
Hughes, A. J., Daniel, S. E., Ben‐Shlomo, Y., & Lees, A. J. (2002) · Brain · doi:10.1093/brain/awf080 · Cited by 1,250 · see citing works
Self-citation
Preliminary NINDS neuropathologic criteria for Steele‐Richardson‐Olszewski syndrome (progressive supranuclear palsy)
Hauw, J., Daniel, S. E., Dickson, D. W., Horoupian, D. S., Jellinger, K. A., Lantos, P. L., McKee, A. C., Tabaton, M., & Litvan, I. (1994) · Neurology · doi:10.1212/wnl.44.11.2015 · Cited by 854 · see citing works
Parkinson’s Disease and Movement Disorders
Tn, M., & Bhattacharyya, K. (2005) · Jaypee Brothers Medical Publishers (P) Ltd. eBooks · doi:10.5005/jp/books/10587 · Cited by 804 · see citing works
Characteristics of two distinct clinical phenotypes in pathologically proven progressive supranuclear palsy: Richardson's syndrome and PSP-parkinsonism
Williams, D. R., de Silva, R., Paviour, D. C., Pittman, A. M., Watt, H., Kilford, L., Holton, J. L., Révész, T., & Lees, A. J. (2005) · Brain · doi:10.1093/brain/awh488 · Cited by 733 · see citing works
Self-citation
Office of Rare Diseases Neuropathologic Criteria for Corticobasal Degeneration
Dickson, D. W., Bergeron, C., Chin, S. S., Duyckaerts, C., Horoupian, D., Ikeda, K., Jellinger, K., Lantos, P. L., Lippa, C. F., Mirra, S. S., et al. (2002) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/61.11.935 · Cited by 724 · see citing works
Clinicopathological and imaging correlates of progressive aphasia and apraxia of speech
Josephs, K. A. (2006) · Brain · doi:10.1093/brain/awl078 · Cited by 679 · see citing works
Prevalence of progressive supranuclear palsy and multiple system atrophy: a cross-sectional study
Schrag, A. E., Ben‐Shlomo, Y., & Quinn, N. P. (1999) · The Lancet · doi:10.1016/s0140-6736(99)04137-9 · Cited by 640 · see citing works
Parkinson's Disease and Movement Disorders
Kieburtz, K. D. (1994) · Archives of Neurology · doi:10.1001/archneur.1994.00540220013003 · Cited by 617 · see citing works
A clinical rating scale for progressive supranuclear palsy
Golbe, L. I., & Ohman‐Strickland, P. (2007) · Brain · doi:10.1093/brain/awm032 · Cited by 614 · see citing works
Clinicopathological correlates in frontotemporal dementia
Hodges, J. R., Davies, R. R., Xuereb, J. H., Casey, B., Broe, M., Bak, T. H., Kril, J. J., & Halliday, G. M. (2004) · Annals of Neurology · doi:10.1002/ana.20203 · Cited by 580 · see citing works
Heterogeneity of Parkinson's disease in the early clinical stages using a data driven approach
Lewis, S. J. G. (2005) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.2003.033530 · Cited by 547 · see citing works
THE NEUROLOGY OF EYE MOVEMENTS
Leigh, R. J., & Zee, D. S. (1984) · Optometry and Vision Science · doi:10.1097/00006324-198402000-00014 · Cited by 501 · see citing works
Validity and Reliability of the Preliminary NINDS Neuropathologic Criteria for Progressive Supranuclear Palsy and Related Disorders
Litvan, I., Hauw, J., Bartko, J. J., Lantos, P. L., Daniel, S. E., Horoupian, D. S., McKee, A. C., Dickson, D. W., Bancher, C., Tabaton, M., et al. (1996) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199601000-00010 · Cited by 474 · see citing works
Clinicopathologic analysis of frontotemporal and corticobasal degenerations and PSP
Josephs, K. A., Petersen, R. C., Knopman, D. S., Boeve, B. F., Whitwell, J. L., Duffy, J. R., Parisi, J. E., & Dickson, D. W. (2006) · Neurology · doi:10.1212/01.wnl.0000191307.69661.c3 · Cited by 455 · see citing works
Clinical outcomes of progressive supranuclear palsy and multiple system atrophy
O’Sullivan, S. S., Massey, L. A., Williams, D. R., Silveira‐Moriyama, L., Kempster, P. A., Holton, J. L., Révész, T., & Lees, A. J. (2008) · Brain · doi:10.1093/brain/awn065 · Cited by 423 · see citing works
Self-citation
Pathologic heterogeneity in clinically diagnosed corticobasal degeneration
Boeve, B. F., Maraganore, D. M., Parisi, J. E., Ahlskog, J. E., Graff-Radford, N., Caselli, R. J., Dickson, D. W., Kokmen, E., & Petersen, R. C. (1999) · Neurology · doi:10.1212/wnl.53.4.795 · Cited by 417 · see citing works
Pathological tau burden and distribution distinguishes progressive supranuclear palsy-parkinsonism from Richardson's syndrome
Williams, D. R., Holton, J. L., Strand, C., Pittman, A. M., de Silva, R., Lees, A. J., & Révész, T. (2007) · Brain · doi:10.1093/brain/awm104 · Cited by 415 · see citing works
Self-citation
Incidence of progressive supranuclear palsy and multiple system atrophy in Olmsted County, Minnesota, 1976 to 1990
Bower, J. H., Maraganore, D. M., McDonnell, S. K., et al. (1997) · Neurology · doi:10.1212/wnl.49.5.1284 · Cited by 400 · see citing works
Accuracy of clinical criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome)
Litvan, I., Agid, Y., Jankovic, J. J., Goetz, C. G., Brandel, J., Lai, E. C., Wenning, G. K., D'Olhaberriague, L., Verny, M., Chaudhuri, К. R., et al. (1996) · Neurology · doi:10.1212/wnl.46.4.922 · Cited by 347 · see citing works
Movement Disorders 2
Burnstine, T. H. (1988) · Neurology · doi:10.1212/wnl.38.8.1337 · Cited by 324 · see citing works
The Primate Thalamus Is a Key Target for Brain Dopamine
García‐Cabezas, M. Á., García‐Cabezas, M. Á., Rico, B., & Cavada, C. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0968-05.2005 · Cited by 320 · see citing works
Clinical features and natural history of progressive supranuclear palsy
Nath, U., Ben‐Shlomo, Y., Thomson, R., Lees, A. J., & Burn, D. J. (2003) · Neurology · doi:10.1212/01.wnl.0000052991.70149.68 · Cited by 282 · see citing works
Self-citation
The clinical and pathological spectrum of Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy): a reappraisal
Daniel, S. E., de Bruin, V. M. S., & Lees, A. J. (1995) · Brain · doi:10.1093/brain/118.3.759 · Cited by 276 · see citing works
Self-citation
Linkage disequilibrium fine mapping and haplotype association analysis of the tau gene in progressive supranuclear palsy and corticobasal degeneration
Pittman, A. M., Myers, A. J., Abou‐Sleiman, P. M., Fung, H., Kaleem, M., Marlowe, L., Duckworth, J., Leung, D. G., Williams, D. R., Kilford, L., et al. (2005) · Journal of Medical Genetics · doi:10.1136/jmg.2005.031377 · Cited by 275 · see citing works
Self-citation
Progressive supranuclear palsy pathology caused by a novel silent mutation in exon 10 of the tau gene
Stanford, P. M., Halliday, G. M., Brooks, W. S., Kwok, J. B. J., Storey, C. E., Creasey, H., Morris, J. G. L., Fulham, M. J., & Schofield, P. R. (2000) · Brain · doi:10.1093/brain/123.5.880 · Cited by 262 · see citing works
Tauopathies: classification and clinical update on neurodegenerative diseases associated with microtubule‐associated protein tau
Williams, D. R. (2006) · Internal Medicine Journal · doi:10.1111/j.1445-5994.2006.01153.x · Cited by 259 · see citing works
Self-citation
The prevalence of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome) in the UK
Nath, U. (2001) · Brain · doi:10.1093/brain/124.7.1438 · Cited by 253 · see citing works
Pure akinesia with gait freezing: A third clinical phenotype of progressive supranuclear palsy
Williams, D. R., Holton, J. L., Strand, K. M., Révész, T., & Lees, A. J. (2007) · Movement Disorders · doi:10.1002/mds.21698 · Cited by 240 · see citing works
Self-citation
The clinical features and natural history of the Steele‐Richardson‐Olszewski syndrome (progressive supranuclear palsy)
Maher, E. R., & Lees, A. J. (1986) · Neurology · doi:10.1212/wnl.36.7.1005 · Cited by 236 · see citing works
Self-citation
Mutations in progranulin (GRN) within the spectrum of clinical and pathological phenotypes of frontotemporal dementia
Swieten, J. C. V., & Heutink, P. (2008) · The Lancet Neurology · doi:10.1016/s1474-4422(08)70194-7 · Cited by 234 · see citing works
Pathological inclusion bodies in tauopathies contain distinct complements of tau with three or four microtubule‐binding repeat domains as demonstrated by new specific monoclonal antibodies
de Silva, R., Lashley, T., Gibb, G., Hanger, D. P., Hope, A., Reid, A. R., Bandopadhyay, R., Utton, M. A., Strand, C., Jowett, T. P., et al. (2003) · Neuropathology and Applied Neurobiology · doi:10.1046/j.1365-2990.2003.00463.x · Cited by 220 · see citing works
Self-citation
Predictors of falls and fractures in bradykinetic rigid syndromes: a retrospective study
Williams, D. R. (2006) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.2005.074070 · Cited by 203 · see citing works
Self-citation
An R5L τ mutation in a subject with a progressive supranuclear palsy phenotype
Poorkaj, P., Muma, N. A., Zhukareva, V. A., Cochran, E. J., Shannon, K. M., Hurtig, H. I., Koller, W. C., Bird, T. D., Trojanowski, J. Q., Lee, V. M. ‐., et al. (2002) · Annals of Neurology · doi:10.1002/ana.10340 · Cited by 196 · see citing works
Atypical progressive supranuclear palsy underlying progressive apraxia of speech and nonfluent aphasia
Josephs, K. A., Boeve, B. F., Duffy, J. R., Smith, G. E., Knopman, D. S., Parisi, J. E., Petersen, R. C., & Dickson, D. W. (2005) · Neurocase · doi:10.1080/13554790590963004 · Cited by 191 · see citing works
Accuracy of clinical diagnosis of progressive supranuclear palsy
Osaki, Y., Ben‐Shlomo, Y., Lees, A. J., Daniel, S. E., Colosimo, C., Wenning, G. K., & Quinn, N. P. (2003) · Movement Disorders · doi:10.1002/mds.10680 · Cited by 184 · see citing works
Self-citation
Progressive Supranuclear Palsy
Golbe, L. I. (2014) · Seminars in Neurology · doi:10.1055/s-0034-1381736 · Cited by 178 · see citing works
Dynamic properties of horizontal and vertical eye movements in parkinsonian syndromes
Rottach, K. G., Riley, D. E., DiScenna, A. O., Zivotofsky, A. Z., & Leigh, R. J. (1996) · Annals of Neurology · doi:10.1002/ana.410390314 · Cited by 177 · see citing works
Tau protein and neurodegeneration
Goedert, M. (2004) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2003.12.015 · Cited by 177 · see citing works
Frontal presentation in progressive supranuclear palsy
Kaat, L. D., Boon, A. J. W., Kamphorst, W., Ravid, R., Duivenvoorden, H. J., & Swieten, J. C. V. (2007) · Neurology · doi:10.1212/01.wnl.0000267643.24870.26 · Cited by 174 · see citing works
Corticodentatonigral degeneration with neuronal achromasia: a progressive disorder of late adult life.
Rebeiz, J. J., Kolodny, E. H., & Ep, R. (1967) · PubMed · Cited by 171 · see citing works
Guadeloupean parkinsonism: a cluster of progressive supranuclear palsy‐like tauopathy
Caparros-Lefebvre, D., Sergeant, N., Lees, A. J., Camuzat, A., Daniel, S. E., Lannuzel, A., Brice, A., TOLOSA, E. S., Delacourte, A., & Duyckaerts, C. J. (2002) · Brain · doi:10.1093/brain/awf086 · Cited by 169 · see citing works
Self-citation
Longitudinal ocular motor study in corticobasal degeneration and progressive supranuclear palsy
Rivaud-Péchoux, S., Vidailhet, M., Gallouëdec, G., Litvan, I., Gaymard, B. M., & Pierrot‐Deseilligny, C. (2000) · Neurology · doi:10.1212/wnl.54.5.1029 · Cited by 157 · see citing works
Clinical features differentiating patients with postmortem confirmed progressive supranuclear palsy and corticobasal degeneration
Litvan, I., Grimes, D. A., Lang, A. E., Jankovic, J. J., McKee, A. C., Verny, M., Jellinger, K. A., Chaudhuri, К. R., & Pearce, R. K. B. (1999) · Journal of Neurology · doi:10.1007/bf03161075 · Cited by 133 · see citing works
Progressive supranuclear palsy diagnosis and confounding features: Report on 16 autopsied cases
Birdi, S., Rajput, A., Fenton, M., Donat, J., Rozdilsky, B., Robinson, C., Macaulay, R., & George, D. (2002) · Movement Disorders · doi:10.1002/mds.10211 · Cited by 133 · see citing works
Increased tau burden in the cortices of progressive supranuclear palsy presenting with corticobasal syndrome
Tsuboi, Y., Josephs, K. A., Boeve, B. F., Litvan, I., Caselli, R. J., Caviness, J. N., Uitti, R. J., Bott, A. D., & Dickson, D. W. (2005) · Movement Disorders · doi:10.1002/mds.20478 · Cited by 129 · see citing works
Progressive supranuclear palsy
Santacruz, P., Uttl, B., Litvan, I., et al. (1998) · Neurology · doi:10.1212/wnl.50.6.1637 · Cited by 127 · see citing works
SUPRANUCLEAR OPHTHALMOPLEGIA, PSEUDOBULBAR PALSY, NUCHAL DYSTONIA AND DEMENTIA. A CLINICAL REPORT ON EIGHT CASES OF "HETEROGENOUS SYSTEM DEGENERATION".
Richardson, J. C., Steele, J. C., & Olszewski, J. (1963) · PubMed · Cited by 125 · see citing works
Progression of gait, speech and swallowing deficits in progressive supranuclear palsy
Goetz, C. G., Leurgans, S. E., Lang, A. E., et al. (2003) · Neurology · doi:10.1212/01.wnl.0000052686.97625.27 · Cited by 120 · see citing works
Using the presence of visual hallucinations to differentiate Parkinson's disease from atypical parkinsonism
Williams, D. R., Warren, J. D., & Lees, A. J. (2007) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.2007.124677 · Cited by 115 · see citing works
Self-citation
A NEUROVISCERAL STORAGE DISEASE WITH VERTICAL SUPRANUCLEAR OPHTHALMOPLEGIA, AND ITS RELATIONSHIP TO NIEMANN-PICK DISEASE
Neville, B. G. R., Lake, B. D., Stephens, R., et al. (1973) · Brain · doi:10.1093/brain/96.1.97 · Cited by 107 · see citing works
Clinical and neuropathologic features of progressive supranuclear palsy with severe pallido-nigro-luysial degeneration and axonal dystrophy
Ahmed, Z., Josephs, K. A., Gonzalez, J., DelleDonne, A., & Dickson, D. W. (2007) · Brain · doi:10.1093/brain/awm301 · Cited by 103 · see citing works
Alzheimer Disease: Clinical and Biological Heterogeneity
Friedland, R. P., Koss, E., Haxby, J. V., Grady, C. L., Luxenberg, J. S., Schapiro, M. B., & Kaye, J. A. (1988) · Annals of Internal Medicine · doi:10.7326/0003-4819-109-4-298 · Cited by 101 · see citing works
Neurodegeneration: The Molecular Pathology of Dementia and Movement Disorders
Dickson, D. W. (2011) · Wiley eBooks · doi:10.1002/9781444341256 · Cited by 92 · see citing works
Tau exon 10 +16 mutation FTDP-17 presenting clinically as sporadic young onset PSP
Morris, H. R., Osaki, Y., Holton, J. L., Lees, A. J., Wood, N. W., Révész, T., & Quinn, N. P. (2003) · Neurology · doi:10.1212/01.wnl.0000072325.27824.a5 · Cited by 92 · see citing works
Self-citation
Whipple's disease mimicking progressive supranuclear palsy: the diagnostic value of eye movement recording
Averbuch‐Heller, L., Paulson, G. W., Daroff, R. B., et al. (1999) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.66.4.532 · Cited by 90 · see citing works
Primary progressive freezing gait: A syndrome with many causes
Factor, S. A., Higgins, D. S., & Qian, J. X. (2006) · Neurology · doi:10.1212/01.wnl.0000196469.52995.ab · Cited by 88 · see citing works
Pathological, clinical and genetic heterogeneity in progressive supranuclear palsy
Morris, H. R., Gibb, G., Katzenschlager, R., Wood, N. W., Hanger, D. P., Strand, C., Lashley, T., Daniel, S. E., Lees, A. J., Anderton, B. H., et al. (2002) · Brain · doi:10.1093/brain/awf109 · Cited by 82 · see citing works
Self-citation
The syndrome of 'pure akinesia' and its relationship to progressive supranuclear palsy
Riley, D. E., Fogt, N., & Leigh, R. J. (1994) · Neurology · doi:10.1212/wnl.44.6.1025 · Cited by 81 · see citing works
Diffuse Lewy body disease presenting with a supranuclear gaze palsy.
Fearnley, J., Révész, T., Brooks, D. J., et al. (1991) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.54.2.159 · Cited by 80 · see citing works
Pathological heterogeneity in progressive supranuclear palsy and corticobasal degeneration
Wakabayashi, K., & Takahashi, H. (2004) · Neuropathology · doi:10.1111/j.1440-1789.2003.00543.x · Cited by 79 · see citing works
Functional brain imaging in pure akinesia with gait freezing: [18F] FDG PET and [18F] FP‐CIT PET analyses
Park, H. K., Kim, J. S., Im, K. C., et al. (2008) · Movement Disorders · doi:10.1002/mds.22347 · Cited by 67 · see citing works
A Clinicopathological Study of Vascular Progressive Supranuclear Palsy
Josephs, K. A., Ishizawa, T., Tsuboi, Y., et al. (2002) · Archives of Neurology · doi:10.1001/archneur.59.10.1597 · Cited by 63 · see citing works
Long lasting pure freezing of gait preceding progressive supranuclear palsy: A clinicopathological study
Compta, Y., Valldeoriola, F., TOLOSA, E. S., et al. (2007) · Movement Disorders · doi:10.1002/mds.21612 · Cited by 63 · see citing works
Different Tau Pathology Pattern in Two Clinical Phenotypes of Progressive Supranuclear Palsy
Jellinger, K. A. (2008) · Neurodegenerative Diseases · doi:10.1159/000121388 · Cited by 61 · see citing works
Corticobasal syndrome with tau pathology
Cordato, N. J., Halliday, G. M., McCann, H., Davies, L. W., Williamson, P., FULHAM, M. J., & Morris, J. G. (2001) · Movement Disorders · doi:10.1002/mds.1124 · Cited by 59 · see citing works
Procerus sign in progressive supranuclear palsy
Romano, S., & Colosimo, C. (2001) · Neurology · doi:10.1212/wnl.57.10.1928 · Cited by 59 · see citing works
The Prevalence of Parkinson’s Disease in an Area of North Tyneside in the North-East of England
Porter, B., Macfarlane, R., Unwin, N. C., & Walker, R. W. (2006) · Neuroepidemiology · doi:10.1159/000091657 · Cited by 58 · see citing works
Frontotemporal lobar degeneration with ubiquitin-only-immunoreactive neuronal changes: broadening the clinical picture to include progressive supranuclear palsy
Paviour, D. C. (2004) · Brain · doi:10.1093/brain/awh265 · Cited by 56 · see citing works
Distinct Pathological Features of the Gallyas- and Tau-positive Glia in the Parkinsonism-Dementia Complex and Amyotrophic Lateral Sclerosis of Guam
Oyanagi, K., Makifuchi, T., Ohtoh, T., et al. (1997) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199703000-00010 · Cited by 52 · see citing works
J. Clifford Richardson and 50 years of progressive supranuclear palsy
Williams, D. R., Lees, A. J., Wherrett, J. R., & Steele, J. C. (2008) · Neurology · doi:10.1212/01.wnl.0000286938.39473.0e · Cited by 52 · see citing works
Self-citation
The Saccadic System
Leigh, R. J., & Zee, D. S. (2015) · Oxford University Press eBooks · doi:10.1093/med/9780199969289.003.0004 · Cited by 52 · see citing works
Blink reflex elicited by auditory stimulation in the rabbit
Hori, A., Yasuhara, A., Naito, H., et al. (1986) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(86)90141-3 · Cited by 50 · see citing works
Progressive supranuclear palsy phenotype secondary to CADASIL
van Gerpen, J. A., Ahlskog, J. E., & Petty, G. W. (2003) · Parkinsonism & Related Disorders · doi:10.1016/s1353-8020(02)00146-3 · Cited by 50 · see citing works
Genetic linkage of autosomal dominant progressive supranuclear palsy to 1q31.1
Ros, R., Gómez‐Garre, P., Hirano, M., Tai, Y., Ampuero, I., Vidal, L., Rojo, A., Fontán, A., Vazquez, A., Fanjul, S., et al. (2005) · Annals of Neurology · doi:10.1002/ana.20449 · Cited by 49 · see citing works
Parkinson's Disease and Movement Disorders, 2nd Ed.
Al‐Hakim, M. (1994) · Neurology · doi:10.1212/wnl.44.3_part_1.587-b · Cited by 49 · see citing works
Syndrome resembling PSP after surgical repair of ascending aorta dissection or aneurysm
Mokri, B., Ahlskog, J. E., Fulgham, J. R., et al. (2004) · Neurology · doi:10.1212/01.wnl.0000115170.40838.9b · Cited by 48 · see citing works
Substantia Nigra in Progressive Supranuclear Palsy, Corticobasal Degeneration, and Parkinsonism-Dementia Complex of Guam: Specific Pathological Features
Oyanagi, K., Tsuchiya, K., Yamazaki, M., & Ikeda, K. (2001) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/60.4.393 · Cited by 46 · see citing works
How do patients with parkinsonism present? A clinicopathological study
Williams, D. R., & Lees, A. J. (2009) · Internal Medicine Journal · doi:10.1111/j.1445-5994.2008.01635.x · Cited by 44 · see citing works
Self-citation
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Supranuclear disturbances of ocular motility in Lytico‐Bodig
Lepore, F. E., Steele, J. C., Cox, T. A., et al. (1988) · Neurology · doi:10.1212/wnl.38.12.1849 · Cited by 41 · see citing works
Progressive supranuclear palsy presenting with pure akinesia.
Mizusawa, H., Mochizuki, A., Ohkoshi, N., Yoshizawa, K., Kanazawa, I., & Imai, H. (1993) · PubMed · Cited by 39 · see citing works
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“, 2012), (iv) late stage AD with high pathology scores of plaques and tangles, and (v) progressive supranuclear palsy (PSP), another neurodegenerative disorder of tauopathy (Williams and Lees, 2009).”
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Authors: Williams, D. R., & Lees, A. J.
Affiliations: University College London (GB)
National Hospital for Neurology and Neurosurgery (GB)
Corresponding author: Williams, David R
ORCID: Williams, David R
Lees, Andrew J
Venue: The Lancet Neurology
Publisher: Elsevier BV
Published: 2009-03
Volume: 8
Issue: 3
Pages: 270-279
ISSN: 1474-4422 (ISSN-L)
DOI: 10.1016/s1474-4422(09)70042-0
OpenAlex: W2156821098
Cited by: 650
References: 107
Citations by year: 2026: 30 · 2025: 26 · 2024: 36 · 2023: 33 · 2022: 32 · 2021: 26 · 2020: 43 · 2019: 40 · 2018: 30 · 2017: 58 · 2016: 50 · 2015: 47 · 2014: 45 · 2013: 31 · 2012: 36
FWCI: 4.57
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: The Lancet Neurology (publishedVersion)
PubMed (publishedVersion)
UCL Discovery (University College London) (submittedVersion)
Topics: Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Keywords: progressive supranuclear palsy, postural instability, mild dementia, neurofibrillary tangles, phosphorylated tau, disease classification, clinicopathological correlation, atypical parkinsonism, diagnostic challenges, disease biomarkers, clinical course
MeSH terms: Brain, Humans, Mutation, Supranuclear Palsy, Progressive, tau Proteins

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Progressive supranuclear palsy: clinicopathological concepts and diagnostic challenges

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