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01-05-2017 | Original Paper

Incipient progressive supranuclear palsy is more common than expected and may comprise clinicopathological subtypes: a forensic autopsy series

Authors: Koji Yoshida, Yukiko Hata, Koshi Kinoshita, Shutaro Takashima, Kortaro Tanaka, Naoki Nishida

Published in: Acta Neuropathologica | Issue 5/2017

Abstract

We investigated 998 serial Japanese forensic autopsy cases (0–101 years old, mean age 61.7 ± 21.9), with no case selection, using immunohistochemistry to detect cases with progressive supranuclear palsy (PSP). Twenty-nine cases (mean age 82.3 ± 7.2 years, 11 males, 18 females) fulfilled the National Institute of Neuronal Disorders and Stroke (NINDS)-PSP pathological criteria (2.9% of all cases, 4.6% of cases over 60). All had neuronal and glial inclusions in the basal ganglia and brainstem. However, 13 cases had low tau pathology and were categorized as atypical PSP. In addition to PSP pathology, multiple types of astrocytic inclusions and comorbid proteinopathies, particularly a high prevalence of argyrophilic grain disease, were found. All cases had not been diagnosed with PSP and had preserved daily functioning prior to death. However, 14 (48.3%), 11 (37.9%), and 16 (55.2%) cases showed signs of dementia, depressive state, and gait disturbance, respectively. Sixteen accidental death cases (55.2%), including from falls and getting lost, and 11 suicide cases (37.9%) appear to have a relationship with incipient PSP pathology. Cluster analysis using the distribution and amount of 4-repeat-tau pathology classified the cases into three subgroups: Group 1 (10 cases) had typical PSP pathology and seven cases (70.0%) had dementia as the most frequent symptom; Group 2 (7 cases) had significantly higher frequency of gait disorder (6 cases, 85.7%), and less neocortical tau pathology than Group 1; Group 3 (12 cases) had relatively mild PSP pathology and high argyrophilic grain burdens. Granular-shaped astrocytes were the dominant astrocytic inclusion in all cases. We conclude that in forensic cases incipient PSP occurs with a higher prevalence than expected. If these findings can be extrapolated to other population-based cohorts, PSP may be more common than previously thought.

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Armstrong RA, Lantos PL, Cairns NJ (2007) Progressive supranuclear palsy (PSP): a quantitative study of the pathological changes in cortical and subcortical regions of eight cases. J Neural Transm 114:1569–1577. doi:10.1007/s00702-007-0796-3 CrossRefPubMed

Baker M, Litvan I, Houlden H, Adamson J, Dickson D, Perez-Tur J, Hardy J, Lynch T, Bigio E, Hutton M (1999) Association of an extended haplotype in the tau gene with progressive supranuclear palsy. Hum Mol Genet 8:711–715. doi:10.1093/hmg/8.4.711 CrossRefPubMed

Bigio EH, Brown DF, White CL III (1999) Progressive supranuclear palsy with dementia: cortical pathology. J Neuropathol Exp Neurol 58:359–364. doi:10.1097/00005072-199904000-00006 CrossRefPubMed

Birdi S, Rajput AH, Fenton M, Donat JR, Rozdilsky B, Robinson C, Macaulay R, George D (2002) Progressive supranuclear palsy diagnosis and confounding features: report on 16 autopsied cases. Mov Disord 17:1255–1264. doi:10.1002/mds.10211 CrossRefPubMed

Bloise MC, Berardelli I, Roselli V, Pasquini M, Stirpe P, Colosimo C, Berardelli A, Fabbrini G (2014) Psychiatric disturbances in patients with progressive supranuclear palsy: a case–control study. Parkinsonism Relat Disord 20:965–968. doi:10.1016/j.parkreldis.2014.05.015 CrossRefPubMed

Botez G, Probst A, Ipsen S, Tolnay M (1999) Astrocytes expressing hyperphosphorylated tau protein without glial fibrillary tangles in argyrophilic grain disease. Acta Neuropathol 98:251–256. doi:10.1007/s004010051077 CrossRefPubMed

Bower JH, Maraganore DM, McDonnell SK, Rocca WA (1997) Incidence of progressive supranuclear palsy and multiple system atrophy in Olmsted County, Minnesota, 1976 to 1990. Neurology 49:1284–1288. doi:10.1212/WNL.49.5.1284 CrossRefPubMed

Braak H, Alafuzoff I, Arzberger T, Kretzschmar H, Del Tredici K (2006) Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol 112:389–404. doi:10.1007/s00401-006-0127-z CrossRefPubMedPubMedCentral

Braak H, Ghebremedhin E, Rüb U, Bratzke H, Del Tredici K (2004) Stages in the development of Parkinson’s disease-related pathology. Cell Tissue Res 318:121–134. doi:10.1007/s00441-004-0956-9 CrossRefPubMed

10.

Brenneis C, Seppi K, Schocke M, Benke T, Wenning GK, Poewe W (2004) Voxel based morphometry reveals a distinct pattern of frontal atrophy in progressive supranuclear palsy. J Neurol Neurosurg Psychiatry 75:246–249. doi:10.1136/jnnp.2003.015297 PubMedPubMedCentral

11.

Buee L, Delacoute A (1999) Comparative biochemistry of tau in progressive supranuclear palsy, corticobasal degeneration, FTDP-17 and Pick’s disease. Brain Pathol 9:681–693. doi:10.1111/j.1750-3639.1999.tb00550.x CrossRefPubMed

12.

Chiò A, Magnani C, Schiffer D (1998) Prevalence of Parkinson’s disease in Northwestern Italy: comparison of tracer methodology and clinical ascertainment of cases. Mov Disord 13:400–405. doi:10.1002/mds.870130305 CrossRefPubMed

13.

Colosimo C, Bak TH, Bologna M, Berardelli A (2014) Fifty years of progressive supranuclear palsy. J Neurol Neurosurg Psychiatry 85:938–944. doi:10.1136/jnnp-2013-305740 CrossRefPubMed

14.

Compta Y, Valldeoriola F, Tolosa E, Rey MJ, Martí MJ, Valls-Solé J (2007) Long lasting pure freezing of gait preceding progressive supranuclear palsy: a clinicopathological study. Mov Disord 22:1954–1958. doi:10.1002/mds.21612 CrossRefPubMed

15.

Del Tredici K, Braak H (2016) Sporadic Parkinson’s disease: development and distribution of a-synuclein pathology. Neuropathol Appl Neurobiol 42:33–50. doi:10.1111/nan.12298 CrossRefPubMed

16.

Dickson DW, Ahmed Z, Algom AA, Tsuboi Y, Josephs KA (2010) Neuropathology of variants of progressive supranuclear palsy. Curr Opin Neurol 23:394–400. doi:10.1097/WCO.0b013e32833be924 CrossRefPubMed

17.

Dickson DW, Hauw J, Agid Y, Litvan L (2011) Progressive supranuclear palsy and corticobasal degeneration. In: Dickson DW, Weller RO (eds) Neurodegeneration; the molecular pathology of dementia and movement disorders, 2nd edn. Wiley-Blackwell, Oxford, pp 133–155CrossRef

18.

Dickson DW, Rademakers R, Hutton ML (2007) Progressive supranuclear palsy: pathology and genetics. Brain Pathol 17:74–82. doi:10.1111/j.1750-3639.2007.00054.x CrossRefPubMed

19.

Donker Kaat L, Boon A, Kamphorst W, Ravid R, Duivenvoorden H, Van Swieten J (2007) Frontal presentation in progressive supranuclear palsy. Neurology 69:723–729. doi:10.1212/01.wnl.0000267643.24870.26 CrossRefPubMed

20.

Dugger BN, Hentz JG, Adler CH, Sabbagh MN, Shill HA, Jacobson S, Caviness JN, Belden C, Driver-Dunckley E, Davis KJ (2014) Clinicopathological outcomes of prospectively followed normal elderly brain bank volunteers. J Neuropathol Exp Neurol 73:244–252. doi:10.1097/NEN.0000000000000046 CrossRefPubMedPubMedCentral

21.

Evans W, Fung HC, Steele J, Eerola J, Tienari P, Pittman A, Silva Rd, Myers A, Vrieze FW, Singleton A, Hardy J (2004) The tau H2 haplotype is almost exclusively Caucasian in origin. Neurosci Lett 369:183–185. doi:10.1016/j.neulet.2004.05.119 CrossRefPubMed

22.

Evidente VG, Adler CH, Sabbagh MN, Connor DJ, Hentz JG, Caviness JN, Sue LI, Beach TG (2011) Neuropathological findings of PSP in the elderly without clinical PSP: possible incidental PSP? Parkinsonism Relat Disord 17:365–371. doi:10.1016/j.parkreldis.2011.02.017 CrossRefPubMedPubMedCentral

23.

Feany MB, Dickson DW (1995) Widespread cytoskeletal pathology characterizes corticobasal degeneration. Am J Pathol 146:1388–1396PubMedPubMedCentral

24.

Golbe LI, Davis PH, Schoenberg BS, Duvoisin RC (1988) Prevalence and natural history of progressive supranuclear palsy. Neurology 38:1031–1034. doi:10.1212/WNL.38.7.1031 CrossRefPubMed

25.

Hauw JJ, Daniel SE, Dickson D, Horoupian DS, Jellinger K, Lantos PL, McKee A, Tabaton M, Litvan I (1994) Preliminary NINDS neuropathologic criteria for Steele–Richardson–Olszewski syndrome (progressive supranuclear palsy). Neurology 44:2015–2019. doi:10.1212/WNL.44.11.2015 CrossRefPubMed

26.

Höglinger GU, Melhem NM, Dickson DW, Sleiman PM, Wang LS, Klei L et al (2011) Identification of common variants influencing risk of the tauopathy progressive supranuclear palsy. Nat Genet 43:699–705. doi:10.1038/ng.859 CrossRefPubMedPubMedCentral

27.

Hyman BT, Phelps CH, Beach TG, Bigio EH, Cairns NJ, Carrillo MC, Dickson DW, Duyckaerts C, Frosch MP, Masliah E, Mirra SS, Nelson PT, Schneider JA, Thal DR, Thies B, Trojanowski JQ, Vinters HV, Montine TJ (2012) National Institute on Aging-Alzheimer’s Association guidelines for the neuropathologic assessment of Alzheimer’s disease. Alzheimers Dement 8:1–13. doi:10.1016/j.jalz.2011.10.007 CrossRefPubMedPubMedCentral

28.

Ikeda K, Akiyama H, Arai T, Matsushita M, Tsuchiya K, Miyazaki H (2000) Clinical aspects of argyrophilic grain disease. Clin Neuropathol 19:278–284PubMed

29.

Irwin DJ, Cohen TJ, Grossman M, Arnold SE, McCarty-Wood E, Van Deerlin VM, Lee VM, Trojanowski JQ (2013) Acetylated tau neuropathology in sporadic and hereditary tauopathies. Am J Pathol 183:344–351. doi:10.1016/j.ajpath.2013.04.025 CrossRefPubMedPubMedCentral

30.

Iwasaki Y, Yoshida M, Hattori M, Goto A, Aiba I, Hashizume Y, Sobue G (2004) Distribution of tuft-shaped astrocytes in the cerebral cortex in progressive supranuclear palsy. Acta Neuropathol 108:399–405. doi:10.1007/s00401-004-0904-5 CrossRefPubMed

31.

Jackson JA, Jankovic J, Ford J (1983) Progressive supranuclear palsy: clinical features and response to treatment in 16 patients. Ann Neurol 13:273–278. doi:10.1002/ana.410130308 CrossRefPubMed

32.

Josephs KA, Murray ME, Whitwell JL, Tosakulwong N, Weigand SD, Petrucelli L, Liesinger AM, Petersen RC, Parisi JE, Dickson DW (2016) Updated TDP-43 in Alzheimer’s disease staging scheme. Acta Neuropathol 131:571–585. doi:10.1007/s00401-016-1537-1 CrossRefPubMed

33.

Kanazawa M, Shimohata T, Toyoshima Y, Tada M, Kakita A, Morita T, Ozawa T, Takahashi H, Nishizawa M (2009) Cerebellar involvement in progressive supranuclear palsy: a clinicopathological study. Mov Disord 24:1312–1318. doi:10.1002/mds.22583 CrossRefPubMed

34.

Kawashima M, Miyake M, Kusumi M, Adachi Y, Nakashima K (2004) Prevalence of progressive supranuclear palsy in Yonago, Japan. Mov Disord 19:1239–1240. doi:10.1002/mds.20149 CrossRefPubMed

35.

Kim WH, Lee YS, Jung SH, Choi HJ, Lee MJ, Kang MH, Kim CE, Lee JS, Bae JN (2009) Major depressive disorder preceding the onset of progressive supranuclear palsy. Psychiatry Investig 6:112–114. doi:10.4306/pi.2009.6.2.112 CrossRefPubMedPubMedCentral

36.

Komori T, Arai N, Oda M, Nakayama H, Mori H, Yagishita S, Takahashi T, Amano N, Murayama S, Murakami S (1998) Astrocytic plaques and tufts of abnormal fibers do not coexist in corticobasal degeneration and progressive supranuclear palsy. Acta Neuropathol 96:401–408. doi:10.1007/s004010050911 CrossRefPubMed

37.

Kovacs GG, Ferrer I, Grinberg LT, Alafuzoff I, Attems J, Budka H, Cairns NJ, Crary JF, Duyckaerts C, Ghetti B et al (2016) Aging-related tau astrogliopathy (ARTAG): harmonized evaluation strategy. Acta Neuropathol 131:87–102. doi:10.1007/s00401-015-1509-x CrossRefPubMed

38.

Kovacs GG, Milenkovic I, Wöhrer A, Höftberger R, Gelpi E, Haberler C, Hönigschnabl S, Reiner-Concin A, Heinzl H, Jungwirth S (2013) Non-Alzheimer neurodegenerative pathologies and their combinations are more frequent than commonly believed in the elderly brain: a community-based autopsy series. Acta Neuropathol 126:365–384. doi:10.1007/s00401-013-1157-y CrossRefPubMed

39.

Kovacs GG, Molnár K, László L, Ströbel T, Botond G, Hönigschnabl S, Reiner-Concin A, Palkovits M, Fischer P, Budka H (2011) A peculiar constellation of tau pathology defines a subset of dementia in the elderly. Acta Neuropathol 122:205–222. doi:10.1007/s00401-011-0819-x CrossRefPubMed

40.

Ling H, de Silva R, Massey LA, Courtney R, Hondhamuni G, Bajaj N, Lowe J, Holton JL, Lees A, Revesz T (2014) Characteristics of progressive supranuclear palsy presenting with corticobasal syndrome: a cortical variant. Neuropathol Appl Neurobiol 40:149–163. doi:10.1111/nan.12037 CrossRefPubMedPubMedCentral

41.

Ling H, Holton JL, Shaw K, Davey K, Lashley T, Revesz T (2015) Histological evidence of chronic traumatic encephalopathy in a large series of neurodegenerative diseases. Acta Neuropathol 130:891–893. doi:10.1007/s00401-015-1496-y CrossRefPubMed

42.

Ling H, Kovacs GG, Vonsattel JP, Davey K, Mok KY, Hardy J, Morris HR, Warner TT, Holton JL, Revesz T (2016) Astrogliopathy predominates the earliest stage of corticobasal degeneration. Brain 126:3237–3252. doi:10.1093/brain/aww256 CrossRef

43.

Litvan I, Mangone CA, McKee A, Verny M, Parsa A, Jellinger K, D’Olhaberriague L, Chaudhuri KR, Pearce RK (1996) Natural history of progressive supranuclear palsy (Steele–Richardson–Olszewski syndrome) and clinical predictors of survival: a clinicopathological study. J Neurol Neurosurg Psychiatry 61:615–620. doi:10.1136/jnnp.60.6.615 CrossRef

44.

Litvan I, Hauw JJ, Bartko JJ, Lantos PL, Daniel SE, Horoupian DS, McKee A, Dickson D, Bancher C, Tabaton M, Jellinger K, Anderson DW (1996) Validity and reliability of the preliminary NINDS neuropathologic criteria for progressive supranuclear palsy and related disorders. J Neuropathol Exp Neurol 55:97–105. doi:10.1097/00005072-199601000-00010 CrossRefPubMed

45.

Liu AK, Goldfinger MH, Questali HE, Pearce RKB, Gentleman SM (2016) ARTAG in the basal forebrain: widening the constellation of astrocytic tau pathology. Acta Neuropathol Commun 4:59. doi:10.1186/s40478-016-0330-7 CrossRefPubMedPubMedCentral

46.

Mackenzie IR, Neumann M, Baborie A, Sampathu DM, Du Plessis D, Jaros E, Perry RH, Trojanowski JQ, Mann DM, Lee VM (2011) A harmonized classification system for FTLD-TDP pathology. Acta Neuropathol 122:111–113. doi:10.1007/s00401-011-0845-8 CrossRefPubMedPubMedCentral

47.

Maher E, Lees A (1986) The clinical features and natural history of the Steele–Richardson–Olszewski syndrome (progressive supranuclear palsy). Neurology 36:1005–1008. doi:10.1212/WNL.36.7.1005 CrossRefPubMed

48.

Maurage C-A, Sergeant N, Schraen-Maschke S, Lebert F, Ruchoux M-M, Sablonnière B, Pasquier F, Delacourte A (2003) Diffuse form of argyrophilic grain disease: a new variant of four-repeat tauopathy different from limbic argyrophilic grain disease. Acta Neuropathol 106:575–583. doi:10.1007/S00401-003-0762-6 CrossRefPubMed

49.

Mckee AC, Cairns NJ, Dickson DW, Folkerth RD, Keene CD, Litvan I, Perl DP, Stein TD, Vonsattel JP, Stewart W, Tripodis Y, Crary JF, Bieniek KF, Dams-O’Connor K, Alvarez VE, Gordon WA (2016) The first NINDS/NIBIB consensus meeting to define neuropathological criteria for the diagnosis of chronic traumatic encephalopathy. Acta Neuropathol 131:75–86. doi:10.1007/s00401-015-1515-z CrossRefPubMed

50.

McKee AC, Stein TD, Kiernan PT, Alvarez VE (2015) The neuropathology of chronic traumatic encephalopathy. Brain Pathol 25:350–364. doi:10.1111/bpa.12248 CrossRefPubMedPubMedCentral

51.

McKee AC, Stern RA, Nowinski CJ, Stein TD, Alvarez VE, Daneshvar DH et al (2013) The spectrum of disease in chronic traumatic encephalopathy. Brain 136:43–64. doi:10.1093/brain/aws307 CrossRefPubMed

52.

McKeith IG, Dickson DW, Lowe J, Emre M, O’Brien JT, Feldman H, Cummings J, Duda JE, Lippa C, Perry EK, et al, Consortium on DLB (2005) Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium. Neurology 65:1863–1872. doi:10.1212/01.wnl.0000187889.17253.b1

53.

Millar D, Griffiths P, Zermansky AJ, Burn DJ (2006) Characterizing behavioral and cognitive dysexecutive changes in progressive supranuclear palsy. Mov Disord 21:199–207. doi:10.1002/mds.20707 CrossRefPubMed

54.

Mirra SS, Heyman A, McKeel D, Sumi SM, Crain BJ, Brownlee LM, Vogel FS, Hughes JP, van Belle G, Berg L (1991) The Consortium to Establish a Registry for Alzheimer’s Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer’s disease. Neurology 41:479–486. doi:10.1212/WNL.41.4.479 CrossRefPubMed

55.

Nath U, Ben-Shlomo Y, Thomson RG, Lees AJ, Burn DJ (2003) Clinical features and natural history of progressive supranuclear palsy: a clinical cohort study. Neurology 60:910–916. doi:10.1212/01.WNL.0000052991.70149.68 CrossRefPubMed

56.

Nath U, Ben-Shlomo Y, Thomson RG, Morris HR, Wood NW, Lees AJ, Burn DJ (2001) The prevalence of progressive supranuclear palsy (Steele–Richardson–Olszewski syndrome) in the UK. Brain 124:1438–1449. doi:10.1093/brain/124.7.1438 CrossRefPubMed

57.

Nishida N, Hata Y, Yoshida K, Kinoshita K (2015) Neuropathologic features of suicide victims who presented with acute poststroke depression: significance of association with neurodegenerative disorders. J Neuropathol Exp Neurol 74:401–410. doi:10.1097/NEN.0000000000000184 CrossRefPubMed

58.

Nishida N, Yoshida K, Hata Y, Arai Y, Kinoshita K (2015) Pathological features of preclinical or early clinical stages of corticobasal degeneration: a comparison with advanced cases. Neuropathol Appl Neurobiol 41:893–905. doi:10.1111/nan.12229 CrossRefPubMed

59.

Osaki Y, Morita Y, Kuwahara T, Miyano I, Doi Y (2011) Prevalence of Parkinson’s disease and atypical parkinsonian syndromes in a rural Japanese district. Acta Neurol Scand 124:182–187. doi:10.1111/j.1600-0404.2010.01442.x CrossRefPubMed

60.

Papapetropoulos S, Gonzalez J, Mash DC (2005) Natural history of progressive supranuclear palsy: a clinicopathologic study from a population of brain donors. Eur Neurol 54:1–9. doi:10.1159/000086754 CrossRefPubMed

61.

Quante A, Jakob F, Wolf J (2008) Depression preceding the onset of progressive supranuclear paralysis: a case report. J Neuropsychiatry Clin Neurosci 20:247–248. doi:10.1176/jnp.2008.20.2.247a CrossRefPubMed

62.

Respondek G, Stamelou M, Kurz C, Ferguson LW, Rajput A, Chiu WZ, van Swieten JC, Troakes C, Al Sarraj S, Gelpi E (2014) The phenotypic spectrum of progressive supranuclear palsy: a retrospective multicenter study of 100 definite cases. Mov Disord 29:1758–1766. doi:10.1002/mds.26054 CrossRefPubMed

63.

Saito Y, Ruberu NN, Sawabe M, Arai T, Tanaka N, Kakuta Y, Yamanouchi H, Murayama S (2004) Staging of argyrophilic grains: an age-associated tauopathy. J Neuropathol Exp Neurol 63:911–918. doi:10.1093/jnen/63.9.911 CrossRefPubMed

64.

Schrag A, Ben-Shlomo Y, Quinn NP (1999) Prevalence of progressive supranuclear palsy and multiple system atrophy: a cross-sectional study. Lancet 354:1771–1775. doi:10.1016/S0140-6736(99)04137-9 CrossRefPubMed

65.

Steele JC, Richardson JC, Olszewski J (1964) 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 10:333–359. doi:10.1001/archneur.1964.00460160003001 CrossRefPubMed

66.

Tatsumi S, Mimuro M, Iwasaki Y, Takahashi R, Kakita A, Takahashi H, Yoshida M (2014) Argyrophilic grains are reliable disease-specific features of corticobasal degeneration. J Neuropathol Exp Neurol 73:30–38. doi:10.1097/NEN.0000000000000022 CrossRefPubMed

67.

Thal DR, Rub U, Orantes M, Braak H (2002) Phases of A beta-deposition in the human brain and its relevance for the development of AD. Neurology 58:1791–1800. doi:10.1212/WNL.58.12.1791 CrossRefPubMed

68.

Togo T, Isojima D, Akatsu H, Suzuki K, Uchikado H, Katsuse O, Iseki E, Kosaka K, Hirayasu Y (2005) Clinical features of argyrophilic grain disease: a retrospective survey of cases with neuropsychiatric symptoms. Am J Geriatr Psychiatry 13:1083–1091. doi:10.1176/appi.ajgp.13.12.1083 CrossRefPubMed

69.

Tolney M, Monsch AU, Probst A (2001) Argyrophilic grain disease. A frequent dementing disorder in aged patients. Adv Exp Med Biol 487:39–58CrossRef

70.

Tsuboi Y, Josephs KA, Boeve BF, Litvan I, Caselli RJ, Caviness JN, Uitti RJ, Bott AD, Dickson DW (2005) Increased tau burden in the cortices of progressive supranuclear palsy presenting with corticobasal syndrome. Mov Disord 20:982–988. doi:10.1002/mds.20478 CrossRefPubMed

71.

Wermuth L, Joensen P, Bünger N, Jeune B (1997) High prevalence of Parkinson’s disease in the Faroe Islands. Neurology 49:426–432. doi:10.1212/WNL.49.2.426 CrossRefPubMed

72.

Williams DR, de Silva R, Paviour DC, Pittman A, Watt HC, Kilford L, Holton JL, Revesz T, Lees AJ (2005) Characteristics of two distinct clinical phenotypes in pathologically proven progressive supranuclear palsy: Richardson’s syndrome and PSP-parkinsonism. Brain 128:1247–1258. doi:10.1093/brain/awh488 CrossRefPubMed

73.

Williams DR, Holton JL, Strand K, Revesz T, Lees AJ (2007) Pure akinesia with gait freezing: a third clinical phenotype of progressive supranuclear palsy. Mov Disord 22:2235–2241. doi:10.1002/mds.21698 CrossRefPubMed

74.

Yokoyama Y, Toyoshima Y, Shiga A, Tada M, Kitamura H, Hasegawa K, Onodera O, Ikeuchi T, Someya T, Nishizawa M, Kakita A, Takahashi H (2015) Pathological and clinical spectrum of progressive supranuclear palsy: with special reference to astrocytic tau pathology. Brain Pathol 26:155–166. doi:10.1111/bpa.12265 CrossRefPubMed

75.

Yoshida M (2014) Astrocytic inclusions in progressive supranuclear palsy and corticobasal degeneration. Neuropathology 34:555–570. doi:10.1111/neup.12143 CrossRefPubMed

Title: Incipient progressive supranuclear palsy is more common than expected and may comprise clinicopathological subtypes: a forensic autopsy series
Authors: Koji Yoshida
Yukiko Hata
Koshi Kinoshita
Shutaro Takashima
Kortaro Tanaka
Naoki Nishida
Publication date: 01-05-2017
Publisher: Springer Berlin Heidelberg
Published in: Acta Neuropathologica / Issue 5/2017
Print ISSN: 0001-6322
Electronic ISSN: 1432-0533
DOI: https://doi.org/10.1007/s00401-016-1665-7

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Incipient progressive supranuclear palsy is more common than expected and may comprise clinicopathological subtypes: a forensic autopsy series

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