The phenotypic spectrum of progressive supranuclear palsy: A retrospective multicenter study of 100 definite cases
The phenotypic variability of progressive supranuclear palsy (PSP) may account for its frequent misdiagnosis, in particular in early stages of the disease. However, large multicenter studies to define the frequency and natural history of PSP phenotypes are missing. In a cohort of 100 autopsy‐confirm...
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| Published in | Movement disorders Vol. 29; no. 14; pp. 1758 - 1766 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Blackwell Publishing Ltd
01.12.2014
Wiley Subscription Services, Inc |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0885-3185 1531-8257 1531-8257 |
| DOI | 10.1002/mds.26054 |
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| Abstract | The phenotypic variability of progressive supranuclear palsy (PSP) may account for its frequent misdiagnosis, in particular in early stages of the disease. However, large multicenter studies to define the frequency and natural history of PSP phenotypes are missing. In a cohort of 100 autopsy‐confirmed patients we studied the phenotypic spectrum of PSP by retrospective chart review. Patients were derived from five brain banks with expertise in neurodegenerative disorders with referrals from multiple academic hospitals. The clinical characteristics of the 100 cases showed remarkable heterogeneity. Most strikingly, only 24% of cases presented as Richardson's Syndrome (RS), and more than half of the cases either showed overlapping features of several predescribed phenotypes, or features not fitting proposed classification criteria for PSP phenotypes. Classification of patients according to predominant clinical features in the first 2 years of the disease course allowed a more comprehensive description of the phenotypic spectrum. These predominance types differed significantly with regard to survival time and frequency of cognitive deficits. In summary, the phenotypic spectrum of PSP may be broader and more variable than previously described in single‐center studies. Thus, too strict clinical criteria defining distinct phenotypes may not reflect this variability. A more pragmatic clinical approach using predominance types could potentially be more helpful in the early recognition of and for making prognostic predictions for these patients. Given the limitations arising from the retrospective nature of this analysis, a systematic validation in a prospective cohort study is imperative. © 2014 International Parkinson and Movement Disorder Society |
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| AbstractList | The phenotypic variability of progressive supranuclear palsy (PSP) may account for its frequent misdiagnosis, in particular in early stages of the disease. However, large multicenter studies to define the frequency and natural history of PSP phenotypes are missing. In a cohort of 100 autopsy-confirmed patients we studied the phenotypic spectrum of PSP by retrospective chart review. Patients were derived from five brain banks with expertise in neurodegenerative disorders with referrals from multiple academic hospitals. The clinical characteristics of the 100 cases showed remarkable heterogeneity. Most strikingly, only 24% of cases presented as Richardson's Syndrome (RS), and more than half of the cases either showed overlapping features of several predescribed phenotypes, or features not fitting proposed classification criteria for PSP phenotypes. Classification of patients according to predominant clinical features in the first 2 years of the disease course allowed a more comprehensive description of the phenotypic spectrum. These predominance types differed significantly with regard to survival time and frequency of cognitive deficits. In summary, the phenotypic spectrum of PSP may be broader and more variable than previously described in single-center studies. Thus, too strict clinical criteria defining distinct phenotypes may not reflect this variability. A more pragmatic clinical approach using predominance types could potentially be more helpful in the early recognition of and for making prognostic predictions for these patients. Given the limitations arising from the retrospective nature of this analysis, a systematic validation in a prospective cohort study is imperative.The phenotypic variability of progressive supranuclear palsy (PSP) may account for its frequent misdiagnosis, in particular in early stages of the disease. However, large multicenter studies to define the frequency and natural history of PSP phenotypes are missing. In a cohort of 100 autopsy-confirmed patients we studied the phenotypic spectrum of PSP by retrospective chart review. Patients were derived from five brain banks with expertise in neurodegenerative disorders with referrals from multiple academic hospitals. The clinical characteristics of the 100 cases showed remarkable heterogeneity. Most strikingly, only 24% of cases presented as Richardson's Syndrome (RS), and more than half of the cases either showed overlapping features of several predescribed phenotypes, or features not fitting proposed classification criteria for PSP phenotypes. Classification of patients according to predominant clinical features in the first 2 years of the disease course allowed a more comprehensive description of the phenotypic spectrum. These predominance types differed significantly with regard to survival time and frequency of cognitive deficits. In summary, the phenotypic spectrum of PSP may be broader and more variable than previously described in single-center studies. Thus, too strict clinical criteria defining distinct phenotypes may not reflect this variability. A more pragmatic clinical approach using predominance types could potentially be more helpful in the early recognition of and for making prognostic predictions for these patients. Given the limitations arising from the retrospective nature of this analysis, a systematic validation in a prospective cohort study is imperative. The phenotypic variability of progressive supranuclear palsy (PSP) may account for its frequent misdiagnosis, in particular in early stages of the disease. However, large multicenter studies to define the frequency and natural history of PSP phenotypes are missing. In a cohort of 100 autopsy‐confirmed patients we studied the phenotypic spectrum of PSP by retrospective chart review. Patients were derived from five brain banks with expertise in neurodegenerative disorders with referrals from multiple academic hospitals. The clinical characteristics of the 100 cases showed remarkable heterogeneity. Most strikingly, only 24% of cases presented as Richardson's Syndrome (RS), and more than half of the cases either showed overlapping features of several predescribed phenotypes, or features not fitting proposed classification criteria for PSP phenotypes. Classification of patients according to predominant clinical features in the first 2 years of the disease course allowed a more comprehensive description of the phenotypic spectrum. These predominance types differed significantly with regard to survival time and frequency of cognitive deficits. In summary, the phenotypic spectrum of PSP may be broader and more variable than previously described in single‐center studies. Thus, too strict clinical criteria defining distinct phenotypes may not reflect this variability. A more pragmatic clinical approach using predominance types could potentially be more helpful in the early recognition of and for making prognostic predictions for these patients. Given the limitations arising from the retrospective nature of this analysis, a systematic validation in a prospective cohort study is imperative. © 2014 International Parkinson and Movement Disorder Society The phenotypic variability of progressive supranuclear palsy (PSP) may account for its frequent misdiagnosis, in particular in early stages of the disease. However, large multicenter studies to define the frequency and natural history of PSP phenotypes are missing. In a cohort of 100 autopsy-confirmed patients we studied the phenotypic spectrum of PSP by retrospective chart review. Patients were derived from five brain banks with expertise in neurodegenerative disorders with referrals from multiple academic hospitals. The clinical characteristics of the 100 cases showed remarkable heterogeneity. Most strikingly, only 24% of cases presented as Richardson's Syndrome (RS), and more than half of the cases either showed overlapping features of several predescribed phenotypes, or features not fitting proposed classification criteria for PSP phenotypes. Classification of patients according to predominant clinical features in the first 2 years of the disease course allowed a more comprehensive description of the phenotypic spectrum. These predominance types differed significantly with regard to survival time and frequency of cognitive deficits. In summary, the phenotypic spectrum of PSP may be broader and more variable than previously described in single-center studies. Thus, too strict clinical criteria defining distinct phenotypes may not reflect this variability. A more pragmatic clinical approach using predominance types could potentially be more helpful in the early recognition of and for making prognostic predictions for these patients. Given the limitations arising from the retrospective nature of this analysis, a systematic validation in a prospective cohort study is imperative. The phenotypic variability of progressive supranuclear palsy (PSP) may account for its frequent misdiagnosis, in particular in early stages of the disease. However, large multicenter studies to define the frequency and natural history of PSP phenotypes are missing. In a cohort of 100 autopsy-confirmed patients we studied the phenotypic spectrum of PSP by retrospective chart review. Patients were derived from five brain banks with expertise in neurodegenerative disorders with referrals from multiple academic hospitals. The clinical characteristics of the 100 cases showed remarkable heterogeneity. Most strikingly, only 24% of cases presented as Richardson's Syndrome (RS), and more than half of the cases either showed overlapping features of several predescribed phenotypes, or features not fitting proposed classification criteria for PSP phenotypes. Classification of patients according to predominant clinical features in the first 2 years of the disease course allowed a more comprehensive description of the phenotypic spectrum. These predominance types differed significantly with regard to survival time and frequency of cognitive deficits. In summary, the phenotypic spectrum of PSP may be broader and more variable than previously described in single-center studies. Thus, too strict clinical criteria defining distinct phenotypes may not reflect this variability. A more pragmatic clinical approach using predominance types could potentially be more helpful in the early recognition of and for making prognostic predictions for these patients. Given the limitations arising from the retrospective nature of this analysis, a systematic validation in a prospective cohort study is imperative. copyright 2014 International Parkinson and Movement Disorder Society |
| Author | al Sarraj, Safa Gelpi, Ellen Höglinger, Günter U. Gaig, Carles Kurz, Carolin Oertel, Wolfgang H. Stamelou, Maria Rajput, Alexander Wagenpfeil, Stefan Giese, Armin Roeber, Sigrun Tolosa, Eduardo Arzberger, Thomas van Swieten, John C. Chiu, Wan Zheng Ferguson, Leslie W. Troakes, Claire Respondek, Gesine |
| Author_xml | – sequence: 1 givenname: Gesine surname: Respondek fullname: Respondek, Gesine organization: Department of Neurology, Technische Universität München, Munich, Germany – sequence: 2 givenname: Maria surname: Stamelou fullname: Stamelou, Maria organization: Department of Neurology, Philipps Universität, Marburg, Germany – sequence: 3 givenname: Carolin surname: Kurz fullname: Kurz, Carolin organization: Department of Neurology, Technische Universität München, Munich, Germany – sequence: 4 givenname: Leslie W. surname: Ferguson fullname: Ferguson, Leslie W. organization: Division of Neurology, Royal University Hospital, University of Saskatchewan, Canada – sequence: 5 givenname: Alexander surname: Rajput fullname: Rajput, Alexander organization: Division of Neurology, Royal University Hospital, University of Saskatchewan, Canada – sequence: 6 givenname: Wan Zheng surname: Chiu fullname: Chiu, Wan Zheng organization: Department of Neurology, Erasmus Medical Centre, Rotterdam, The Netherlands – sequence: 7 givenname: John C. surname: van Swieten fullname: van Swieten, John C. organization: Department of Neurology, Erasmus Medical Centre, Rotterdam, The Netherlands – sequence: 8 givenname: Claire surname: Troakes fullname: Troakes, Claire organization: MRC London Neurodegenerative Diseases Brain Bank, King's College, London, UK – sequence: 9 givenname: Safa surname: al Sarraj fullname: al Sarraj, Safa organization: MRC London Neurodegenerative Diseases Brain Bank, King's College, London, UK – sequence: 10 givenname: Ellen surname: Gelpi fullname: Gelpi, Ellen organization: Neurological Tissue Bank and Neurology Department, Hospital Clínic de Barcelona, Universitat de Barcelona, IDIBAPS, Catalonia, Barcelona, Spain – sequence: 11 givenname: Carles surname: Gaig fullname: Gaig, Carles organization: Neurological Tissue Bank and Neurology Department, Hospital Clínic de Barcelona, Universitat de Barcelona, IDIBAPS, Catalonia, Barcelona, Spain – sequence: 12 givenname: Eduardo surname: Tolosa fullname: Tolosa, Eduardo organization: Neurology Service, Hospital Clínic de Barcelona, Universitat de Barcelona, IDIBAPS, Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), Catalonia, Barcelona, Spain – sequence: 13 givenname: Wolfgang H. surname: Oertel fullname: Oertel, Wolfgang H. organization: Department of Neurology, Philipps Universität, Marburg, Germany – sequence: 14 givenname: Armin surname: Giese fullname: Giese, Armin organization: Center for Neuropathology and Prion Research, Ludwig Maximilians University, Munich, Germany – sequence: 15 givenname: Sigrun surname: Roeber fullname: Roeber, Sigrun organization: Center for Neuropathology and Prion Research, Ludwig Maximilians University, Munich, Germany – sequence: 16 givenname: Thomas surname: Arzberger fullname: Arzberger, Thomas organization: Center for Neuropathology and Prion Research, Ludwig Maximilians University, Munich, Germany – sequence: 17 givenname: Stefan surname: Wagenpfeil fullname: Wagenpfeil, Stefan organization: Department of Medical Statistics and Epidemiology, Technische Universität München, Munich, Germany – sequence: 18 givenname: Günter U. surname: Höglinger fullname: Höglinger, Günter U. email: guenter.hoeglinger@dzne.de organization: Department of Neurology, Technische Universität München, Munich, Germany |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25370486$$D View this record in MEDLINE/PubMed |
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| References | Boeve B, Dickson D, Duffy J, Bartleson J, Trenerry M, Petersen R. Progressive nonfluent aphasia and subsequent aphasic dementia associated with atypical progressive supranuclear palsy pathology. Eur Neurol 2003;49:72-78. Imai H, Nakamura T, Kondo T, Narabayashi H. Dopa-unresponsive pure akinesia or freezing. A condition within a wide spectrum of PSP? Adv Neurol 1993;60:622-625. Respondek G, Roeber S, Kretzschmar H, et al. Accuracy of the National Institute for Neurological Disorders and Stroke/Society for Progressive Supranuclear Palsy and neuroprotection and natural history in Parkinson plus syndromes criteria for the diagnosis of progressive supranuclear palsy. Mov Disord 2013;28:504-509. Donker Kaat L, Boon AJ, Kamphorst W, Ravid R, Duivenvoorden HJ, van Swieten JC. Frontal presentation in progressive supranuclear palsy. Neurology 2007;69:723-729. Osaki Y, Ben-Shlomo Y, Lees AJ, Daniel SE, Colosimo C, Wenning G, Quinn N. Accuracy of clinical diagnosis of progressive supranuclear palsy. Mov Disord 2004;19:181-189. Kanazawa M, Shimohata T, Toyoshima Y, et al. Cerebellar involvement in progressive supranuclear palsy: a clinicopathological study. Mov Disord 2009;24:1312-1318. Bensimon G, Ludolph A, Agid Y, Vidailhet M, Payan C, Leigh PN, NNIPPS Study Group. Riluzole treatment, survival and diagnostic criteria in Parkinson plus disorders: the NNIPPS study. Brain 2009;132:156-171. Josephs KA, Duffy JR. Apraxia of speech and nonfluent aphasia: a new clinical marker for corticobasal degeneration and progressive supranuclear palsy. Curr Opin Neurol 2008;21:688-692. Hauw JJ, Daniel SE, Dickson D, et al. Preliminary NINDS Neuropathologic criteria for Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy). [Review]. Neurology 1994;44:2015-2019. Kleinschmidt-DeMasters BK. Early progressive supranuclear palsy: pathology and clinical presentation. Clin Neuropathol 1989;8:79-84. Armstrong MJ, Litvan I, Lang AE, et al. Criteria for the diagnosis of corticobasal degeneration. Neurology 2013;29;80:496-503. Williams DR, Lee W. Clinical features and criteria for the diagnosis of progressive supranuclear palsy. Neurodegen Dis Manage 2012;2:1-9. Mochizuki A, Ueda Y, Komatsuzaki Y, Tsuchiya K, Arai T, Shoji S. Progressive supranuclear palsy presenting with primary progressive aphasia: clinicopathological report of an autopsy case. Acta Neuropathol 2003;105:610-614. Tsuboi Y, Josephs KA, Boeve BF, et al. Increased tau burden in the cortices of progressive supranuclear palsy presenting with corticobasal syndrome. Mov Disord 2005;20:982-988. Josephs KA, Petersen RC, Knopman DS, et al. Clinicopathologic analysis of frontotemporal and corticobasal degenerations and PSP. Neurology 2006;66:41-48. Litvan I, Agid Y, Calne D, et al. Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome): report of the NINDS-SPSP international workshop. Neurology 1996;47:1-9. Hassan A, Parisi JE, Josephs KA. Autopsy-proven progressive supranuclear palsy presenting as behavioral variant frontotemporal dementia. Neurocase 2012;18:478-488. Imai H, Narabayashi H, Sakata E. "Pure akinesia" and the later added supranuclear ophthalmoplegia. Adv Neurol 1987;45:207-212. Iwasaki Y, Mori K, Ito M, Tatsumi S, Mimuro M, Yoshida M. An autopsied case of progressive supranuclear palsy presenting with cerebellar ataxia and severe cerebellar involvement. Neuropathology 2013;33:561-567. Williams DR, Holton JL, Strand K, Revesz T, Lees AJ. Pure akinesia with gait freezing: a third clinical phenotype of progressive supranuclear palsy. Mov Disord 2007;22:2235-2241. Dubas F, Gray F, Escourolle R. Steele-Richardson-Olszewski disease without ophthalmoplegia. 6 clinico-anatomic cases. [Review]. Rev Neurol (Paris) 1983;139:407-416. Han HJ, Kim H, Park JH, et al. Behavioral changes as the earliest clinical manifestation of progressive supranuclear palsy. J Clin Neurol 2010;6:148-151. Davis PH, Bergeron C, McLachlan DR. Atypical presentation of progressive supranuclear palsy. Ann Neurol 1985;17:337-343. Williams DR, de Silva R, Paviour DC, et al. Characteristics of two distinct clinical phenotypes in pathologically proven progressive supranuclear palsy: Richardson's syndrome and PSP-parkinsonism. Brain 2005;128:1247-1258. Birdi S, Rajput AH, Fenton M, et al. Progressive supranuclear palsy diagnosis and confounding features: report on 16 autopsied cases. Mov Disord 2002;17:1255-1264. Ling H, de Silva R, Massey LA, et al. Characteristics of progressive supranuclear palsy presenting with corticobasal syndrome: a cortical variant. Neuropathol Appl Neurobiol 2014;40:149-163. Campbell-Taylor I. Atypical presentation of progressive supranuclear palsy. Ann Neurol 1986;20:375. Daniel SE, de Bruin VM, Lees AJ. The clinical and pathological spectrum of Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy): a reappraisal. Brain 1995;118:759-770. Mizusawa H, Mochizuki A, Ohkoshi N, Yoshizawa K, Kanazawa I, Imai H. Progressive supranuclear palsy presenting with pure akinesia. Adv Neurol 1993;60:618-621. Morris HR, Gibb G, Katzenschlager R, et al. Pathological, clinical and genetic heterogeneity in progressive supranuclear palsy. Brain 2002;125:969-975. Steele JC, Richardson JC, Olszewski J. 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 1964;10:333-359. Compta Y, Valldeoriola F, Tolosa E, Rey MJ, Martí MJ, Valls-Solé J. Long lasting pure freezing of gait preceding progressive supranuclear palsy: a clinicopathological study. Mov Disord 2007;22:1954-1958. Matsuo H, Takashima H, Kishikawa M, et al. Pure akinesia: an atypical manifestation of progressive supranuclear palsy. J Neurol Neurosurg Psychiatry 1991;54:397-400. Williams DR, Lees AJ. Progressive supranuclear palsy: clinicopathological concepts and diagnostic challenges. Lancet Neurol 2009;8:270-279. 1983; 139 2002; 17 2009; 24 2013; 28 1991; 54 1993; 60 1989; 8 2009; 132 1995; 118 1994; 44 2005; 20 2012; 18 2014; 40 1985; 17 1987; 45 2012; 2 2003; 105 2013; 33 1986; 20 2004; 19 2006; 66 2013; 29;80 2002; 125 2005; 128 1964; 10 2003; 49 2009; 8 2008; 21 1996; 47 2007; 22 2010; 6 2007; 69 e_1_2_8_28_1 e_1_2_8_29_1 e_1_2_8_24_1 e_1_2_8_25_1 e_1_2_8_26_1 e_1_2_8_27_1 e_1_2_8_3_1 e_1_2_8_2_1 Imai H (e_1_2_8_10_1) 1993; 60 Mochizuki A (e_1_2_8_22_1) 2003; 105 e_1_2_8_5_1 e_1_2_8_6_1 e_1_2_8_9_1 e_1_2_8_20_1 e_1_2_8_21_1 e_1_2_8_23_1 e_1_2_8_17_1 e_1_2_8_18_1 e_1_2_8_19_1 e_1_2_8_13_1 Imai H (e_1_2_8_7_1) 1987; 45 e_1_2_8_14_1 e_1_2_8_35_1 Mizusawa H (e_1_2_8_11_1) 1993; 60 e_1_2_8_15_1 e_1_2_8_16_1 e_1_2_8_32_1 Dubas F (e_1_2_8_4_1) 1983; 139 e_1_2_8_31_1 Kleinschmidt‐DeMasters BK (e_1_2_8_8_1) 1989; 8 e_1_2_8_34_1 e_1_2_8_12_1 e_1_2_8_33_1 e_1_2_8_30_1 |
| References_xml | – reference: Armstrong MJ, Litvan I, Lang AE, et al. Criteria for the diagnosis of corticobasal degeneration. Neurology 2013;29;80:496-503. – reference: Birdi S, Rajput AH, Fenton M, et al. Progressive supranuclear palsy diagnosis and confounding features: report on 16 autopsied cases. Mov Disord 2002;17:1255-1264. – reference: Tsuboi Y, Josephs KA, Boeve BF, et al. Increased tau burden in the cortices of progressive supranuclear palsy presenting with corticobasal syndrome. Mov Disord 2005;20:982-988. – reference: Morris HR, Gibb G, Katzenschlager R, et al. Pathological, clinical and genetic heterogeneity in progressive supranuclear palsy. Brain 2002;125:969-975. – reference: Hauw JJ, Daniel SE, Dickson D, et al. Preliminary NINDS Neuropathologic criteria for Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy). [Review]. Neurology 1994;44:2015-2019. – reference: Boeve B, Dickson D, Duffy J, Bartleson J, Trenerry M, Petersen R. Progressive nonfluent aphasia and subsequent aphasic dementia associated with atypical progressive supranuclear palsy pathology. Eur Neurol 2003;49:72-78. – reference: Osaki Y, Ben-Shlomo Y, Lees AJ, Daniel SE, Colosimo C, Wenning G, Quinn N. Accuracy of clinical diagnosis of progressive supranuclear palsy. Mov Disord 2004;19:181-189. – reference: Matsuo H, Takashima H, Kishikawa M, et al. Pure akinesia: an atypical manifestation of progressive supranuclear palsy. J Neurol Neurosurg Psychiatry 1991;54:397-400. – reference: Williams DR, Lees AJ. Progressive supranuclear palsy: clinicopathological concepts and diagnostic challenges. Lancet Neurol 2009;8:270-279. – reference: Campbell-Taylor I. Atypical presentation of progressive supranuclear palsy. Ann Neurol 1986;20:375. – reference: Hassan A, Parisi JE, Josephs KA. Autopsy-proven progressive supranuclear palsy presenting as behavioral variant frontotemporal dementia. Neurocase 2012;18:478-488. – reference: Litvan I, Agid Y, Calne D, et al. Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome): report of the NINDS-SPSP international workshop. Neurology 1996;47:1-9. – reference: Kleinschmidt-DeMasters BK. Early progressive supranuclear palsy: pathology and clinical presentation. Clin Neuropathol 1989;8:79-84. – reference: Bensimon G, Ludolph A, Agid Y, Vidailhet M, Payan C, Leigh PN, NNIPPS Study Group. Riluzole treatment, survival and diagnostic criteria in Parkinson plus disorders: the NNIPPS study. Brain 2009;132:156-171. – reference: Mochizuki A, Ueda Y, Komatsuzaki Y, Tsuchiya K, Arai T, Shoji S. Progressive supranuclear palsy presenting with primary progressive aphasia: clinicopathological report of an autopsy case. Acta Neuropathol 2003;105:610-614. – reference: Kanazawa M, Shimohata T, Toyoshima Y, et al. Cerebellar involvement in progressive supranuclear palsy: a clinicopathological study. Mov Disord 2009;24:1312-1318. – reference: Daniel SE, de Bruin VM, Lees AJ. The clinical and pathological spectrum of Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy): a reappraisal. Brain 1995;118:759-770. – reference: Davis PH, Bergeron C, McLachlan DR. Atypical presentation of progressive supranuclear palsy. Ann Neurol 1985;17:337-343. – reference: Steele JC, Richardson JC, Olszewski J. 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 1964;10:333-359. – reference: Josephs KA, Petersen RC, Knopman DS, et al. Clinicopathologic analysis of frontotemporal and corticobasal degenerations and PSP. Neurology 2006;66:41-48. – reference: Compta Y, Valldeoriola F, Tolosa E, Rey MJ, Martí MJ, Valls-Solé J. Long lasting pure freezing of gait preceding progressive supranuclear palsy: a clinicopathological study. Mov Disord 2007;22:1954-1958. – reference: Williams DR, Lee W. Clinical features and criteria for the diagnosis of progressive supranuclear palsy. Neurodegen Dis Manage 2012;2:1-9. – reference: Williams DR, Holton JL, Strand K, Revesz T, Lees AJ. Pure akinesia with gait freezing: a third clinical phenotype of progressive supranuclear palsy. Mov Disord 2007;22:2235-2241. – reference: Williams DR, de Silva R, Paviour DC, et al. Characteristics of two distinct clinical phenotypes in pathologically proven progressive supranuclear palsy: Richardson's syndrome and PSP-parkinsonism. Brain 2005;128:1247-1258. – reference: Imai H, Nakamura T, Kondo T, Narabayashi H. Dopa-unresponsive pure akinesia or freezing. A condition within a wide spectrum of PSP? Adv Neurol 1993;60:622-625. – reference: Han HJ, Kim H, Park JH, et al. Behavioral changes as the earliest clinical manifestation of progressive supranuclear palsy. J Clin Neurol 2010;6:148-151. – reference: Respondek G, Roeber S, Kretzschmar H, et al. Accuracy of the National Institute for Neurological Disorders and Stroke/Society for Progressive Supranuclear Palsy and neuroprotection and natural history in Parkinson plus syndromes criteria for the diagnosis of progressive supranuclear palsy. Mov Disord 2013;28:504-509. – reference: Imai H, Narabayashi H, Sakata E. "Pure akinesia" and the later added supranuclear ophthalmoplegia. Adv Neurol 1987;45:207-212. – reference: Ling H, de Silva R, Massey LA, et al. Characteristics of progressive supranuclear palsy presenting with corticobasal syndrome: a cortical variant. Neuropathol Appl Neurobiol 2014;40:149-163. – reference: Dubas F, Gray F, Escourolle R. Steele-Richardson-Olszewski disease without ophthalmoplegia. 6 clinico-anatomic cases. [Review]. 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| Title | The phenotypic spectrum of progressive supranuclear palsy: A retrospective multicenter study of 100 definite cases |
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