Typical and atypical pathology in primary progressive aphasia variants

Objective To characterize in vivo signatures of pathological diagnosis in a large cohort of patients with primary progressive aphasia (PPA) variants defined by current diagnostic classification. Methods Extensive clinical, cognitive, neuroimaging, and neuropathological data were collected from 69 pa...

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Published in:	Annals of neurology Vol. 81; no. 3; pp. 430 - 443
Main Authors:	Spinelli, Edoardo G., Mandelli, Maria Luisa, Miller, Zachary A., Santos‐Santos, Miguel A, Wilson, Stephen M., Agosta, Federica, Grinberg, Lea T., Huang, Eric J., Trojanowski, John Q., Meyer, Marita, Henry, Maya L., Comi, Giancarlo, Rabinovici, Gil, Rosen, Howard J., Filippi, Massimo, Miller, Bruce L., Seeley, William W., Gorno‐Tempini, Maria Luisa
Format:	Journal Article
Language:	English
Published:	United States Wiley Subscription Services, Inc 01.03.2017
Subjects:	Aged Aged, 80 and over Alzheimer Disease - classification Alzheimer Disease - pathology Alzheimer Disease - physiopathology Aphasia, Primary Progressive - classification Aphasia, Primary Progressive - pathology Aphasia, Primary Progressive - physiopathology Atrophy - pathology Female Frontotemporal Lobar Degeneration - classification Frontotemporal Lobar Degeneration - pathology Frontotemporal Lobar Degeneration - physiopathology Gray Matter - diagnostic imaging Humans Male Medical imaging Middle Aged Neuropathology Pathology Pick Disease of the Brain - pathology Pick Disease of the Brain - physiopathology Primary Progressive Nonfluent Aphasia - pathology Primary Progressive Nonfluent Aphasia - physiopathology Support Vector Machine tau Proteins - metabolism White Matter - diagnostic imaging
ISSN:	0364-5134, 1531-8249, 1531-8249
Online Access:	Get full text
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Abstract	Objective To characterize in vivo signatures of pathological diagnosis in a large cohort of patients with primary progressive aphasia (PPA) variants defined by current diagnostic classification. Methods Extensive clinical, cognitive, neuroimaging, and neuropathological data were collected from 69 patients with sporadic PPA, divided into 29 semantic (svPPA), 25 nonfluent (nfvPPA), 11 logopenic (lvPPA), and 4 mixed PPA. Patterns of gray matter (GM) and white matter (WM) atrophy at presentation were assessed and tested as predictors of pathological diagnosis using support vector machine (SVM) algorithms. Results A clinical diagnosis of PPA was associated with frontotemporal lobar degeneration (FTLD) with transactive response DNA‐binding protein (TDP) inclusions in 40.5%, FTLD‐tau in 40.5%, and Alzheimer disease (AD) pathology in 19% of cases. Each variant was associated with 1 typical pathology; 24 of 29 (83%) svPPA showed FTLD‐TDP type C, 22 of 25 (88%) nfvPPA showed FTLD‐tau, and all 11 lvPPA had AD. Within FTLD‐tau, 4R‐tau pathology was commonly associated with nfvPPA, whereas Pick disease was observed in a minority of subjects across all variants except for lvPPA. Compared with pathologically typical cases, svPPA‐tau showed significant extrapyramidal signs, greater executive impairment, and severe striatal and frontal GM and WM atrophy. nfvPPA‐TDP patients lacked general motor symptoms or significant WM atrophy. Combining GM and WM volumes, SVM analysis showed 92.7% accuracy to distinguish FTLD‐tau and FTLD‐TDP pathologies across variants. Interpretation Each PPA clinical variant is associated with a typical and most frequent cognitive, neuroimaging, and neuropathological profile. Specific clinical and early anatomical features may suggest rare and atypical pathological diagnosis in vivo. Ann Neurol 2017;81:430–443
AbstractList	To characterize in vivo signatures of pathological diagnosis in a large cohort of patients with primary progressive aphasia (PPA) variants defined by current diagnostic classification.OBJECTIVETo characterize in vivo signatures of pathological diagnosis in a large cohort of patients with primary progressive aphasia (PPA) variants defined by current diagnostic classification.Extensive clinical, cognitive, neuroimaging, and neuropathological data were collected from 69 patients with sporadic PPA, divided into 29 semantic (svPPA), 25 nonfluent (nfvPPA), 11 logopenic (lvPPA), and 4 mixed PPA. Patterns of gray matter (GM) and white matter (WM) atrophy at presentation were assessed and tested as predictors of pathological diagnosis using support vector machine (SVM) algorithms.METHODSExtensive clinical, cognitive, neuroimaging, and neuropathological data were collected from 69 patients with sporadic PPA, divided into 29 semantic (svPPA), 25 nonfluent (nfvPPA), 11 logopenic (lvPPA), and 4 mixed PPA. Patterns of gray matter (GM) and white matter (WM) atrophy at presentation were assessed and tested as predictors of pathological diagnosis using support vector machine (SVM) algorithms.A clinical diagnosis of PPA was associated with frontotemporal lobar degeneration (FTLD) with transactive response DNA-binding protein (TDP) inclusions in 40.5%, FTLD-tau in 40.5%, and Alzheimer disease (AD) pathology in 19% of cases. Each variant was associated with 1 typical pathology; 24 of 29 (83%) svPPA showed FTLD-TDP type C, 22 of 25 (88%) nfvPPA showed FTLD-tau, and all 11 lvPPA had AD. Within FTLD-tau, 4R-tau pathology was commonly associated with nfvPPA, whereas Pick disease was observed in a minority of subjects across all variants except for lvPPA. Compared with pathologically typical cases, svPPA-tau showed significant extrapyramidal signs, greater executive impairment, and severe striatal and frontal GM and WM atrophy. nfvPPA-TDP patients lacked general motor symptoms or significant WM atrophy. Combining GM and WM volumes, SVM analysis showed 92.7% accuracy to distinguish FTLD-tau and FTLD-TDP pathologies across variants.RESULTSA clinical diagnosis of PPA was associated with frontotemporal lobar degeneration (FTLD) with transactive response DNA-binding protein (TDP) inclusions in 40.5%, FTLD-tau in 40.5%, and Alzheimer disease (AD) pathology in 19% of cases. Each variant was associated with 1 typical pathology; 24 of 29 (83%) svPPA showed FTLD-TDP type C, 22 of 25 (88%) nfvPPA showed FTLD-tau, and all 11 lvPPA had AD. Within FTLD-tau, 4R-tau pathology was commonly associated with nfvPPA, whereas Pick disease was observed in a minority of subjects across all variants except for lvPPA. Compared with pathologically typical cases, svPPA-tau showed significant extrapyramidal signs, greater executive impairment, and severe striatal and frontal GM and WM atrophy. nfvPPA-TDP patients lacked general motor symptoms or significant WM atrophy. Combining GM and WM volumes, SVM analysis showed 92.7% accuracy to distinguish FTLD-tau and FTLD-TDP pathologies across variants.Each PPA clinical variant is associated with a typical and most frequent cognitive, neuroimaging, and neuropathological profile. Specific clinical and early anatomical features may suggest rare and atypical pathological diagnosis in vivo. Ann Neurol 2017;81:430-443.INTERPRETATIONEach PPA clinical variant is associated with a typical and most frequent cognitive, neuroimaging, and neuropathological profile. Specific clinical and early anatomical features may suggest rare and atypical pathological diagnosis in vivo. Ann Neurol 2017;81:430-443. Objective To characterize in vivo signatures of pathological diagnosis in a large cohort of patients with primary progressive aphasia (PPA) variants defined by current diagnostic classification. Methods Extensive clinical, cognitive, neuroimaging, and neuropathological data were collected from 69 patients with sporadic PPA, divided into 29 semantic (svPPA), 25 nonfluent (nfvPPA), 11 logopenic (lvPPA), and 4 mixed PPA. Patterns of gray matter (GM) and white matter (WM) atrophy at presentation were assessed and tested as predictors of pathological diagnosis using support vector machine (SVM) algorithms. Results A clinical diagnosis of PPA was associated with frontotemporal lobar degeneration (FTLD) with transactive response DNA-binding protein (TDP) inclusions in 40.5%, FTLD-tau in 40.5%, and Alzheimer disease (AD) pathology in 19% of cases. Each variant was associated with 1 typical pathology; 24 of 29 (83%) svPPA showed FTLD-TDP type C, 22 of 25 (88%) nfvPPA showed FTLD-tau, and all 11 lvPPA had AD. Within FTLD-tau, 4R-tau pathology was commonly associated with nfvPPA, whereas Pick disease was observed in a minority of subjects across all variants except for lvPPA. Compared with pathologically typical cases, svPPA-tau showed significant extrapyramidal signs, greater executive impairment, and severe striatal and frontal GM and WM atrophy. nfvPPA-TDP patients lacked general motor symptoms or significant WM atrophy. Combining GM and WM volumes, SVM analysis showed 92.7% accuracy to distinguish FTLD-tau and FTLD-TDP pathologies across variants. Interpretation Each PPA clinical variant is associated with a typical and most frequent cognitive, neuroimaging, and neuropathological profile. Specific clinical and early anatomical features may suggest rare and atypical pathological diagnosis in vivo. Ann Neurol 2017;81:430-443 Objective To characterize in vivo signatures of pathological diagnosis in a large cohort of patients with primary progressive aphasia (PPA) variants defined by current diagnostic classification. Methods Extensive clinical, cognitive, neuroimaging, and neuropathological data were collected from 69 patients with sporadic PPA, divided into 29 semantic (svPPA), 25 nonfluent (nfvPPA), 11 logopenic (lvPPA), and 4 mixed PPA. Patterns of gray matter (GM) and white matter (WM) atrophy at presentation were assessed and tested as predictors of pathological diagnosis using support vector machine (SVM) algorithms. Results A clinical diagnosis of PPA was associated with frontotemporal lobar degeneration (FTLD) with transactive response DNA‐binding protein (TDP) inclusions in 40.5%, FTLD‐tau in 40.5%, and Alzheimer disease (AD) pathology in 19% of cases. Each variant was associated with 1 typical pathology; 24 of 29 (83%) svPPA showed FTLD‐TDP type C, 22 of 25 (88%) nfvPPA showed FTLD‐tau, and all 11 lvPPA had AD. Within FTLD‐tau, 4R‐tau pathology was commonly associated with nfvPPA, whereas Pick disease was observed in a minority of subjects across all variants except for lvPPA. Compared with pathologically typical cases, svPPA‐tau showed significant extrapyramidal signs, greater executive impairment, and severe striatal and frontal GM and WM atrophy. nfvPPA‐TDP patients lacked general motor symptoms or significant WM atrophy. Combining GM and WM volumes, SVM analysis showed 92.7% accuracy to distinguish FTLD‐tau and FTLD‐TDP pathologies across variants. Interpretation Each PPA clinical variant is associated with a typical and most frequent cognitive, neuroimaging, and neuropathological profile. Specific clinical and early anatomical features may suggest rare and atypical pathological diagnosis in vivo. Ann Neurol 2017;81:430–443 To characterize in vivo signatures of pathological diagnosis in a large cohort of patients with primary progressive aphasia (PPA) variants defined by current diagnostic classification. Extensive clinical, cognitive, neuroimaging, and neuropathological data were collected from 69 patients with sporadic PPA, divided into 29 semantic (svPPA), 25 nonfluent (nfvPPA), 11 logopenic (lvPPA), and 4 mixed PPA. Patterns of gray matter (GM) and white matter (WM) atrophy at presentation were assessed and tested as predictors of pathological diagnosis using support vector machine (SVM) algorithms. A clinical diagnosis of PPA was associated with frontotemporal lobar degeneration (FTLD) with transactive response DNA-binding protein (TDP) inclusions in 40.5%, FTLD-tau in 40.5%, and Alzheimer disease (AD) pathology in 19% of cases. Each variant was associated with 1 typical pathology; 24 of 29 (83%) svPPA showed FTLD-TDP type C, 22 of 25 (88%) nfvPPA showed FTLD-tau, and all 11 lvPPA had AD. Within FTLD-tau, 4R-tau pathology was commonly associated with nfvPPA, whereas Pick disease was observed in a minority of subjects across all variants except for lvPPA. Compared with pathologically typical cases, svPPA-tau showed significant extrapyramidal signs, greater executive impairment, and severe striatal and frontal GM and WM atrophy. nfvPPA-TDP patients lacked general motor symptoms or significant WM atrophy. Combining GM and WM volumes, SVM analysis showed 92.7% accuracy to distinguish FTLD-tau and FTLD-TDP pathologies across variants. Each PPA clinical variant is associated with a typical and most frequent cognitive, neuroimaging, and neuropathological profile. Specific clinical and early anatomical features may suggest rare and atypical pathological diagnosis in vivo. Ann Neurol 2017;81:430-443.
Author	Grinberg, Lea T. Henry, Maya L. Mandelli, Maria Luisa Wilson, Stephen M. Trojanowski, John Q. Huang, Eric J. Rosen, Howard J. Meyer, Marita Rabinovici, Gil Seeley, William W. Miller, Zachary A. Comi, Giancarlo Filippi, Massimo Miller, Bruce L. Spinelli, Edoardo G. Gorno‐Tempini, Maria Luisa Santos‐Santos, Miguel A Agosta, Federica
AuthorAffiliation	2 Neuroimaging Research Unit, Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan, Italy 4 Department of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, PA, USA 1 Memory and Aging Center, University of California, San Francisco, CA, USA 3 Department of Speech, Language, and Hearing Sciences, University of Arizona, Tucson, AZ, USA 5 Department of Communication Sciences and Disorders, University of Texas, Austin, TX, USA
AuthorAffiliation_xml	– name: 4 Department of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, PA, USA – name: 1 Memory and Aging Center, University of California, San Francisco, CA, USA – name: 2 Neuroimaging Research Unit, Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan, Italy – name: 3 Department of Speech, Language, and Hearing Sciences, University of Arizona, Tucson, AZ, USA – name: 5 Department of Communication Sciences and Disorders, University of Texas, Austin, TX, USA
Author_xml	– sequence: 1 givenname: Edoardo G. surname: Spinelli fullname: Spinelli, Edoardo G. organization: Vita‐Salute San Raffaele University – sequence: 2 givenname: Maria Luisa surname: Mandelli fullname: Mandelli, Maria Luisa organization: University of California – sequence: 3 givenname: Zachary A. surname: Miller fullname: Miller, Zachary A. organization: University of California – sequence: 4 givenname: Miguel A surname: Santos‐Santos fullname: Santos‐Santos, Miguel A organization: University of California – sequence: 5 givenname: Stephen M. surname: Wilson fullname: Wilson, Stephen M. organization: Vanderbilt University Medical Center – sequence: 6 givenname: Federica surname: Agosta fullname: Agosta, Federica organization: Vita‐Salute San Raffaele University – sequence: 7 givenname: Lea T. surname: Grinberg fullname: Grinberg, Lea T. organization: University of California – sequence: 8 givenname: Eric J. surname: Huang fullname: Huang, Eric J. organization: University of California – sequence: 9 givenname: John Q. surname: Trojanowski fullname: Trojanowski, John Q. organization: University of Pennsylvania – sequence: 10 givenname: Marita surname: Meyer fullname: Meyer, Marita organization: University of California – sequence: 11 givenname: Maya L. surname: Henry fullname: Henry, Maya L. organization: University of Texas – sequence: 12 givenname: Giancarlo surname: Comi fullname: Comi, Giancarlo organization: Vita‐Salute San Raffaele University – sequence: 13 givenname: Gil surname: Rabinovici fullname: Rabinovici, Gil organization: University of California – sequence: 14 givenname: Howard J. surname: Rosen fullname: Rosen, Howard J. organization: University of California – sequence: 15 givenname: Massimo surname: Filippi fullname: Filippi, Massimo organization: Vita‐Salute San Raffaele University – sequence: 16 givenname: Bruce L. surname: Miller fullname: Miller, Bruce L. organization: University of California – sequence: 17 givenname: William W. surname: Seeley fullname: Seeley, William W. organization: University of California – sequence: 18 givenname: Maria Luisa surname: Gorno‐Tempini fullname: Gorno‐Tempini, Maria Luisa email: marialuisa.gornotempini@ucsf.edu organization: University of California
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/28133816$$D View this record in MEDLINE/PubMed
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Snippet	Objective To characterize in vivo signatures of pathological diagnosis in a large cohort of patients with primary progressive aphasia (PPA) variants defined by... To characterize in vivo signatures of pathological diagnosis in a large cohort of patients with primary progressive aphasia (PPA) variants defined by current... Objective To characterize in vivo signatures of pathological diagnosis in a large cohort of patients with primary progressive aphasia (PPA) variants defined by...
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SubjectTerms	Aged Aged, 80 and over Alzheimer Disease - classification Alzheimer Disease - pathology Alzheimer Disease - physiopathology Aphasia, Primary Progressive - classification Aphasia, Primary Progressive - pathology Aphasia, Primary Progressive - physiopathology Atrophy - pathology Female Frontotemporal Lobar Degeneration - classification Frontotemporal Lobar Degeneration - pathology Frontotemporal Lobar Degeneration - physiopathology Gray Matter - diagnostic imaging Humans Male Medical imaging Middle Aged Neuropathology Pathology Pick Disease of the Brain - pathology Pick Disease of the Brain - physiopathology Primary Progressive Nonfluent Aphasia - pathology Primary Progressive Nonfluent Aphasia - physiopathology Support Vector Machine tau Proteins - metabolism White Matter - diagnostic imaging
Title	Typical and atypical pathology in primary progressive aphasia variants
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