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C9orf72, age at onset, and ancestry help discriminate behavioral from language variants in FTLD cohorts

OBJECTIVE: We sought to characterize C9orf72 expansions in relation to genetic ancestry and age at onset (AAO) and to use these measures to discriminate the behavioral from the language variant syndrome in a large pan-European cohort of frontotemporal lobar degeneration (FTLD) cases. METHODS: We eva...

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Autores principales: Costa, Beatrice, Manzoni, Claudia, Bernal-Quiros, Manuel, Kia, Demis A., Aguilar, Miquel, Alvarez, Ignacio, Alvarez, Victoria, Andreassen, Ole, Anfossi, Maria, Bagnoli, Silvia, Benussi, Luisa, Bernardi, Livia, Binetti, Giuliano, Blackburn, Daniel, Boada, Mercè, Borroni, Barbara, Bowns, Lucy, Bråthen, Geir, Bruni, Amalia C., Chiang, Huei-Hsin, Clarimon, Jordi, Colville, Shuna, Conidi, Maria E., Cope, Tom E., Cruchaga, Carlos, Cupidi, Chiara, Di Battista, Maria Elena, Diehl-Schmid, Janine, Diez-Fairen, Monica, Dols-Icardo, Oriol, Durante, Elisabetta, Flisar, Dušan, Frangipane, Francesca, Galimberti, Daniela, Gallo, Maura, Gallucci, Maurizio, Ghidoni, Roberta, Graff, Caroline, Grafman, Jordan H., Grossman, Murray, Hardy, John, Hernández, Isabel, Holloway, Guy J.T., Huey, Edward D., Illán-Gala, Ignacio, Karydas, Anna, Khoshnood, Behzad, Kramberger, Milica G., Kristiansen, Mark, Lewis, Patrick A., Lleó, Alberto, Madhan, Gaganjit K., Maletta, Raffaele, Maver, Aleš, Menendez-Gonzalez, Manuel, Milan, Graziella, Miller, Bruce, Mol, Merel O., Momeni, Parastoo, Moreno-Grau, Sonia, Morris, Chris M., Nacmias, Benedetta, Nilsson, Christer, Novelli, Valeria, Öijerstedt, Linn, Padovani, Alessandro, Pal, Suvankar, Panchbhaya, Yasmin, Pastor, Pau, Peterlin, Borut, Piaceri, Irene, Pickering-Brown, Stuart, Pijnenburg, Yolande A.L., Puca, Annibale A., Rainero, Innocenzo, Rendina, Antonella, Richardson, Anna M.T., Rogaeva, Ekaterina, Rogelj, Boris, Rollinson, Sara, Rossi, Giacomina, Rossmeier, Carola, Rowe, James B., Rubino, Elisa, Ruiz, Agustín, Sanchez-Valle, Raquel, Sando, Sigrid B., Santillo, Alexander F., Saxon, Jennifer, Scarpini, Elio, Serpente, Maria, Smirne, Nicoletta, Sorbi, Sandro, Suh, EunRan, Tagliavini, Fabrizio, Thompson, Jennifer C., Trojanowski, John Q., Van Deerlin, Vivianna M., Van der Zee, Julie, Van Broeckhoven, Christine, van Rooij, Jeroen, Van Swieten, John C., Veronesi, Arianna, Vitale, Emilia, Waldö, Maria L., Woodward, Cathy, Yokoyama, Jennifer, Escott-Price, Valentina, Polke, James M., Ferrari, Raffaele
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Lippincott Williams & Wilkins 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7836664/
https://www.ncbi.nlm.nih.gov/pubmed/32943482
http://dx.doi.org/10.1212/WNL.0000000000010914
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author Costa, Beatrice
Manzoni, Claudia
Bernal-Quiros, Manuel
Kia, Demis A.
Aguilar, Miquel
Alvarez, Ignacio
Alvarez, Victoria
Andreassen, Ole
Anfossi, Maria
Bagnoli, Silvia
Benussi, Luisa
Bernardi, Livia
Binetti, Giuliano
Blackburn, Daniel
Boada, Mercè
Borroni, Barbara
Bowns, Lucy
Bråthen, Geir
Bruni, Amalia C.
Chiang, Huei-Hsin
Clarimon, Jordi
Colville, Shuna
Conidi, Maria E.
Cope, Tom E.
Cruchaga, Carlos
Cupidi, Chiara
Di Battista, Maria Elena
Diehl-Schmid, Janine
Diez-Fairen, Monica
Dols-Icardo, Oriol
Durante, Elisabetta
Flisar, Dušan
Frangipane, Francesca
Galimberti, Daniela
Gallo, Maura
Gallucci, Maurizio
Ghidoni, Roberta
Graff, Caroline
Grafman, Jordan H.
Grossman, Murray
Hardy, John
Hernández, Isabel
Holloway, Guy J.T.
Huey, Edward D.
Illán-Gala, Ignacio
Karydas, Anna
Khoshnood, Behzad
Kramberger, Milica G.
Kristiansen, Mark
Lewis, Patrick A.
Lleó, Alberto
Madhan, Gaganjit K.
Maletta, Raffaele
Maver, Aleš
Menendez-Gonzalez, Manuel
Milan, Graziella
Miller, Bruce
Mol, Merel O.
Momeni, Parastoo
Moreno-Grau, Sonia
Morris, Chris M.
Nacmias, Benedetta
Nilsson, Christer
Novelli, Valeria
Öijerstedt, Linn
Padovani, Alessandro
Pal, Suvankar
Panchbhaya, Yasmin
Pastor, Pau
Peterlin, Borut
Piaceri, Irene
Pickering-Brown, Stuart
Pijnenburg, Yolande A.L.
Puca, Annibale A.
Rainero, Innocenzo
Rendina, Antonella
Richardson, Anna M.T.
Rogaeva, Ekaterina
Rogelj, Boris
Rollinson, Sara
Rossi, Giacomina
Rossmeier, Carola
Rowe, James B.
Rubino, Elisa
Ruiz, Agustín
Sanchez-Valle, Raquel
Sando, Sigrid B.
Santillo, Alexander F.
Saxon, Jennifer
Scarpini, Elio
Serpente, Maria
Smirne, Nicoletta
Sorbi, Sandro
Suh, EunRan
Tagliavini, Fabrizio
Thompson, Jennifer C.
Trojanowski, John Q.
Van Deerlin, Vivianna M.
Van der Zee, Julie
Van Broeckhoven, Christine
van Rooij, Jeroen
Van Swieten, John C.
Veronesi, Arianna
Vitale, Emilia
Waldö, Maria L.
Woodward, Cathy
Yokoyama, Jennifer
Escott-Price, Valentina
Polke, James M.
Ferrari, Raffaele
author_facet Costa, Beatrice
Manzoni, Claudia
Bernal-Quiros, Manuel
Kia, Demis A.
Aguilar, Miquel
Alvarez, Ignacio
Alvarez, Victoria
Andreassen, Ole
Anfossi, Maria
Bagnoli, Silvia
Benussi, Luisa
Bernardi, Livia
Binetti, Giuliano
Blackburn, Daniel
Boada, Mercè
Borroni, Barbara
Bowns, Lucy
Bråthen, Geir
Bruni, Amalia C.
Chiang, Huei-Hsin
Clarimon, Jordi
Colville, Shuna
Conidi, Maria E.
Cope, Tom E.
Cruchaga, Carlos
Cupidi, Chiara
Di Battista, Maria Elena
Diehl-Schmid, Janine
Diez-Fairen, Monica
Dols-Icardo, Oriol
Durante, Elisabetta
Flisar, Dušan
Frangipane, Francesca
Galimberti, Daniela
Gallo, Maura
Gallucci, Maurizio
Ghidoni, Roberta
Graff, Caroline
Grafman, Jordan H.
Grossman, Murray
Hardy, John
Hernández, Isabel
Holloway, Guy J.T.
Huey, Edward D.
Illán-Gala, Ignacio
Karydas, Anna
Khoshnood, Behzad
Kramberger, Milica G.
Kristiansen, Mark
Lewis, Patrick A.
Lleó, Alberto
Madhan, Gaganjit K.
Maletta, Raffaele
Maver, Aleš
Menendez-Gonzalez, Manuel
Milan, Graziella
Miller, Bruce
Mol, Merel O.
Momeni, Parastoo
Moreno-Grau, Sonia
Morris, Chris M.
Nacmias, Benedetta
Nilsson, Christer
Novelli, Valeria
Öijerstedt, Linn
Padovani, Alessandro
Pal, Suvankar
Panchbhaya, Yasmin
Pastor, Pau
Peterlin, Borut
Piaceri, Irene
Pickering-Brown, Stuart
Pijnenburg, Yolande A.L.
Puca, Annibale A.
Rainero, Innocenzo
Rendina, Antonella
Richardson, Anna M.T.
Rogaeva, Ekaterina
Rogelj, Boris
Rollinson, Sara
Rossi, Giacomina
Rossmeier, Carola
Rowe, James B.
Rubino, Elisa
Ruiz, Agustín
Sanchez-Valle, Raquel
Sando, Sigrid B.
Santillo, Alexander F.
Saxon, Jennifer
Scarpini, Elio
Serpente, Maria
Smirne, Nicoletta
Sorbi, Sandro
Suh, EunRan
Tagliavini, Fabrizio
Thompson, Jennifer C.
Trojanowski, John Q.
Van Deerlin, Vivianna M.
Van der Zee, Julie
Van Broeckhoven, Christine
van Rooij, Jeroen
Van Swieten, John C.
Veronesi, Arianna
Vitale, Emilia
Waldö, Maria L.
Woodward, Cathy
Yokoyama, Jennifer
Escott-Price, Valentina
Polke, James M.
Ferrari, Raffaele
author_sort Costa, Beatrice
collection PubMed
description OBJECTIVE: We sought to characterize C9orf72 expansions in relation to genetic ancestry and age at onset (AAO) and to use these measures to discriminate the behavioral from the language variant syndrome in a large pan-European cohort of frontotemporal lobar degeneration (FTLD) cases. METHODS: We evaluated expansions frequency in the entire cohort (n = 1,396; behavioral variant frontotemporal dementia [bvFTD] [n = 800], primary progressive aphasia [PPA] [n = 495], and FTLD–motor neuron disease [MND] [n = 101]). We then focused on the bvFTD and PPA cases and tested for association between expansion status, syndromes, genetic ancestry, and AAO applying statistical tests comprising Fisher exact tests, analysis of variance with Tukey post hoc tests, and logistic and nonlinear mixed-effects model regressions. RESULTS: We found C9orf72 pathogenic expansions in 4% of all cases (56/1,396). Expansion carriers differently distributed across syndromes: 12/101 FTLD-MND (11.9%), 40/800 bvFTD (5%), and 4/495 PPA (0.8%). While addressing population substructure through principal components analysis (PCA), we defined 2 patients groups with Central/Northern (n = 873) and Southern European (n = 523) ancestry. The proportion of expansion carriers was significantly higher in bvFTD compared to PPA (5% vs 0.8% [p = 2.17 × 10(−5); odds ratio (OR) 6.4; confidence interval (CI) 2.31–24.99]), as well as in individuals with Central/Northern European compared to Southern European ancestry (4.4% vs 1.8% [p = 1.1 × 10(−2); OR 2.5; CI 1.17–5.99]). Pathogenic expansions and Central/Northern European ancestry independently and inversely correlated with AAO. Our prediction model (based on expansions status, genetic ancestry, and AAO) predicted a diagnosis of bvFTD with 64% accuracy. CONCLUSIONS: Our results indicate correlation between pathogenic C9orf72 expansions, AAO, PCA-based Central/Northern European ancestry, and a diagnosis of bvFTD, implying complex genetic risk architectures differently underpinning the behavioral and language variant syndromes.
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spelling pubmed-78366642021-01-27 C9orf72, age at onset, and ancestry help discriminate behavioral from language variants in FTLD cohorts Costa, Beatrice Manzoni, Claudia Bernal-Quiros, Manuel Kia, Demis A. Aguilar, Miquel Alvarez, Ignacio Alvarez, Victoria Andreassen, Ole Anfossi, Maria Bagnoli, Silvia Benussi, Luisa Bernardi, Livia Binetti, Giuliano Blackburn, Daniel Boada, Mercè Borroni, Barbara Bowns, Lucy Bråthen, Geir Bruni, Amalia C. Chiang, Huei-Hsin Clarimon, Jordi Colville, Shuna Conidi, Maria E. Cope, Tom E. Cruchaga, Carlos Cupidi, Chiara Di Battista, Maria Elena Diehl-Schmid, Janine Diez-Fairen, Monica Dols-Icardo, Oriol Durante, Elisabetta Flisar, Dušan Frangipane, Francesca Galimberti, Daniela Gallo, Maura Gallucci, Maurizio Ghidoni, Roberta Graff, Caroline Grafman, Jordan H. Grossman, Murray Hardy, John Hernández, Isabel Holloway, Guy J.T. Huey, Edward D. Illán-Gala, Ignacio Karydas, Anna Khoshnood, Behzad Kramberger, Milica G. Kristiansen, Mark Lewis, Patrick A. Lleó, Alberto Madhan, Gaganjit K. Maletta, Raffaele Maver, Aleš Menendez-Gonzalez, Manuel Milan, Graziella Miller, Bruce Mol, Merel O. Momeni, Parastoo Moreno-Grau, Sonia Morris, Chris M. Nacmias, Benedetta Nilsson, Christer Novelli, Valeria Öijerstedt, Linn Padovani, Alessandro Pal, Suvankar Panchbhaya, Yasmin Pastor, Pau Peterlin, Borut Piaceri, Irene Pickering-Brown, Stuart Pijnenburg, Yolande A.L. Puca, Annibale A. Rainero, Innocenzo Rendina, Antonella Richardson, Anna M.T. Rogaeva, Ekaterina Rogelj, Boris Rollinson, Sara Rossi, Giacomina Rossmeier, Carola Rowe, James B. Rubino, Elisa Ruiz, Agustín Sanchez-Valle, Raquel Sando, Sigrid B. Santillo, Alexander F. Saxon, Jennifer Scarpini, Elio Serpente, Maria Smirne, Nicoletta Sorbi, Sandro Suh, EunRan Tagliavini, Fabrizio Thompson, Jennifer C. Trojanowski, John Q. Van Deerlin, Vivianna M. Van der Zee, Julie Van Broeckhoven, Christine van Rooij, Jeroen Van Swieten, John C. Veronesi, Arianna Vitale, Emilia Waldö, Maria L. Woodward, Cathy Yokoyama, Jennifer Escott-Price, Valentina Polke, James M. Ferrari, Raffaele Neurology Article OBJECTIVE: We sought to characterize C9orf72 expansions in relation to genetic ancestry and age at onset (AAO) and to use these measures to discriminate the behavioral from the language variant syndrome in a large pan-European cohort of frontotemporal lobar degeneration (FTLD) cases. METHODS: We evaluated expansions frequency in the entire cohort (n = 1,396; behavioral variant frontotemporal dementia [bvFTD] [n = 800], primary progressive aphasia [PPA] [n = 495], and FTLD–motor neuron disease [MND] [n = 101]). We then focused on the bvFTD and PPA cases and tested for association between expansion status, syndromes, genetic ancestry, and AAO applying statistical tests comprising Fisher exact tests, analysis of variance with Tukey post hoc tests, and logistic and nonlinear mixed-effects model regressions. RESULTS: We found C9orf72 pathogenic expansions in 4% of all cases (56/1,396). Expansion carriers differently distributed across syndromes: 12/101 FTLD-MND (11.9%), 40/800 bvFTD (5%), and 4/495 PPA (0.8%). While addressing population substructure through principal components analysis (PCA), we defined 2 patients groups with Central/Northern (n = 873) and Southern European (n = 523) ancestry. The proportion of expansion carriers was significantly higher in bvFTD compared to PPA (5% vs 0.8% [p = 2.17 × 10(−5); odds ratio (OR) 6.4; confidence interval (CI) 2.31–24.99]), as well as in individuals with Central/Northern European compared to Southern European ancestry (4.4% vs 1.8% [p = 1.1 × 10(−2); OR 2.5; CI 1.17–5.99]). Pathogenic expansions and Central/Northern European ancestry independently and inversely correlated with AAO. Our prediction model (based on expansions status, genetic ancestry, and AAO) predicted a diagnosis of bvFTD with 64% accuracy. CONCLUSIONS: Our results indicate correlation between pathogenic C9orf72 expansions, AAO, PCA-based Central/Northern European ancestry, and a diagnosis of bvFTD, implying complex genetic risk architectures differently underpinning the behavioral and language variant syndromes. Lippincott Williams & Wilkins 2020-12-15 /pmc/articles/PMC7836664/ /pubmed/32943482 http://dx.doi.org/10.1212/WNL.0000000000010914 Text en Copyright © 2020 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology. https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License 4.0 (CC BY) (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Article
Costa, Beatrice
Manzoni, Claudia
Bernal-Quiros, Manuel
Kia, Demis A.
Aguilar, Miquel
Alvarez, Ignacio
Alvarez, Victoria
Andreassen, Ole
Anfossi, Maria
Bagnoli, Silvia
Benussi, Luisa
Bernardi, Livia
Binetti, Giuliano
Blackburn, Daniel
Boada, Mercè
Borroni, Barbara
Bowns, Lucy
Bråthen, Geir
Bruni, Amalia C.
Chiang, Huei-Hsin
Clarimon, Jordi
Colville, Shuna
Conidi, Maria E.
Cope, Tom E.
Cruchaga, Carlos
Cupidi, Chiara
Di Battista, Maria Elena
Diehl-Schmid, Janine
Diez-Fairen, Monica
Dols-Icardo, Oriol
Durante, Elisabetta
Flisar, Dušan
Frangipane, Francesca
Galimberti, Daniela
Gallo, Maura
Gallucci, Maurizio
Ghidoni, Roberta
Graff, Caroline
Grafman, Jordan H.
Grossman, Murray
Hardy, John
Hernández, Isabel
Holloway, Guy J.T.
Huey, Edward D.
Illán-Gala, Ignacio
Karydas, Anna
Khoshnood, Behzad
Kramberger, Milica G.
Kristiansen, Mark
Lewis, Patrick A.
Lleó, Alberto
Madhan, Gaganjit K.
Maletta, Raffaele
Maver, Aleš
Menendez-Gonzalez, Manuel
Milan, Graziella
Miller, Bruce
Mol, Merel O.
Momeni, Parastoo
Moreno-Grau, Sonia
Morris, Chris M.
Nacmias, Benedetta
Nilsson, Christer
Novelli, Valeria
Öijerstedt, Linn
Padovani, Alessandro
Pal, Suvankar
Panchbhaya, Yasmin
Pastor, Pau
Peterlin, Borut
Piaceri, Irene
Pickering-Brown, Stuart
Pijnenburg, Yolande A.L.
Puca, Annibale A.
Rainero, Innocenzo
Rendina, Antonella
Richardson, Anna M.T.
Rogaeva, Ekaterina
Rogelj, Boris
Rollinson, Sara
Rossi, Giacomina
Rossmeier, Carola
Rowe, James B.
Rubino, Elisa
Ruiz, Agustín
Sanchez-Valle, Raquel
Sando, Sigrid B.
Santillo, Alexander F.
Saxon, Jennifer
Scarpini, Elio
Serpente, Maria
Smirne, Nicoletta
Sorbi, Sandro
Suh, EunRan
Tagliavini, Fabrizio
Thompson, Jennifer C.
Trojanowski, John Q.
Van Deerlin, Vivianna M.
Van der Zee, Julie
Van Broeckhoven, Christine
van Rooij, Jeroen
Van Swieten, John C.
Veronesi, Arianna
Vitale, Emilia
Waldö, Maria L.
Woodward, Cathy
Yokoyama, Jennifer
Escott-Price, Valentina
Polke, James M.
Ferrari, Raffaele
C9orf72, age at onset, and ancestry help discriminate behavioral from language variants in FTLD cohorts
title C9orf72, age at onset, and ancestry help discriminate behavioral from language variants in FTLD cohorts
title_full C9orf72, age at onset, and ancestry help discriminate behavioral from language variants in FTLD cohorts
title_fullStr C9orf72, age at onset, and ancestry help discriminate behavioral from language variants in FTLD cohorts
title_full_unstemmed C9orf72, age at onset, and ancestry help discriminate behavioral from language variants in FTLD cohorts
title_short C9orf72, age at onset, and ancestry help discriminate behavioral from language variants in FTLD cohorts
title_sort c9orf72, age at onset, and ancestry help discriminate behavioral from language variants in ftld cohorts
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7836664/
https://www.ncbi.nlm.nih.gov/pubmed/32943482
http://dx.doi.org/10.1212/WNL.0000000000010914
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