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1. An Automated Toolbox to Predict Single Subject Atrophy in Presymptomatic Granulin Mutation Carriers

Author

Premi, Enrico, Costa, Tommaso, Moreno, Fermin, Panman, Jessica, Papma, Janne, Pievani, Michela, Pijnenburg, Yolande, Polito, Cristina, Prioni, Sara, Prix, Catharina, Rademakers As London Ontario Geneticist, Rosa, Redaelli, Veronica, Rittman, Tim, Santana, Isabel, Rogaeva, Ekaterina, Rosa-Neto, Pedro, Rossi, Giacomina, Rossor, Martin, Santiago, Beatriz, Scarpini, Elio, Schönecker, Sonja, Semler, Elisa, Shafei, Rachelle, Shoesmith, Christen, Laforce, Robert, Tábuas-Pereira, Miguel, Tainta, Mikel, Taipa, Ricardo, Tang-Wai, David, L Thomas, David, Thompson, Paul, Thonberg, Hakan, Timberlake, Carolyn, Tiraboschi, Pietro, Van Damme, Philip, Ducharme, Simon, Vandenbulcke, Mathieu, Veldsman, Michele, Verdelho, Ana, Villanua, Jorge, Warren, Jason, Wilke, Carlo, Woollacott, Ione, Wlasich, Elisabeth, Zetterberg, Henrik, Zulaica, Miren, Graff, Caroline, Galimberti, Daniela, Masellis, Mario, Tartaglia, Carmela, Rowe, James B, Finger, Elizabeth, Gazzina, Stefano, Tagliavini, Fabrizio, de Mendonça, Alexandre, Vandenberghe, Rik, Gerhard, Alexander, Butler, Chris R, Danek, Adrian, Synofzik, Matthis, Levin, Johannes, Otto, Markus, Ghidoni, Roberta, Benussi, Alberto, Frisoni, Giovanni B, Sorbi, Sandro, Peakman, Georgia, Todd, Emily, Bocchetta, Martina, Rohrer, Johnathan D, Borroni, Barbara, Members, GENFI Consortium, Afonso, Sónia, Rosario Almeida, Maria, Cauda, Franco, Anderl-Straub, Sarah, Andersson, Christin, Antonell, Anna, Arighi, Andrea, Balasa, Mircea, Barandiaran, Myriam, Bargalló, Nuria, Bartha, Robart, Bender, Benjamin, Benussi, Luisa, Gasparotti, Roberto, Bessi, Valentina, Binetti, Giuliano, Black, Sandra, Borrego-Ecija, Sergi, Bras, Jose, Bruffaerts, Rose, Caroppo, Paola, Cash, David, Castelo-Branco, Miguel, Convery, Rhian, Archetti, Silvana, Cope, Thomas, de Arriba, María, Di Fede, Giuseppe, Díaz, Zigor, Duro, Diana, Fenoglio, Chiara, Ferrari, Camilla, B Ferreira, Catarina, Fox, Nick, Freedman, Morris, Alberici, Antonella, Fumagalli, Giorgio, Gabilondo, Alazne, Gauthier, Serge, Giaccone, Giorgio, Gorostidi, Ana, Greaves, Caroline, Guerreiro, Rita, Heller, Carolin, Hoegen, Tobias, Indakoetxea, Begoña, van Swieten, John C, Jelic, Vesna, Jiskoot, Lize, Karnath, Hans Otto, Keren, Ron, Langheinrich, Tobias, João Leitão, Maria, Lladó, Albert, Lombardi, Gemma, Loosli, Sandra, Maruta, Carolina, Sanchez-Valle, Raquel, Mead, Simon, Meeter, Lieke, Miltenberger, Gabriel, van Minkelen, Rick, Mitchell, Sara, Moore, Katrina, Nacmias, Benedetta, Nicholas, Jennifer, Öijerstedt, Linn, Olives, Jaume, GENFI Consortium Members, Neurology, Rowe, James [0000-0001-7216-8679], and Apollo - University of Cambridge Repository

Subjects
genetics [Granulins], Frontotemporal dementia, granulin, magnetic resonance imaging, mutation, preclinical, presymptomatic, Atrophy, Brain, Granulins, Humans, Magnetic Resonance Imaging, Mutation, Progranulins, Frontotemporal Dementia, Medizin, genetics [Mutation], diagnostic imaging [Frontotemporal Dementia], frontotemporal dementia, genetics [Progranulins], methods [Magnetic Resonance Imaging], SDG 3 - Good Health and Well-being, pathology [Brain], Settore BIO/13 - Biologia Applicata, ddc:610, diagnostic imaging [Brain], genetics [Frontotemporal Dementia], pathology [Atrophy], Frontotemporal dementia, granulin, magnetic resonance imaging, mutation, preclinical, presymptomatic, General Neuroscience, General Medicine, Psychiatry and Mental health, Clinical Psychology, pathology [Frontotemporal Dementia], Geriatrics and Gerontology
Abstract

Background:Magnetic resonance imaging (MRI) measures may be used as outcome markers in frontotemporal dementia (FTD). Objectives:To predict MRI cortical thickness (CT) at follow-up at the single subject level, using brain MRI acquired at baseline in preclinical FTD. Methods:84 presymptomatic subjects carrying Granulin mutations underwent MRI scans at baseline and at follow-up (31.2±16.5 months). Multivariate nonlinear mixed-effects model was used for estimating individualized CT at follow-up based on baseline MRI data. The automated user-friendly preGRN-MRI script was coded. Results:Prediction accuracy was high for each considered brain region (i.e., prefrontal region, real CT at follow-up versus predicted CT at follow-up, mean error ≤1.87%). The sample size required to detect a reduction in decline in a 1-year clinical trial was equal to 52 subjects (power = 0.80, alpha = 0.05). Conclusion:The preGRN-MRI tool, using baseline MRI measures, was able to predict the expected MRI atrophy at follow-up in presymptomatic subjects carrying GRN mutations with good performances. This tool could be useful in clinical trials, where deviation of CT from the predicted model may be considered an effect of the intervention itself. Swedish Frontotemporal Dementia Initiative Schörling Foundation; Swedish Research Council: JPND Prefrontals, 2015-02926 ,2018-02754; Swedish Alzheimer foundation; Swedish Brain Foundation; Karolinska Institutet Doctoral Funding; KI StratNeuro; Swedish Dementia foundation and Stockholm County Council ALF/Region Stockholm.

Published
2022
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2. Error in Article Information

Author

Benussi, Alberto, Premi, Enrico, Laforce, Robert, Lladò, Albert, Lombardi, Gemma, Loosli, Sandra, Maruta, Carolina, Mead, Simon, Meeter, Lieke, Miltenberger, Gabriel, van Minkelen, Rick, Mitchell, Sara, Moore, Katrina, Graff, Caroline, Nacmias, Benedetta, Nicholas, Jennifer, Öijerstedt, Linn, Olives, Jaume, Ourselin, Sebastien, Padovani, Alessandro, Panman, Jessica, M Papma, Janne, Pievani, Michela, Pijnenburg, Yolande, Synofzik, Matthis, Polito, Cristina, Prioni, Sara, Prix, Catharina, Rademakers, Rosa, Redaelli, Veronica, Rinaldi, Daisy, Rittman, Tim, Rogaeva, Ekaterina, Rollin, Adeline, Rosa-Neto, Pedro, Galimberti, Daniela, Rossi, Giacomina, Rossor, Martin, Santiago, Beatriz, Saracino, Dario, Sayah, Sabrina, Scarpini, Elio, Schönecker, Sonja, Seelaar, Harro, Semler, Elisa, Shafei, Rachelle, Masellis, Mario, Shoesmith, Christen, Tábuas-Pereira, Miguel, Tainta, Mikel, Taipa, Ricardo, Tang-Wai, David, L Thomas, David, Thompson, Paul, Thonberg, Hakan, Timberlake, Carolyn, Tiraboschi, Pietro, Tartaglia, Carmela, Todd, Emily, Van Damme, Philip, Vandenbulcke, Mathieu, Veldsman, Michele, Verdelho, Ana, Villanua, Jorge, Warren, Jason, Wilke, Carlo, Woollacott, Ione, Wlasich, Elisabeth, Rowe, James B, Zetterberg, Henrik, Zulaica, Miren, Finger, Elizabeth, Vandenberghe, Rik, de Mendonça, Alexandre, Gazzina, Stefano, Tagliavini, Fabrizio, Santana, Isabel, Ducharme, Simon, Butler, Chris R, Gerhard, Alexander, Levin, Johannes, Danek, Adrian, Otto, Markus, Frisoni, Giovanni, Ghidoni, Roberta, Brattini, Chiara, Sorbi, Sandro, Le Ber, Isabelle, Pasquier, Florence, Peakman, Georgia, Bocchetta, Martina, Rohrer, Jonathan D, Borroni, Barbara, Initiative, Genetic FTD, Afonso, Sònia, Bonomi, Elisa, Rosario Almeida, Maria, Anderl-Straub, Sarah, Andersson, Christin, Antonell, Anna, Archetti, Silvana, Arighi, Andrea, Balasa, Mircea, Barandiaran, Myriam, Bargallò, Nuria, Bartha, Robart, Alberici, Antonella, Bender, Benjamin, Benussi, Luisa, Bertoux, Maxime, Bertrand, Anne, Bessi, Valentina, Binetti, Giuliano, Black, Sandra, Borrego-Ecija, Sergi, Bras, Jose, Brice, Alexis, Jiskoot, Lize, Bruffaerts, Rose, Camuzat, Agnès, Cañada, Marta, Caroppo, Paola, Cash, David, Castelo-Branco, Miguel, Colliot, Olivier, Convery, Rhian, Cope, Thomas, Cosseddu, Maura, van Swieten, John C, Deramecourt, Vincent, de Arriba, Marìa, Di Fede, Giuseppe, Dìez, Alina, Duro, Diana, Fenoglio, Chiara, Ferrari, Camilla, B Ferreira, Catarina, Fox, Nick, Freedman, Morris, Sanchez-Valle, Raquel, Fumagalli, Giorgio, Funkiewiez, Aurélie, Gabilondo, Alazne, Gasparotti, Roberto, Gauthier, Serge, Giaccone, Giorgio, Gorostidi, Ana, Greaves, Caroline, Guerreiro, Rita, Moreno, Fermin, Heller, Carolin, Hoegen, Tobias, Indakoetxea, Begoña, Jelic, Vesna, Karnath, Hans-Otto, Keren, Ron, Kuchcinski, Gregory, Langheinrich, Tobias, Lebouvier, Thibaud, and João Leitão, Maria

Subjects
ddc:610
Published
2021
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3. Progression of Behavioral Disturbances and Neuropsychiatric Symptoms in Patients With Genetic Frontotemporal Dementia

Author

Benussi, Alberto, Premi, Enrico, Laforce, Robert, Lladò, Albert, Lombardi, Gemma, Loosli, Sandra, Maruta, Carolina, Mead, Simon, Meeter, Lieke, Miltenberger, Gabriel, van Minkelen, Rick, Mitchell, Sara, Moore, Katrina, Graff, Caroline, Nacmias, Benedetta, Nicholas, Jennifer, Öijerstedt, Linn, Olives, Jaume, Ourselin, Sebastien, Padovani, Alessandro, Panman, Jessica, M Papma, Janne, Pievani, Michela, Pijnenburg, Yolande, Synofzik, Matthis, Polito, Cristina, Prioni, Sara, Prix, Catharina, Rademakers, Rosa, Redaelli, Veronica, Rinaldi, Daisy, Rittman, Tim, Rogaeva, Ekaterina, Rollin, Adeline, Rosa-Neto, Pedro, Galimberti, Daniela, Rossi, Giacomina, Rossor, Martin, Santiago, Beatriz, Saracino, Dario, Sayah, Sabrina, Scarpini, Elio, Schönecker, Sonja, Seelaar, Harro, Semler, Elisa, Shafei, Rachelle, Masellis, Mario, Shoesmith, Christen, Tábuas-Pereira, Miguel, Tainta, Mikel, Taipa, Ricardo, Tang-Wai, David, L Thomas, David, Thompson, Paul, Thonberg, Hakan, Timberlake, Carolyn, Tiraboschi, Pietro, Tartaglia, Carmela, Todd, Emily, Van Damme, Philip, Vandenbulcke, Mathieu, Veldsman, Michele, Verdelho, Ana, Villanua, Jorge, Warren, Jason, Wilke, Carlo, Woollacott, Ione, Wlasich, Elisabeth, Rowe, James B, Zetterberg, Henrik, Zulaica, Miren, Finger, Elizabeth, Vandenberghe, Rik, de Mendonça, Alexandre, Gazzina, Stefano, Tagliavini, Fabrizio, Santana, Isabel, Ducharme, Simon, Butler, Chris R, Gerhard, Alexander, Levin, Johannes, Danek, Adrian, Otto, Markus, Frisoni, Giovanni, Ghidoni, Roberta, Brattini, Chiara, Sorbi, Sandro, Le Ber, Isabelle, Pasquier, Florence, Peakman, Georgia, Bocchetta, Martina, Rohrer, Jonathan D, Borroni, Barbara, Initiative, Genetic FTD, Afonso, Sònia, Bonomi, Elisa, Rosario Almeida, Maria, Anderl-Straub, Sarah, Andersson, Christin, Antonell, Anna, Archetti, Silvana, Arighi, Andrea, Balasa, Mircea, Barandiaran, Myriam, Bargallò, Nuria, Bartha, Robart, Alberici, Antonella, Bender, Benjamin, Benussi, Luisa, Bertoux, Maxime, Bertrand, Anne, Bessi, Valentina, Binetti, Giuliano, Black, Sandra, Borrego-Ecija, Sergi, Bras, Jose, Brice, Alexis, Jiskoot, Lize, Bruffaerts, Rose, Camuzat, Agnès, Cañada, Marta, Caroppo, Paola, Cash, David, Castelo-Branco, Miguel, Colliot, Olivier, Convery, Rhian, Cope, Thomas, Cosseddu, Maura, van Swieten, John C, Deramecourt, Vincent, de Arriba, Marìa, Di Fede, Giuseppe, Dìez, Alina, Duro, Diana, Fenoglio, Chiara, Ferrari, Camilla, B Ferreira, Catarina, Fox, Nick, Freedman, Morris, Sanchez-Valle, Raquel, Fumagalli, Giorgio, Funkiewiez, Aurélie, Gabilondo, Alazne, Gasparotti, Roberto, Gauthier, Serge, Giaccone, Giorgio, Gorostidi, Ana, Greaves, Caroline, Guerreiro, Rita, Moreno, Fermin, Heller, Carolin, Hoegen, Tobias, Indakoetxea, Begoña, Jelic, Vesna, Karnath, Hans-Otto, Keren, Ron, Kuchcinski, Gregory, Langheinrich, Tobias, Lebouvier, Thibaud, João Leitão, Maria, Genetic FTD Initiative (GENFI), Repositório da Universidade de Lisboa, Neurology, Rowe, James [0000-0001-7216-8679], and Apollo - University of Cambridge Repository

Subjects
Male, Longitudinal study, Pediatrics, Hallucinations, FEATURES, VARIANT, Medizin, Anxiety, physiopathology [Frontotemporal Dementia], 0302 clinical medicine, Interquartile range, Medicine, Apathy, Longitudinal Studies, genetics [Frontotemporal Dementia], Depression (differential diagnoses), Granulins, Original Investigation, Depression, Aged, C9orf72 Protein, Canada, Compulsive Behavior, Disease Progression, Europe, Female, Humans, Middle Aged, tau Proteins, Frontotemporal Dementia, General Medicine, 3. Good health, Online Only, Neurology, Compulsive behavior, medicine.symptom, Life Sciences & Biomedicine, Frontotemporal dementia, Cohort study, medicine.medical_specialty, genetics [Granulins], DIAGNOSTIC-CRITERIA, epidemiology [Frontotemporal Dementia], MAPT protein, human, 03 medical and health sciences, Medicine, General & Internal, 030225 pediatrics, General & Internal Medicine, mental disorders, ddc:610, LOBAR DEGENERATION, genetics [C9orf72 Protein], Science & Technology, business.industry, Research, DISEASE PROGRESSION, Correction, medicine.disease, genetics [tau Proteins], ONSET, Other, C9orf72 protein, human, business, 030217 neurology & neurosurgery
Abstract

© 2021 Benussi A et al. JAMA Network Open. This is an open access article distributed under the terms of the CC-BY License., Importance: Behavioral disturbances are core features of frontotemporal dementia (FTD); however, symptom progression across the course of disease is not well characterized in genetic FTD. Objective: To investigate behavioral symptom frequency and severity and their evolution and progression in different forms of genetic FTD. Design, setting, and participants: This longitudinal cohort study, the international Genetic FTD Initiative (GENFI), was conducted from January 30, 2012, to May 31, 2019, at 23 multicenter specialist tertiary FTD research clinics in the United Kingdom, the Netherlands, Belgium, France, Spain, Portugal, Italy, Germany, Sweden, Finland, and Canada. Participants included a consecutive sample of 232 symptomatic FTD gene variation carriers comprising 115 with variations in C9orf72, 78 in GRN, and 39 in MAPT. A total of 101 carriers had at least 1 follow-up evaluation (for a total of 400 assessments). Gene variations were included only if considered pathogenetic. Main outcomes and measures: Behavioral and neuropsychiatric symptoms were assessed across disease duration and evaluated from symptom onset. Hierarchical generalized linear mixed models were used to model behavioral and neuropsychiatric measures as a function of disease duration and variation. Results: Of 232 patients with FTD, 115 (49.6%) had a C9orf72 expansion (median [interquartile range (IQR)] age at evaluation, 64.3 [57.5-69.7] years; 72 men [62.6%]; 115 White patients [100%]), 78 (33.6%) had a GRN variant (median [IQR] age, 63.4 [58.3-68.8] years; 40 women [51.3%]; 77 White patients [98.7%]), and 39 (16.8%) had a MAPT variant (median [IQR] age, 56.3 [49.9-62.4] years; 25 men [64.1%]; 37 White patients [94.9%]). All core behavioral symptoms, including disinhibition, apathy, loss of empathy, perseverative behavior, and hyperorality, were highly expressed in all gene variant carriers (>50% patients), with apathy being one of the most common and severe symptoms throughout the disease course (51.7%-100% of patients). Patients with MAPT variants showed the highest frequency and severity of most behavioral symptoms, particularly disinhibition (79.3%-100% of patients) and compulsive behavior (64.3%-100% of patients), compared with C9orf72 carriers (51.7%-95.8% of patients with disinhibition and 34.5%-75.0% with compulsive behavior) and GRN carriers (38.2%-100% with disinhibition and 20.6%-100% with compulsive behavior). Alongside behavioral symptoms, neuropsychiatric symptoms were very frequently reported in patients with genetic FTD: anxiety and depression were most common in GRN carriers (23.8%-100% of patients) and MAPT carriers (26.1%-77.8% of patients); hallucinations, particularly auditory and visual, were most common in C9orf72 carriers (10.3%-54.5% of patients). Most behavioral and neuropsychiatric symptoms increased in the early-intermediate phases and plateaued in the late stages of disease, except for depression, which steadily declined in C9orf72 carriers, and depression and anxiety, which surged only in the late stages in GRN carriers. Conclusions and relevance: This cohort study suggests that behavioral and neuropsychiatric disturbances differ between the common FTD gene variants and have different trajectories throughout the course of disease. These findings have crucial implications for counseling patients and caregivers and for the design of disease-modifying treatment trials in genetic FTD., This work is supported by the Joint Programme–Neurodegenerative Disease Research grant no. JPND2019-466-090 “GENFI-prox” (Drs Synofzik, van Swieten, Otto, Graff, Rohrer, and Borroni), the Centre d’Investigation Clinique grant no. ANR/DGOS PRTS 2015-2019 PREV-DEMALS (Dr Le Ber), the Centre pour l’Acquisition et le Traitement des Images platform grant no. ANR-10-IAIHU-06 (Dr Le Ber), the UK Medical Research Council grant no. MR/M023664/1 (Dr Rohrer), the Italian Ministry of Health grant no. 733051042 (Dr Galimberti), and the Canadian Institutes of Health Research as part of a Centres of Excellence in Neurodegeneration grant no. MOP 327387 (Dr Masellis), a Canadian Institutes of Health Research operating grant.

Published
2021
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