Presymptomatic cognitive and neuroanatomical changes in genetic frontotemporal dementia in the Genetic Frontotemporal dementia Initiative (GENFI) study: a cross-sectional analysis

doi:10.1016/S1474-4422(14)70324-2

Multicenter Study

. 2015 Mar;14(3):253-62.

doi: 10.1016/S1474-4422(14)70324-2. Epub 2015 Feb 4.

Presymptomatic cognitive and neuroanatomical changes in genetic frontotemporal dementia in the Genetic Frontotemporal dementia Initiative (GENFI) study: a cross-sectional analysis

Jonathan D Rohrer¹, Jennifer M Nicholas², David M Cash³, John van Swieten⁴, Elise Dopper⁴, Lize Jiskoot⁴, Rick van Minkelen⁵, Serge A Rombouts⁶, M Jorge Cardoso³, Shona Clegg¹, Miklos Espak³, Simon Mead⁷, David L Thomas⁸, Enrico De Vita⁹, Mario Masellis¹⁰, Sandra E Black¹⁰, Morris Freedman¹¹, Ron Keren¹², Bradley J MacIntosh¹⁰, Ekaterina Rogaeva¹³, David Tang-Wai¹², Maria Carmela Tartaglia¹³, Robert Laforce Jr¹⁴, Fabrizio Tagliavini¹⁵, Pietro Tiraboschi¹⁵, Veronica Redaelli¹⁵, Sara Prioni¹⁵, Marina Grisoli¹⁵, Barbara Borroni¹⁶, Alessandro Padovani¹⁶, Daniela Galimberti¹⁷, Elio Scarpini¹⁷, Andrea Arighi¹⁷, Giorgio Fumagalli¹⁷, James B Rowe¹⁸, Ian Coyle-Gilchrist¹⁸, Caroline Graff¹⁹, Marie Fallström²⁰, Vesna Jelic²¹, Anne Kinhult Ståhlbom¹⁹, Christin Andersson²², Håkan Thonberg¹⁹, Lena Lilius²³, Giovanni B Frisoni²⁴, Michela Pievani²⁵, Martina Bocchetta²⁶, Luisa Benussi²⁵, Roberta Ghidoni²⁵, Elizabeth Finger²⁷, Sandro Sorbi²⁸, Benedetta Nacmias²⁸, Gemma Lombardi²⁸, Cristina Polito²⁹, Jason D Warren¹, Sebastien Ourselin³, Nick C Fox¹, Martin N Rossor³⁰, Giuliano Binetti

Affiliations

¹ Dementia Research Centre, University College London, London, UK.
² Dementia Research Centre, University College London, London, UK; Department of Medical Statistics, London School of Hygiene & Tropical Medicine, London, UK.
³ Dementia Research Centre, University College London, London, UK; Department of Neurodegenerative Disease, University College London Institute of Neurology, and Centre for Medical Image Computing, University College London, London, UK.
⁴ Department of Neurology, Erasmus Medical Center, Rotterdam, Netherlands.
⁵ Department of Clinical Genetics, Erasmus Medical Center, Rotterdam, Netherlands.
⁶ Institute of Psychology, Leiden University, and Department of Radiology, Leiden University Medical Center, Leiden, Netherlands.
⁷ Medical Research Council Prion Unit, University College London, London, UK.
⁸ Dementia Research Centre, University College London, London, UK; Neuroradiological Academic Unit, Department of Brain Repair and Rehabilitation, University College London, London, UK.
⁹ Neuroradiological Academic Unit, Department of Brain Repair and Rehabilitation, University College London, London, UK; Lysholm Department of Neuroradiology, National Hospital for Neurology and Neurosurgery, London, UK.
¹⁰ LC Campbell Cognitive Neurology Research Unit, Department of Medicine, Division of Neurology, Sunnybrook Health Sciences Centre, Sunnybrook Research Institute, University of Toronto, Toronto, ON, Canada.
¹¹ Department of Medicine, Division of Neurology, Baycrest, Mount Sinai Hospital, University of Toronto, Toronto, ON, Canada; Rotman Research Institute, Baycrest, Toronto, ON, Canada.
¹² University Health Network Memory Clinic, Toronto Western Hospital, Toronto, ON, Canada.
¹³ Tanz Centre for Research in Neurodegenerative Diseases, University of Toronto, Toronto, ON, Canada.
¹⁴ Clinique Interdisciplinaire de Mémoire, Département des Sciences Neurologiques, Hôpital de l'Enfant-Jésus, and Faculté de Médecine, Université Laval, QC, Canada.
¹⁵ Fondazione Istituto di Ricovero e Cura a Carattere Scientifico Istituto Neurologico Carlo Besta, Milano, Italy.
¹⁶ Neurology Unit, Department of Medical and Experimental Sciences, University of Brescia, Brescia, Italy.
¹⁷ Neurology Unit, Department of Physiopathology and Transplantation, University of Milan, Fondazione Cà Granda, Istituto di Ricovero e Cura a Carattere Scientifico Ospedale Policlinico, Milan, Italy.
¹⁸ Department of Clinical Neurosciences, University of Cambridge, Cambridge, UK.
¹⁹ Department of Neurobiology, Care Sciences and Society, Center for Alzheimer Research, Division of Neurogeriatrics, Karolinska Institutet, Huddinge, Sweden; Department of Geriatric Medicine, Karolinska University Hospital-Huddinge, Stockholm, Sweden.
²⁰ Department of Geriatric Medicine, Karolinska University Hospital-Huddinge, Stockholm, Sweden.
²¹ Division of Clinical Geriatrics, Karolinska Institutet, Huddinge, Sweden; Department of Geriatric Medicine, Karolinska University Hospital-Huddinge, Stockholm, Sweden.
²² Department of Clinical Neuroscience, Karolinska Institutet, Huddinge, Sweden; Department of Psychology, Karolinska University Hospital-Huddinge, Stockholm, Sweden.
²³ Department of Neurobiology, Care Sciences and Society, Center for Alzheimer Research, Division of Neurogeriatrics, Karolinska Institutet, Huddinge, Sweden.
²⁴ Istituto di Ricovero e Cura a Carattere Scientifico Istituto Centro San Giovanni di Dio Fatebenefratelli, Brescia, Italy; Memory Clinic and LANVIE-Laboratory of Neuroimaging of Aging, University Hospitals and University of Geneva, Geneva, Switzerland.
²⁵ Istituto di Ricovero e Cura a Carattere Scientifico Istituto Centro San Giovanni di Dio Fatebenefratelli, Brescia, Italy.
²⁶ Department of Molecular and Translational Medicine, University of Brescia, Brescia, Italy; Istituto di Ricovero e Cura a Carattere Scientifico Istituto Centro San Giovanni di Dio Fatebenefratelli, Brescia, Italy.
²⁷ Department of Clinical Neurological Sciences, University of Western Ontario, London, ON, Canada.
²⁸ Department of Neuroscience, Psychology, Drug Research and Child Health, University of Florence, Florence, Italy.
²⁹ Department of Clinical Pathophysiology, Nuclear Medicine Division, University of Florence, Florence, Italy.
³⁰ Dementia Research Centre, University College London, London, UK. Electronic address: m.rossor@ucl.ac.uk.

PMID: 25662776
PMCID: PMC6742501
DOI: 10.1016/S1474-4422(14)70324-2

Multicenter Study

Presymptomatic cognitive and neuroanatomical changes in genetic frontotemporal dementia in the Genetic Frontotemporal dementia Initiative (GENFI) study: a cross-sectional analysis

Jonathan D Rohrer et al. Lancet Neurol. 2015 Mar.

. 2015 Mar;14(3):253-62.

doi: 10.1016/S1474-4422(14)70324-2. Epub 2015 Feb 4.

Authors

Affiliations

¹ Dementia Research Centre, University College London, London, UK.
² Dementia Research Centre, University College London, London, UK; Department of Medical Statistics, London School of Hygiene & Tropical Medicine, London, UK.
³ Dementia Research Centre, University College London, London, UK; Department of Neurodegenerative Disease, University College London Institute of Neurology, and Centre for Medical Image Computing, University College London, London, UK.
⁴ Department of Neurology, Erasmus Medical Center, Rotterdam, Netherlands.
⁵ Department of Clinical Genetics, Erasmus Medical Center, Rotterdam, Netherlands.
⁶ Institute of Psychology, Leiden University, and Department of Radiology, Leiden University Medical Center, Leiden, Netherlands.
⁷ Medical Research Council Prion Unit, University College London, London, UK.
⁸ Dementia Research Centre, University College London, London, UK; Neuroradiological Academic Unit, Department of Brain Repair and Rehabilitation, University College London, London, UK.
⁹ Neuroradiological Academic Unit, Department of Brain Repair and Rehabilitation, University College London, London, UK; Lysholm Department of Neuroradiology, National Hospital for Neurology and Neurosurgery, London, UK.
¹⁰ LC Campbell Cognitive Neurology Research Unit, Department of Medicine, Division of Neurology, Sunnybrook Health Sciences Centre, Sunnybrook Research Institute, University of Toronto, Toronto, ON, Canada.
¹¹ Department of Medicine, Division of Neurology, Baycrest, Mount Sinai Hospital, University of Toronto, Toronto, ON, Canada; Rotman Research Institute, Baycrest, Toronto, ON, Canada.
¹² University Health Network Memory Clinic, Toronto Western Hospital, Toronto, ON, Canada.
¹³ Tanz Centre for Research in Neurodegenerative Diseases, University of Toronto, Toronto, ON, Canada.
¹⁴ Clinique Interdisciplinaire de Mémoire, Département des Sciences Neurologiques, Hôpital de l'Enfant-Jésus, and Faculté de Médecine, Université Laval, QC, Canada.
¹⁵ Fondazione Istituto di Ricovero e Cura a Carattere Scientifico Istituto Neurologico Carlo Besta, Milano, Italy.
¹⁶ Neurology Unit, Department of Medical and Experimental Sciences, University of Brescia, Brescia, Italy.
¹⁷ Neurology Unit, Department of Physiopathology and Transplantation, University of Milan, Fondazione Cà Granda, Istituto di Ricovero e Cura a Carattere Scientifico Ospedale Policlinico, Milan, Italy.
¹⁸ Department of Clinical Neurosciences, University of Cambridge, Cambridge, UK.
¹⁹ Department of Neurobiology, Care Sciences and Society, Center for Alzheimer Research, Division of Neurogeriatrics, Karolinska Institutet, Huddinge, Sweden; Department of Geriatric Medicine, Karolinska University Hospital-Huddinge, Stockholm, Sweden.
²⁰ Department of Geriatric Medicine, Karolinska University Hospital-Huddinge, Stockholm, Sweden.
²¹ Division of Clinical Geriatrics, Karolinska Institutet, Huddinge, Sweden; Department of Geriatric Medicine, Karolinska University Hospital-Huddinge, Stockholm, Sweden.
²² Department of Clinical Neuroscience, Karolinska Institutet, Huddinge, Sweden; Department of Psychology, Karolinska University Hospital-Huddinge, Stockholm, Sweden.
²³ Department of Neurobiology, Care Sciences and Society, Center for Alzheimer Research, Division of Neurogeriatrics, Karolinska Institutet, Huddinge, Sweden.
²⁴ Istituto di Ricovero e Cura a Carattere Scientifico Istituto Centro San Giovanni di Dio Fatebenefratelli, Brescia, Italy; Memory Clinic and LANVIE-Laboratory of Neuroimaging of Aging, University Hospitals and University of Geneva, Geneva, Switzerland.
²⁵ Istituto di Ricovero e Cura a Carattere Scientifico Istituto Centro San Giovanni di Dio Fatebenefratelli, Brescia, Italy.
²⁶ Department of Molecular and Translational Medicine, University of Brescia, Brescia, Italy; Istituto di Ricovero e Cura a Carattere Scientifico Istituto Centro San Giovanni di Dio Fatebenefratelli, Brescia, Italy.
²⁷ Department of Clinical Neurological Sciences, University of Western Ontario, London, ON, Canada.
²⁸ Department of Neuroscience, Psychology, Drug Research and Child Health, University of Florence, Florence, Italy.
²⁹ Department of Clinical Pathophysiology, Nuclear Medicine Division, University of Florence, Florence, Italy.
³⁰ Dementia Research Centre, University College London, London, UK. Electronic address: m.rossor@ucl.ac.uk.

PMID: 25662776
PMCID: PMC6742501
DOI: 10.1016/S1474-4422(14)70324-2

Erratum in

Lancet Neurol. 2015 Dec;14(12):1151. Binetti, Giuliano [added]

Abstract

Background: Frontotemporal dementia is a highly heritable neurodegenerative disorder. In about a third of patients, the disease is caused by autosomal dominant genetic mutations usually in one of three genes: progranulin (GRN), microtubule-associated protein tau (MAPT), or chromosome 9 open reading frame 72 (C9orf72). Findings from studies of other genetic dementias have shown neuroimaging and cognitive changes before symptoms onset, and we aimed to identify whether such changes could be shown in frontotemporal dementia.

Methods: We recruited participants to this multicentre study who either were known carriers of a pathogenic mutation in GRN, MAPT, or C9orf72, or were at risk of carrying a mutation because a first-degree relative was a known symptomatic carrier. We calculated time to expected onset as the difference between age at assessment and mean age at onset within the family. Participants underwent a standardised clinical assessment and neuropsychological battery. We did MRI and generated cortical and subcortical volumes using a parcellation of the volumetric T1-weighted scan. We used linear mixed-effects models to examine whether the association of neuropsychology and imaging measures with time to expected onset of symptoms differed between mutation carriers and non-carriers.

Findings: Between Jan 30, 2012, and Sept 15, 2013, we recruited participants from 11 research sites in the UK, Italy, the Netherlands, Sweden, and Canada. We analysed data from 220 participants: 118 mutation carriers (40 symptomatic and 78 asymptomatic) and 102 non-carriers. For neuropsychology measures, we noted the earliest significant differences between mutation carriers and non-carriers 5 years before expected onset, when differences were significant for all measures except for tests of immediate recall and verbal fluency. We noted the largest Z score differences between carriers and non-carriers 5 years before expected onset in tests of naming (Boston Naming Test -0·7; SE 0·3) and executive function (Trail Making Test Part B, Digit Span backwards, and Digit Symbol Task, all -0·5, SE 0·2). For imaging measures, we noted differences earliest for the insula (at 10 years before expected symptom onset, mean volume as a percentage of total intracranial volume was 0·80% in mutation carriers and 0·84% in non-carriers; difference -0·04, SE 0·02) followed by the temporal lobe (at 10 years before expected symptom onset, mean volume as a percentage of total intracranial volume 8·1% in mutation carriers and 8·3% in non-carriers; difference -0·2, SE 0·1).

Interpretation: Structural imaging and cognitive changes can be identified 5-10 years before expected onset of symptoms in asymptomatic adults at risk of genetic frontotemporal dementia. These findings could help to define biomarkers that can stage presymptomatic disease and track disease progression, which will be important for future therapeutic trials.

Funding: Centres of Excellence in Neurodegeneration.

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Conflict of interest statement

Declaration of interests

JDR is funded by a National Institute for Health Research Rare Disease Translational Research Collaboration Fellowship. SAR is supported by a Vici grant from the Netherlands Organization for Scientific Research. MM is supported by the Department of Medicine, Sunnybrook Health Sciences Centre, and the Sunnybrook Foundation. He is funded by the Canadian Institutes of Health Research and the Ontario Research Fund. He reports consultancy fees from Novartis, Teva, Union Chimique Belge Canada, General Electric Healthcare, and Bioscape Medical Imaging CRO all outside the submitted work. He also holds a US patent of a pharmacogenetic test for Parkinson’s disease. MF receives support from the Saul A Silverman Family Foundation as a Canada International Scientific Exchange Program and Morris Kerzner Memorial Fund, and is listed on a provisional patent related to methods and kits for differential diagnosis of Alzheimer’s disease versus frontotemporal dementia with blood biomarkers. ER is funded by the Weston Brain Institute and Ontario Research Fund. RL Jr is funded by Réseau de médecine génétique appliquée, Fonds de recherche du Québec—Santé (FRQS). FT, RG, and LB are funded by the Italian Ministry of Health. DG, ES, AA, and GF are supported by the Fondazione Monzino and Italian Ministry of Health, Ricerca Corrente. JBR is supported by a Wellcome Trust Senior Research Fellowship (088324). JBR and IC-G are supported by the National Institute for Health Cambridge Biomedical Research Centre and Biomedical Research Unit in Dementia. BN is funded by Cassa di Risparmio di Pistoia e Pescia (CRPT 2013/0347). SS is funded by Cassa di Risparmio di Firenze (CRF 2013/0199) and the Ministry of Health RF-2010-2319722. JDW is funded by a Wellcome Trust Senior Clinical Fellowship (091673/Z/10/Z). NCF and MNR are National Institute for Health Research Senior Investigators. NCF also reports consultancy fees (all paid to University College London) from Janssen/Pfizer, General Electric Healthcare, IXICO, Johnson & Johnson, Genzyme (Sonofi company), Eisai, Janssen Alzheimer’s Immunotherapy Research and Development, Lilly Research Laboratories (AVID), Eli Lilly, and Novartis Pharma AG all outside the submitted work. He also has a patent QA Box issued. The Dementia Research Centre at University College London is an Alzheimer’s Research UK coordinating centre and has received equipment funded by Alzheimer’s Research UK and Brain Research Trust. MNR also reports fees (paid to University College London) for serving on a Data Monitoring Committee for Servier outside the submitted work. SEB reports personal fees from Pfizer, GlaxoSmithKline, Novartis, Roche, Eli Lilly, Pfizer, Eisai, Boehringer Ingelheim, General Electric Healthcare, and Novartis, and grants from Pfizer, Elan/Transition Therapeutics Ireland Ltd, Roche, Eli Lilly, General Electric Healthcare, and Lundbeck all outside the submitted work. SO is funded by the Engineering and Physical Sciences Research Council (EP/H046410/1, EP/J020990/1, EP/K005278), the Medical Research Council (MR/J01107X/1), the EU-FP7 project VPH-DARE@IT (FP7-ICT-2011-9-601055), and the National Institute for Health Research University College London Hospitals Biomedical Research Centre (NIHR BRC UCLH/UCL High Impact Initiative BW.mn.BRC10269). All other authors declare no competing interests.

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Comment in

Frontotemporal dementia: a peek under its invisibility cloak.
Josephs KA. Josephs KA. Lancet Neurol. 2015 Mar;14(3):236-7. doi: 10.1016/S1474-4422(15)70019-0. Epub 2015 Feb 4. Lancet Neurol. 2015. PMID: 25662775 No abstract available.

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References

1. Seelaar H, Rohrer JD, Pijnenburg YA, Fox NC, van Swieten JC. Clinical, genetic and pathological heterogeneity of frontotemporal dementia: a review. J Neurol Neurosurg Psychiatry. 2011;82:476–86. - PubMed
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[1] Seelaar H, Rohrer JD, Pijnenburg YA, Fox NC, van Swieten JC. Clinical, genetic and pathological heterogeneity of frontotemporal dementia: a review. J Neurol Neurosurg Psychiatry. 2011;82:476–86. - PubMed

[2] Seelaar H, Rohrer JD, Pijnenburg YA, Fox NC, van Swieten JC. Clinical, genetic and pathological heterogeneity of frontotemporal dementia: a review. J Neurol Neurosurg Psychiatry. 2011;82:476–86. - PubMed

[3] Onyike CU, Diehl-Schmid J. The epidemiology of frontotemporal dementia. Int Rev Psychiatry. 2013;25:130–37. - PMC - PubMed

[4] Onyike CU, Diehl-Schmid J. The epidemiology of frontotemporal dementia. Int Rev Psychiatry. 2013;25:130–37. - PMC - PubMed

[5] Rohrer JD, Guerreiro R, Vandrovcova J, et al. The heritability and genetics of frontotemporal lobar degeneration. Neurology. 2009;73:1451–56. - PMC - PubMed

[6] Rohrer JD, Guerreiro R, Vandrovcova J, et al. The heritability and genetics of frontotemporal lobar degeneration. Neurology. 2009;73:1451–56. - PMC - PubMed

[7] Warren JD, Rohrer JD, Rossor MN. Clinical review. Frontotemporal dementia. BMJ. 2013;347:f4827. - PMC - PubMed

[8] Warren JD, Rohrer JD, Rossor MN. Clinical review. Frontotemporal dementia. BMJ. 2013;347:f4827. - PMC - PubMed

[9] Rohrer JD, Warren JD, Fox NC, Rossor MN. Presymptomatic studies in genetic frontotemporal dementia. Rev Neurol (Paris) 2013;169:820–24. - PMC - PubMed

[10] Rohrer JD, Warren JD, Fox NC, Rossor MN. Presymptomatic studies in genetic frontotemporal dementia. Rev Neurol (Paris) 2013;169:820–24. - PMC - PubMed

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Presymptomatic cognitive and neuroanatomical changes in genetic frontotemporal dementia in the Genetic Frontotemporal dementia Initiative (GENFI) study: a cross-sectional analysis

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Presymptomatic cognitive and neuroanatomical changes in genetic frontotemporal dementia in the Genetic Frontotemporal dementia Initiative (GENFI) study: a cross-sectional analysis

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