Clinical recognition of frontotemporal dementia with right anterior temporal predominance: A multicenter retrospective cohort study.

emotion recognition frontotemporal dementia frontotemporal lobar degeneration right anterior temporal lobe semantic dementia social cognition

Journal

Alzheimer's & dementia : the journal of the Alzheimer's Association
ISSN: 1552-5279
Titre abrégé: Alzheimers Dement
Pays: United States
ID NLM: 101231978

Informations de publication

Date de publication:
10 Jul 2024
Historique:
revised: 15 04 2024
received: 31 10 2023
accepted: 26 05 2024
medline: 10 7 2024
pubmed: 10 7 2024
entrez: 10 7 2024
Statut: aheadofprint

Résumé

Although frontotemporal dementia (FTD) with right anterior temporal lobe (RATL) predominance has been recognized, a uniform description of the syndrome is still missing. This multicenter study aims to establish a cohesive clinical phenotype. Retrospective clinical data from 18 centers across 12 countries yielded 360 FTD patients with predominant RATL atrophy through initial neuroimaging assessments. Common symptoms included mental rigidity/preoccupations (78%), disinhibition/socially inappropriate behavior (74%), naming/word-finding difficulties (70%), memory deficits (67%), apathy (65%), loss of empathy (65%), and face-recognition deficits (60%). Real-life examples unveiled impairments regarding landmarks, smells, sounds, tastes, and bodily sensations (74%). Cognitive test scores indicated deficits in emotion, people, social interactions, and visual semantics however, lacked objective assessments for mental rigidity and preoccupations. This study cumulates the largest RATL cohort unveiling unique RATL symptoms subdued in prior diagnostic guidelines. Our novel approach, combining real-life examples with cognitive tests, offers clinicians a comprehensive toolkit for managing these patients. This project is the first international collaboration and largest reported cohort. Further efforts are warranted for precise nomenclature reflecting neural mechanisms. Our results will serve as a clinical guideline for early and accurate diagnoses.

Identifiants

DOI: 10.1002/alz.14076 PMID: 38982845
pubmed: 38982845
doi: 10.1002/alz.14076
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Alzheimer's Association
ID : AACSF-22-849085
Pays : United States
Organisme : Josephs and Whitwell
ID : R01-AG37491
Organisme : Josephs and Whitwell
ID : R01-DC010367
Organisme : Josephs and Whitwell
ID : R21-NS94684
Organisme : KU Leuven
ID : IDN/21/010
Organisme : KU Leuven
ID : C24/18/095
Organisme : Sequoia Fund
Organisme : Swedish Federal Government
ID : 2022-Projekt0080
Organisme : Fondation Planiol
Organisme : Fondation France Alzheimer
Organisme : CNPq
Organisme : Pressman
ID : K23 AG063900-01A1
Organisme : Swedish Research Council
ID : 2022-00775
Organisme : Knut and Alice Wallenberg Foundation
ID : 2017-0383
Organisme : Lund University
Organisme : Swedish Alzheimer Foundation
ID : AF-980907
Organisme : Alzheimer's Society
Pays : United Kingdom
Organisme : Alzheimer's Research UK
Organisme : Royal National Institute for Deaf People
Organisme : NIHR UCLH Biomedical Research Centre
Organisme : Rankin
ID : RF1-AG029577
Organisme : The National Brain Appeal
ID : RF1-AG029577

Informations de copyright

© 2024 The Author(s). Alzheimer's & Dementia published by Wiley Periodicals LLC on behalf of Alzheimer's Association.

Références

Neary D, Snowden JS, Gustafson L, et al. Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. Neurology. 1998;51:1546‐1554.
Rascovsky K, Hodges JR, Knopman D, et al. Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. Brain. 2011;134:2456‐2477.
Gorno‐Tempini ML, Hillis AE, Weintraub S, et al. Classification of primary progressive aphasia and its variants. Neurology. 2011;76:1006‐1014.
Josephs KA, Whitwell JL, Knopman DS, et al. Two distinct subtypes of right temporal variant frontotemporal dementia. Neurology. 2009;73:1443‐1450.
Kumfor F, Landin‐Romero R, Devenney E, et al. On the right side? A longitudinal study of left‐ versus right‐lateralized semantic dementia. Brain J Neurol. 2016;139:986‐998.
Snowden JS, Harris JM, Thompson JC, et al. Semantic dementia and the left and right temporal lobes. Cortex J Devoted Study Nerv Syst Behav. 2018;107:188‐203.
Ulugut Erkoyun H, Groot C, Heilbron R, et al. A clinical‐radiological framework of the right temporal variant of frontotemporal dementia. Brain J Neurol. 2020;143:2831‐2843.
Chan D, Anderson V, Pijnenburg Y, et al. The clinical profile of right temporal lobe atrophy. Brain. 2009;132:1287‐1298.
Younes K, Borghesani V, Montembeault M, et al. Right temporal degeneration and socioemotional semantics: semantic behavioural variant frontotemporal dementia. Brain. 2022;145:4080‐4096.
Boeve BF, Boxer AL, Kumfor F, Pijnenburg Y, Rohrer JD. Advances and controversies in frontotemporal dementia: diagnosis, biomarkers, and therapeutic considerations. Lancet Neurol. 2022;21:258‐272.
Clinical and neuropathological criteria for frontotemporal dementia. The Lund and Manchester Groups. J Neurol Neurosurg Psychiatry. 1994; 57: 416‐418.
Ralph MAL, Jefferies E, Patterson K, Rogers TT. The neural and computational bases of semantic cognition. Nat Rev Neurosci. 2017;18:42‐55.
Binney RJ, Ramsey R. Social semantics: the role of conceptual knowledge and cognitive control in a neurobiological model of the social brain. Neurosci Biobehav Rev. 2020;112:28‐38.
Belder CRS, Chokesuwattanaskul A, Marshall CR, Hardy CJD, Rohrer JD, Warren JD. The problematic syndrome of right temporal lobe atrophy: unweaving the phenotypic rainbow. Front Neurol. 2023;13:1082828.
Mendez MF. Frontotemporal dementia: a window to alexithymia. J Neuropsychiatry Clin Neurosci. 2021;33:157‐160.
Kipps CM, Davies RR, Mitchell J, Kril JJ, Halliday GM, Hodges JR. Clinical significance of lobar atrophy in frontotemporal dementia: application of an MRI visual rating scale. Dement Geriatr Cogn Disord. 2007;23:334‐342.
Bozeat S, Lambon Ralph MA, Patterson K, Garrard P, Hodges JR. Non‐verbal semantic impairment in semantic dementia. Neuropsychologia. 2000;38:1207‐1215.
Fletcher PD, Downey LE, Golden HL, et al. Auditory hedonic phenotypes in dementia: a behavioural and neuroanatomical analysis. Cortex J Devoted Study Nerv Syst Behav. 2015;67:95‐105.
Silva MME, Viveiros CP, Kotsifas NJE, et al. Olfactory impairment in frontotemporal dementia: a systematic review and meta‐analysis. Dement Neuropsychol. 2019;13:154‐161.
Omar R, Mahoney CJ, Buckley AH, Warren JD. Flavour identification in frontotemporal lobar degeneration. J Neurol Neurosurg Psychiatry. 2013;84:88‐93.
Marshall CR, Hardy CJD, Russell LL, et al. Impaired interoceptive accuracy in semantic variant primary progressive aphasia. Front Neurol. 2017;8:610. Accessed December 6, 2022. 10.3389/fneur.2017.00610
Ahmed RM, Iodice V, Daveson N, Kiernan MC, Piguet O, Hodges JR. Autonomic dysregulation in frontotemporal dementia. J Neurol Neurosurg Psychiatry. 2015;86:1048‐1049.
Fletcher PD, Downey LE, Golden HL, et al. Pain and temperature processing in dementia: a clinical and neuroanatomical analysis. Brain J Neurol. 2015;138:3360‐3372.
Ikeda M, Brown J, Holland A, Fukuhara R, Hodges J. Changes in appetite, food preference, and eating habits in frontotemporal dementia and Alzheimer's disease. J Neurol Neurosurg Psychiatry. 2002;73:371‐376.
Restrepo‐Martínez M, Ramirez‐Bermudez J, Chacon‐Gonzalez J, Ruiz‐Garcia R, Malik R, Finger E. Defining repetitive behaviours in frontotemporal dementia. Brain. 2023;147:1149‐1165. doi:https://doi.org/10.1093/brain/awad431
Magrath Guimet N, Miller BL, Allegri RF, Rankin KP. What do we mean by behavioral disinhibition in frontotemporal dementia? Front Neurol. 2021;12:707799.
Bertoux M, Duclos H, Caillaud M, et al. When affect overlaps with concept: emotion recognition in semantic variant of primary progressive aphasia. Brain. 2020;143:3850‐3864.
Rankin KP. Brain networks supporting social cognition in dementia. Curr Behav Neurosci Rep. 2020;7:203‐211.
Hornberger M, Piguet O. Episodic memory in frontotemporal dementia: a critical review. Brain. 2012;135:678‐692.
Irish M, Piguet O. The pivotal role of semantic memory in remembering the past and imagining the future. Front Behav Neurosci. 2013;7(27). doi:10.3389/fnbeh.2013.00027
Sieben A, Van Langenhove T, Vermeiren Y, et al. Hippocampal sclerosis in frontotemporal dementia: when vascular pathology meets neurodegeneration. J Neuropathol Exp Neurol. 2021;80:313‐324.

Auteurs

Hulya Ulugut (H)

Alzheimer Center Amsterdam, Department of Neurology, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, De Boelelaan, Amsterdam, The Netherlands.
Memory and Aging Center, Department of Neurology, UCSF Weill Institute for Neurosciences, University of California, San Francisco, California, USA.
ORCID: 0000-0002-5016-2505

Maxime Bertoux (M)

Lille Neuroscience & Cognition U1172, Univ. Lille, Inserm, CHU Lille, LiCEND & Labex DistALZ, Lille, France.

Kyan Younes (K)

Memory and Aging Center, Department of Neurology, UCSF Weill Institute for Neurosciences, University of California, San Francisco, California, USA.
Stanford Neuroscience Health Center, Department of Neurology, Stanford University, Palo Alto, California, USA.

Maxime Montembeault (M)

Memory and Aging Center, Department of Neurology, UCSF Weill Institute for Neurosciences, University of California, San Francisco, California, USA.
Department of Psychiatry, Douglas Mental Health University Institute, McGill University Health Centre, McGill University, Montreal, Quebec, Canada.

Giorgio G Fumagalli (GG)

Department of Neurology, University of Milan, Milan, Italy.
Università degli Studi di Trento | UNITN·CIMEC - Center for Mind/Brain Sciences, Mattarello, Trentino, Italy.

Bedia Samanci (B)

Department of Neurology, Istanbul University, Fatih, Istanbul, Turkey.

Ignacio Illán-Gala (I)

Sant Pau Memory Unit, Department of Neurology, Hospital de la Santa Creu i Sant Pau, Biomedical Research Institute Sant Pau, Universitat Autònoma de Barcelona, Barcelona, Spain.
Centro de Investigación en Red-Enfermedades Neurodegenerativas (CIBERNED), Madrid, Spain.

Gregory Kuchcinski (G)

Lille Neuroscience & Cognition U1172, Univ. Lille, Inserm, CHU Lille, LiCEND & Labex DistALZ, Lille, France.

Melanie Leroy (M)

Lille Neuroscience & Cognition U1172, Univ. Lille, Inserm, CHU Lille, LiCEND & Labex DistALZ, Lille, France.

Jennifer C Thompson (JC)

Cerebral Function Unit, Greater Manchester Neuroscience Centre, Salford Royal NHS Foundation Trust, Salford, UK.
Division of Neuroscience and Experimental Psychology, Faculty of Biology, Medicine and Health, University of Manchester, Salford, Manchester, UK.

Christopher Kobylecki (C)

Department of Neurology, Manchester Centre for Clinical Neurosciences NHS Foundation Trust, Salford, UK.
Division of Neuroscience, University of Manchester, Salford, Manchester, UK.

Alexander F Santillo (AF)

Clinical Memory Research Unit, Department of Clinical Sciences, Faculty of Medicine, Lund University, Lund, Sweden.

Elisabet Englund (E)

Division of Pathology, Department of Clinical Sciences, Lund University, Lund, Sweden.

Maria Landqvist Waldö (ML)

Division of Clinical Sciences Helsingborg, Department of Clinical Sciences Lund, Lund University, Lund, Sweden.

Lina Riedl (L)

School of Medicine, Department of Psychiatry and Psychotherapy, Technical University of Munich, Munich, Germany.

Jan Van den Stock (J)

Neuropsychiatry, Department of Neurosciences, Leuven Brain Institute, Leuven, Belgium.

Mathieu Vandenbulcke (M)

Neuropsychiatry, Department of Neurosciences, Leuven Brain Institute, Leuven, Belgium.

Rik Vandenberghe (R)

Department of Neurology, University Hospital Leuven, Leuven, Belgium.

Robert Laforce (R)

Clinique Interdisciplinaire de Mémoire (CIME), Département des Sciences Neurologiques, Laval University, Quebec City, Canada.

Simon Ducharme (S)

Department of Psychiatry, Douglas Mental Health University Institute, McGill University Health Centre, McGill University, Montreal, Quebec, Canada.

Peter S Pressman (PS)

Anschutz Medical Campus, Behavioral Neurology Section, Department of Neurology, University of Colorado, Aurora, Colorado, USA.

Paulo Caramelli (P)

Behavioral and Cognitive Neurology Unit, Department of Internal Medicine, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil.

Leonardo Cruz de Souza (LC)

Behavioral and Cognitive Neurology Unit, Department of Internal Medicine, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil.

Leonel T Takada (LT)

Cognitive and Behavioral Unit, Hospital das Clinicas, Department of Neurology, University of São Paulo Medical School, Pacaembu, São Paulo, Brazil.

Hakan Gurvit (H)

Department of Neurology, Istanbul University, Fatih, Istanbul, Turkey.

Oskar Hansson (O)

Clinical Memory Research Unit, Department of Clinical Sciences, Faculty of Medicine, Lund University, Lund, Sweden.

Janine Diehl-Schmid (J)

School of Medicine, Department of Psychiatry and Psychotherapy, Technical University of Munich, Munich, Germany.
Kbo-Inn-Salzach-Klinikum, Clinical Center for Psychiatry, Psychotherapy, Psychosomatic Medicine, Geriatrics and Neurology, Wasserburg/Inn, Germany.

Daniela Galimberti (D)

Department of Biomedical, Surgical and Dental Sciences, University of Milan, Milan, Italy.
Fondazione IRCCS Ca' Granda, Ospedale Maggiore Policlinico, Milan, Italy.

Florence Pasquier (F)

Lille Neuroscience & Cognition U1172, Univ. Lille, Inserm, CHU Lille, LiCEND & Labex DistALZ, Lille, France.

Bruce L Miller (BL)

Memory and Aging Center, Department of Neurology, UCSF Weill Institute for Neurosciences, University of California, San Francisco, California, USA.

Philip Scheltens (P)

Alzheimer Center Amsterdam, Department of Neurology, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, De Boelelaan, Amsterdam, The Netherlands.

Rik Ossenkoppele (R)

Alzheimer Center Amsterdam, Department of Neurology, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, De Boelelaan, Amsterdam, The Netherlands.
Alzheimer Center Amsterdam, Department of Radiology, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, De Boelelaan, Amsterdam, The Netherlands.

Wiesje M van der Flier (WM)

Alzheimer Center Amsterdam, Department of Neurology, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, De Boelelaan, Amsterdam, The Netherlands.

Frederik Barkhof (F)

Alzheimer Center Amsterdam, Department of Radiology, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, De Boelelaan, Amsterdam, The Netherlands.
UCL Institutes of Neurology and Healthcare Engineering, University College London, London, UK.

Nick C Fox (NC)

Dementia Research Centre, UCL Queen Square Institute of Neurology, London, UK.

Virginia E Sturm (VE)

Memory and Aging Center, Department of Neurology, UCSF Weill Institute for Neurosciences, University of California, San Francisco, California, USA.

Toji Miyagawa (T)

Department of Neurology, Mayo Clinic, Rochester, Rochester, Minnesota, USA.

Jennifer L Whitwell (JL)

Department of Radiology, Mayo Clinic, Rochester, Rochester, Minnesota, USA.

Bradley Boeve (B)

Department of Neurology, Mayo Clinic, Rochester, Rochester, Minnesota, USA.

Jonathan D Rohrer (JD)

Dementia Research Centre, UCL Queen Square Institute of Neurology, London, UK.

Maria Luisa Gorno-Tempini (ML)

Memory and Aging Center, Department of Neurology, UCSF Weill Institute for Neurosciences, University of California, San Francisco, California, USA.
Dyslexia Center, University of California San Francisco, UCSF Weill Institute for Neurosciences, University of California, San Francisco, California, USA.

Keith A Josephs (KA)

Department of Neurology, Mayo Clinic, Rochester, Rochester, Minnesota, USA.

Julie Snowden (J)

Cerebral Function Unit, Greater Manchester Neuroscience Centre, Salford Royal NHS Foundation Trust, Salford, UK.
Division of Neuroscience and Experimental Psychology, Faculty of Biology, Medicine and Health, University of Manchester, Salford, Manchester, UK.

Jason D Warren (JD)

Dementia Research Centre, UCL Queen Square Institute of Neurology, London, UK.

Katherine P Rankin (KP)

Memory and Aging Center, Department of Neurology, UCSF Weill Institute for Neurosciences, University of California, San Francisco, California, USA.

Yolande A L Pijnenburg (YAL)

Alzheimer Center Amsterdam, Department of Neurology, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, De Boelelaan, Amsterdam, The Netherlands.

Classifications MeSH