[en] Minimally invasive biomarkers are urgently needed to detect molecular pathology in frontotemporal dementia (FTD) and amyotrophic lateral sclerosis (ALS). Here, we show that plasma extracellular vesicles (EVs) contain quantifiable amounts of TDP-43 and full-length tau, which allow the quantification of 3-repeat (3R) and 4-repeat (4R) tau isoforms. Plasma EV TDP-43 levels and EV 3R/4R tau ratios were determined in a cohort of 704 patients, including 37 genetically and 31 neuropathologically proven cases. Diagnostic groups comprised patients with TDP-43 proteinopathy ALS, 4R tauopathy progressive supranuclear palsy, behavior variant FTD (bvFTD) as a group with either tau or TDP-43 pathology, and healthy controls. EV tau ratios were low in progressive supranuclear palsy and high in bvFTD with tau pathology. EV TDP-43 levels were high in ALS and in bvFTD with TDP-43 pathology. Both markers discriminated between the diagnostic groups with area under the curve values >0.9, and between TDP-43 and tau pathology in bvFTD. Both markers strongly correlated with neurodegeneration, and clinical and neuropsychological markers of disease severity. Findings were replicated in an independent validation cohort of 292 patients including 34 genetically confirmed cases. Taken together, the combination of EV TDP-43 levels and EV 3R/4R tau ratios may aid the molecular diagnosis of FTD, FTD spectrum disorders and ALS, providing a potential biomarker to monitor disease progression and target engagement in clinical trials.
Disciplines :
Neurology
Author, co-author :
Chatterjee, Madhurima; German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany
Özdemir, Selcuk; German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany ; Department of Genetics, Atatürk University, Erzurum, Turkey
Fritz, Christian; German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany
Möbius, Wiebke ; Department of Neurogenetics, Max Planck Institute for Multidisciplinary Sciences, Göttingen, Germany ; Cluster of Excellence 'Multiscale Bioimaging: from Molecular Machines to Networks of Excitable Cells' (MBExC), University of Göttingen, Göttingen, Germany
Kleineidam, Luca; German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany ; Department of Old Age Psychiatry and Cognitive Disorders, University Hospital Bonn, University of Bonn, Bonn, Germany
Mandelkow, Eckhard ; Department of Old Age Psychiatry and Cognitive Disorders, University Hospital Bonn, University of Bonn, Bonn, Germany
Biernat, Jacek; Department of Old Age Psychiatry and Cognitive Disorders, University Hospital Bonn, University of Bonn, Bonn, Germany
Doğdu, Cem; German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany
Peters, Oliver; German Center for Neurodegenerative Diseases (DZNE), Berlin, Germany ; Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Psychiatry and Psychotherapy, Berlin, Germany
Cosma, Nicoleta Carmen ; German Center for Neurodegenerative Diseases (DZNE), Berlin, Germany
Wang, Xiao; German Center for Neurodegenerative Diseases (DZNE), Berlin, Germany
Schneider, Luisa-Sophia; German Center for Neurodegenerative Diseases (DZNE), Berlin, Germany
Priller, Josef ; German Center for Neurodegenerative Diseases (DZNE), Berlin, Germany ; Department of Psychiatry and Psychotherapy, Charité - Universitätsmedizin Berlin, Berlin, Germany ; Department of Psychiatry and Psychotherapy, Technical University of Munich School of Medicine, Munich, Germany ; University of Edinburgh and UK DRI, Edinburgh, UK
Spruth, Eike; Department of Psychiatry and Psychotherapy, Charité - Universitätsmedizin Berlin, Berlin, Germany
Kühn, Andrea A ; German Center for Neurodegenerative Diseases (DZNE), Berlin, Germany ; Movement Disorder and Neuromodulation Unit, Department of Neurology, Charité - Universitätsmedizin Berlin, Berlin, Germany
Krause, Patricia; Movement Disorder and Neuromodulation Unit, Department of Neurology, Charité - Universitätsmedizin Berlin, Berlin, Germany
Klockgether, Thomas; German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany ; Department of Neurology, University of Bonn, Bonn, Germany
Vogt, Ina R; German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany
Kimmich, Okka; German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany
Spottke, Annika; German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany ; Department of Neurology, University of Bonn, Bonn, Germany
Hoffmann, Daniel C; German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany
Fliessbach, Klaus; German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany ; Department of Old Age Psychiatry and Cognitive Disorders, University Hospital Bonn, University of Bonn, Bonn, Germany
Miklitz, Carolin; German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany ; Department of Old Age Psychiatry and Cognitive Disorders, University Hospital Bonn, University of Bonn, Bonn, Germany
McCormick, Cornelia; German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany ; Department of Old Age Psychiatry and Cognitive Disorders, University Hospital Bonn, University of Bonn, Bonn, Germany
Weydt, Patrick; German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany
Falkenburger, Björn; German Center for Neurodegenerative Diseases (DZNE), Dresden, Germany ; Department of Neurology, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany
Brandt, Moritz; German Center for Neurodegenerative Diseases (DZNE), Dresden, Germany ; Department of Neurology, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany
Guenther, René; German Center for Neurodegenerative Diseases (DZNE), Dresden, Germany ; Department of Neurology, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany
Dinter, Elisabeth; German Center for Neurodegenerative Diseases (DZNE), Dresden, Germany ; Department of Neurology, University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany
Wiltfang, Jens; German Center for Neurodegenerative Diseases (DZNE), Göttingen, Germany ; Department of Psychiatry and Psychotherapy, University Medical Center Göttingen, University of Göttingen, Göttingen, Germany ; Neurosciences and Signaling Group, Institute of Biomedicine (iBiMED), Department of Medical Sciences, University of Aveiro, Aveiro, Portugal
Hansen, Niels; German Center for Neurodegenerative Diseases (DZNE), Göttingen, Germany ; Department of Psychiatry and Psychotherapy, University Medical Center Göttingen, University of Göttingen, Göttingen, Germany
Bähr, Mathias; German Center for Neurodegenerative Diseases (DZNE), Göttingen, Germany ; Department of Neurology, University Medical Center, Georg August University, Göttingen, Germany ; Cluster of Excellence Nanoscale Microscopy and Molecular Physiology of the Brain (CNMPB), University Medical Center Göttingen, Göttingen, Germany
Zerr, Inga; German Center for Neurodegenerative Diseases (DZNE), Göttingen, Germany ; Department of Neurology, University Medical Center, Georg August University, Göttingen, Germany
Flöel, Agnes; Department of Neurology, University Medicine Greifswald, Greifswald, Germany ; German Centre for Neurodegenerative Diseases (DZNE), Rostock/Greifswald, Germany
Nestor, Peter J; German Center for Neurodegenerative Diseases (DZNE), Magdeburg, Germany ; Queensland Brain Institute, University of Queensland and Mater Public Hospital, Brisbane, Queensland, Australia
Düzel, Emrah; German Center for Neurodegenerative Diseases (DZNE), Magdeburg, Germany ; Institute of Cognitive Neurology and Dementia Research, Otto-von-Guericke University, Magdeburg, Germany ; Institute of Cognitive Neuroscience, University College London, London, UK
Glanz, Wenzel; German Center for Neurodegenerative Diseases (DZNE), Magdeburg, Germany ; Institute of Cognitive Neurology and Dementia Research, Otto-von-Guericke University, Magdeburg, Germany ; Clinic for Neurology, University Hospital Magdeburg, Magdeburg, Germany
Incesoy, Enise; German Center for Neurodegenerative Diseases (DZNE), Magdeburg, Germany ; Institute of Cognitive Neurology and Dementia Research, Otto-von-Guericke University, Magdeburg, Germany ; Department of Psychiatry and Psychotherapy, University Hospital Magdeburg, Magdeburg, Germany
Bürger, Katharina; German Center for Neurodegenerative Diseases (DZNE), Munich, Germany ; Institute for Stroke and Dementia Research, University Hospital, LMU Munich, Munich, Germany
Janowitz, Daniel; Institute for Stroke and Dementia Research, University Hospital, LMU Munich, Munich, Germany
Perneczky, Robert; German Center for Neurodegenerative Diseases (DZNE), Munich, Germany ; Department of Psychiatry and Psychotherapy, University Hospital, LMU Munich, Munich, Germany ; Munich Cluster for Systems Neurology (SyNergy) Munich, Munich, Germany ; Ageing Epidemiology Research Unit, School of Public Health, Imperial College London, London, UK
Rauchmann, Boris S; Department of Psychiatry and Psychotherapy, University Hospital, LMU Munich, Munich, Germany ; Department of Neuroradiology, University Hospital LMU, Munich, Germany ; Sheffield Institute for Translational Neuroscience (SITraN), University of Sheffield, Sheffield, UK
Hopfner, Franziska; Department of Neurology, University Hospital of Munich, Ludwig-Maximilians-Universität (LMU) Munich, Munich, Germany
Wagemann, Olivia; German Center for Neurodegenerative Diseases (DZNE), Munich, Germany ; Department of Neurology, University Hospital of Munich, Ludwig-Maximilians-Universität (LMU) Munich, Munich, Germany
Levin, Johannes; German Center for Neurodegenerative Diseases (DZNE), Munich, Germany ; Munich Cluster for Systems Neurology (SyNergy) Munich, Munich, Germany ; Department of Neurology, University Hospital of Munich, Ludwig-Maximilians-Universität (LMU) Munich, Munich, Germany
Teipel, Stefan; German Centre for Neurodegenerative Diseases (DZNE), Rostock/Greifswald, Germany ; Department of Psychosomatic Medicine, Rostock University Medical Center, Rostock, Germany
Kilimann, Ingo; German Centre for Neurodegenerative Diseases (DZNE), Rostock/Greifswald, Germany ; Department of Psychosomatic Medicine, Rostock University Medical Center, Rostock, Germany
Goerss, Doreen; German Centre for Neurodegenerative Diseases (DZNE), Rostock/Greifswald, Germany
Prudlo, Johannes; German Centre for Neurodegenerative Diseases (DZNE), Rostock/Greifswald, Germany ; Department of Neurology, Rostock University Medical Centre, Rostock, Germany
Gasser, Thomas; German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany ; Hertie Institute for Clinical Brain Research, Department of Neurodegenerative Diseases, University of Tübingen, Tübingen, Germany
Brockmann, Kathrin ; German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany ; Hertie Institute for Clinical Brain Research, Department of Neurodegenerative Diseases, University of Tübingen, Tübingen, Germany
Mengel, David; German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany ; Hertie Institute for Clinical Brain Research, Department of Neurodegenerative Diseases, University of Tübingen, Tübingen, Germany
Zimmermann, Milan; German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany ; Hertie Institute for Clinical Brain Research, Department of Neurodegenerative Diseases, University of Tübingen, Tübingen, Germany
Synofzik, Matthis; German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany ; Hertie Institute for Clinical Brain Research, Department of Neurodegenerative Diseases, University of Tübingen, Tübingen, Germany
Wilke, Carlo; German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany ; Hertie Institute for Clinical Brain Research, Department of Neurodegenerative Diseases, University of Tübingen, Tübingen, Germany
Selma-González, Judit; Sant Pau Memory Unit, Department of Neurology, Institut de Recerca Sant Pau, Hospital de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona, Barcelona, Spain ; Motor Neuron Disease Clinic, Neuromuscular Diseases Unit, Institut de Recerca Sant Pau, Hospital de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona, Barcelona, Spain
Turon-Sans, Janina; Motor Neuron Disease Clinic, Neuromuscular Diseases Unit, Institut de Recerca Sant Pau, Hospital de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona, Barcelona, Spain ; Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER), Madrid, Spain
Santos-Santos, Miguel Angel; Sant Pau Memory Unit, Department of Neurology, Institut de Recerca Sant Pau, Hospital de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona, Barcelona, Spain ; Centro de Investigación Biomédica en Red de Enfermedades Neurodegenerativas (CIBERNED), Madrid, Spain
Alcolea, Daniel ; Sant Pau Memory Unit, Department of Neurology, Institut de Recerca Sant Pau, Hospital de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona, Barcelona, Spain ; Centro de Investigación Biomédica en Red de Enfermedades Neurodegenerativas (CIBERNED), Madrid, Spain
Rubio-Guerra, Sara ; Sant Pau Memory Unit, Department of Neurology, Institut de Recerca Sant Pau, Hospital de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona, Barcelona, Spain ; Centro de Investigación Biomédica en Red de Enfermedades Neurodegenerativas (CIBERNED), Madrid, Spain
Fortea, Juan ; Sant Pau Memory Unit, Department of Neurology, Institut de Recerca Sant Pau, Hospital de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona, Barcelona, Spain ; Centro de Investigación Biomédica en Red de Enfermedades Neurodegenerativas (CIBERNED), Madrid, Spain
Carbayo, Álvaro ; Motor Neuron Disease Clinic, Neuromuscular Diseases Unit, Institut de Recerca Sant Pau, Hospital de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona, Barcelona, Spain ; Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER), Madrid, Spain
Lleó, Alberto ; Sant Pau Memory Unit, Department of Neurology, Institut de Recerca Sant Pau, Hospital de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona, Barcelona, Spain ; Centro de Investigación Biomédica en Red de Enfermedades Neurodegenerativas (CIBERNED), Madrid, Spain
Rojas-García, Ricardo; Motor Neuron Disease Clinic, Neuromuscular Diseases Unit, Institut de Recerca Sant Pau, Hospital de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona, Barcelona, Spain ; Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER), Madrid, Spain
Illán-Gala, Ignacio; Sant Pau Memory Unit, Department of Neurology, Institut de Recerca Sant Pau, Hospital de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona, Barcelona, Spain ; Centro de Investigación Biomédica en Red de Enfermedades Neurodegenerativas (CIBERNED), Madrid, Spain
Wagner, Michael; German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany ; Department of Old Age Psychiatry and Cognitive Disorders, University Hospital Bonn, University of Bonn, Bonn, Germany
Frommann, Ingo ; German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany ; Department of Old Age Psychiatry and Cognitive Disorders, University Hospital Bonn, University of Bonn, Bonn, Germany
Roeske, Sandra ; German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany
Bertram, Lucas ; German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany
HENEKA, Michael ; University of Luxembourg ; Department of Infectious Diseases and Immunology, University of Massachussetss Medical School, North Worcester, MA, USA
Brosseron, Frederic; German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany
Ramirez, Alfredo ; German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany ; Department of Old Age Psychiatry and Cognitive Disorders, University Hospital Bonn, University of Bonn, Bonn, Germany ; Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), University of Cologne, Cologne, Germany ; Division of Neurogenetics and Molecular Psychiatry, Department of Psychiatry, University of Cologne, Cologne, Germany ; Department of Psychiatry, Glenn Biggs Institute for Alzheimer's & Neurodegenerative Diseases, UT Health San Antonio, San Antonio, TX, USA
Schmid, Matthias; German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany ; Institute for Medical Biometry, Informatics and Epidemiology, University Hospital Bonn, Bonn, Germany
Beschorner, Rudi ; German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany ; Department of Neuropathology, University of Tübingen, Tübingen, Germany
Halle, Annett; German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany ; Department of Neuropathology, University Hospital Bonn, Bonn, Germany
Herms, Jochen; German Center for Neurodegenerative Diseases (DZNE), Munich, Germany ; Munich Cluster for Systems Neurology (SyNergy) Munich, Munich, Germany ; Center for Neuropathology and Prion Research, LMU Munich, Munich, Germany
Neumann, Manuela; German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany ; Department of Neuropathology, University of Tübingen, Tübingen, Germany
Barthélemy, Nicolas R; Department of Neurology, Washington University School of Medicine, St. Louis, MO, USA ; Tracy Family SILQ Center for Neurodegenerative Biology, St. Louis, MO, USA
Bateman, Randall J ; Department of Neurology, Washington University School of Medicine, St. Louis, MO, USA ; Tracy Family SILQ Center for Neurodegenerative Biology, St. Louis, MO, USA
Rizzu, Patrizia; German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany
Heutink, Peter; German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany
Dols-Icardo, Oriol ; Sant Pau Memory Unit, Department of Neurology, Institut de Recerca Sant Pau, Hospital de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona, Barcelona, Spain ; Centro de Investigación Biomédica en Red de Enfermedades Neurodegenerativas (CIBERNED), Madrid, Spain
Höglinger, Günter ; German Center for Neurodegenerative Diseases (DZNE), Munich, Germany ; Munich Cluster for Systems Neurology (SyNergy) Munich, Munich, Germany ; Department of Neurology, University Hospital of Munich, Ludwig-Maximilians-Universität (LMU) Munich, Munich, Germany
Hermann, Andreas ; German Centre for Neurodegenerative Diseases (DZNE), Rostock/Greifswald, Germany ; Translational Neurodegeneration Section 'Albrecht Kossel' and Center for Transdisciplinary Neurosciences, University Medical Center Rostock, Rostock, Germany
Schneider, Anja ; German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany. anja.schneider@dzne.de ; Department of Old Age Psychiatry and Cognitive Disorders, University Hospital Bonn, University of Bonn, Bonn, Germany. anja.schneider@dzne.de
We thank the patients and their caregivers who participated in the study. This study was funded by a grant from the German Federal Ministry of Education and Research (BMBF), grant identifier 01KX2230, to A. Schneider. A. Schneider received funding from BMBF (DESCARTES consortium, grant identifier 01EK2102A, and PREPARE, grant identifier 01GP2213A), Verum Foundation and BMBF/NUM (UTN consortium). E.M. and A. Schneider received funding from Cure Alzheimer\u2019s Fund. C.D. and A. Schneider. received funding from Netzwerke NRW iBehave consortium. E.M. received funding from the Katharina Hardt Foundation. A. Schneider is member of the Deutsche Forschungsgemeinschaft (DFG)-funded Cluster of Excellence ImmunoSensation2\u2014EXC2151\u2014390873048. A. Schneider and A.R. were supported by La Fundaci\u00F3n Reina Sof\u00EDa, proyecto \u2018MANOLO BARR\u00D3S\u2019. A. Schneider and A.H. received funding from the Target ALS Foundation. M.C. received funding from Deutsche Demenzhilfe German Center for Neurodegenerative Diseases (DZNE) Innovative Minds Program and the Manfred-Strohscheer Foundation. L.K. received funding from the Hertie Foundation, Hertie Network of Excellence in Clinical Neurosciences and from the EU Joint Programme\u2014Neurodegenerative Disease Research (JPND), grant no. 01ED2007B (PreAdapt). M.W. and M. Schmid received funding from BMBF (DESCARTES consortium, grant identifier 01EK2102A). C. Miklitz received funding from the Neuro-aCSis clinician scientist program (DFG, project no. 493623632). N.H. has received funding support from the DFG (project no. 5302297989). F.H. was funded by the Else Kr\u00F6ner-Fresenius Foundation and the CurePSP Foundation. M. Synofzik was supported by the JPND GENFI-PROX grant (DLR/DFG 01ED2008B). D.M. and M. Synofzik were supported by the Clinician Scientist program \u2018PRECISE.net\u2019 funded by the Else Kr\u00F6ner-Fresenius-Stiftung. D.M. and M.Z. were supported by the Clinician Scientist Program of the Medical Faculty T\u00FCbingen (D.M., 459-0-0; M.Z., 481-0-0). D.M. was also supported by the Elite Program for Postdoctoral Researchers of the Baden W\u00FCrttemberg Foundation (1.16101.21). K. Brockmann has received research funding from the Michael J. Fox Foundation for Parkinson\u2019s Research (MJFF-022343, MJFF-023275, MJFF-023365), the German Society for Parkinson (DPG), the Health Forum Baden Wuerttemberg, the Else Kr\u00F6ner-Fresenius Stiftung (ClinbrAIn), the University of Tuebingen, and from the DFG (BR-655671-1). J.W. received funding from the BMBF (grant identifier 13GW0479B). R.P. is supported by the DFG (1007) under Germany\u2019s Excellence Strategy within the framework of 1008 the Munich Cluster for Systems Neurology (EXC 2145 SyNergy\u2014ID 390857198), the Davos Alzheimer\u2019s Collaborative, the VERUM Foundation, the Robert Vogel Memorial Foundation, the National Institutes for Health and Care Research (NIHR) Sheffield Biomedical Research Centre (NIHR203321), the University of Cambridge\u2013Ludwig-Maximilians-University Munich Strategic Partnership within the framework of the German Excellence Initiative and Excellence Strategy and the European Commission under the Innovative Health Initiative program (project no. 101132356) R.R.-G. has been funded by Instituto de Salud Carlos III (ISCIII) through project no. PI23/00845, co-funded by European Regional Development Fund/European Social Fund (ERDF/ESF), \u2018A way to make Europe\u2019/\u2018Investing in your future\u2019. M.A.S.-S. is supported by funding from the ISCIII (Juan Rod\u00E9s research grant no. JR18-00018; Fondo de investigaci\u00F3n sanitaria grant no. PI19/00882), the Alzheimer\u2019s Association clinician scientist fellowship (AACSF-22-972945), and the National Institutes of Health (R01AG080470). D.A. received research grants from ISCIII, Spain PI18/00435, PI22/00611, INT19/00016, INT23/00048, and from the Department of Health Generalitat de Catalunya PERIS program SLT006/17/12. I.I.-G. is a senior Atlantic Fellow for Equity in Brain Health at the Global Brain Health Institute (GBHI), and receives funding from the GBHI, the Alzheimer\u2019s Association and the Alzheimer\u2019s Society (GBHI ALZ UK-21-720973 and AACSF-21-850193). I.I.-G. was also supported by the Juan Rod\u00E9s Contract (JR20/0018) and PI21/00791 from ISCIII. O.D.-I. is funded by The Association for Frontotemporal Degeneration (Clinical Research Postdoctoral Fellowship, AFTD 2019\u20132021). This work was supported by research grants from FUNDELA (\u2018Por un mundo sin ELA\u2019) and ISCIII, Spain PI18/00326 and PI21/01395 to O.D.-I. S.R.-G. received funding from Alzheimer\u2019s Association (grant no. AACSF-21-850193). G.H. was funded by the DFG under Germany\u2019s Excellence Strategy within the framework of the Munich Cluster for Systems Neurology (EXC 2145 SyNergy\u2014ID 390857198), DFG (HO2402/18-1 MSAomics). A. Hermann is supported by the Hermann und Lilly Schilling Stiftung f\u00FCr medizinische Forschung im Stifterverband.We thank the patients and their caregivers who participated in the study. This study was funded by a grant from the German Federal Ministry of Education and Research (BMBF), grant identifier 01KX2230, to A. Schneider. A. Schneider received funding from BMBF (DESCARTES consortium, grant identifier 01EK2102A, and PREPARE, grant identifier 01GP2213A), Verum Foundation and BMBF/NUM (UTN consortium). E.M. and A. Schneider received funding from Cure Alzheimer\u2019s Fund. C.D. and A. Schneider. received funding from Netzwerke NRW iBehave consortium. E.M. received funding from the Katharina Hardt Foundation. A. Schneider is member of the Deutsche Forschungsgemeinschaft (DFG)-funded Cluster of Excellence ImmunoSensation\u2014EXC2151\u2014390873048. A. Schneider and A.R. were supported by La Fundaci\u00F3n Reina Sof\u00EDa, proyecto \u2018MANOLO BARR\u00D3S\u2019. A. Schneider and A.H. received funding from the Target ALS Foundation. M.C. received funding from Deutsche Demenzhilfe German Center for Neurodegenerative Diseases (DZNE) Innovative Minds Program and the Manfred-Strohscheer Foundation. L.K. received funding from the Hertie Foundation, Hertie Network of Excellence in Clinical Neurosciences and from the EU Joint Programme\u2014Neurodegenerative Disease Research (JPND), grant no. 01ED2007B (PreAdapt). M.W. and M. Schmid received funding from BMBF (DESCARTES consortium, grant identifier 01EK2102A). C. Miklitz received funding from the Neuro-aCSis clinician scientist program (DFG, project no. 493623632). N.H. has received funding support from the DFG (project no. 5302297989). F.H. was funded by the Else Kr\u00F6ner-Fresenius Foundation and the CurePSP Foundation. M. Synofzik was supported by the JPND GENFI-PROX grant (DLR/DFG 01ED2008B). D.M. and M. Synofzik were supported by the Clinician Scientist program \u2018PRECISE.net\u2019 funded by the Else Kr\u00F6ner-Fresenius-Stiftung. D.M. and M.Z. were supported by the Clinician Scientist Program of the Medical Faculty T\u00FCbingen (D.M., 459-0-0; M.Z., 481-0-0). D.M. was also supported by the Elite Program for Postdoctoral Researchers of the Baden W\u00FCrttemberg Foundation (1.16101.21). K. Brockmann has received research funding from the Michael J. Fox Foundation for Parkinson\u2019s Research (MJFF-022343, MJFF-023275, MJFF-023365), the German Society for Parkinson (DPG), the Health Forum Baden Wuerttemberg, the Else Kr\u00F6ner-Fresenius Stiftung (ClinbrAIn), the University of Tuebingen, and from the DFG (BR-655671-1). J.W. received funding from the BMBF (grant identifier 13GW0479B). R.P. is supported by the DFG (1007) under Germany\u2019s Excellence Strategy within the framework of 1008 the Munich Cluster for Systems Neurology (EXC 2145 SyNergy\u2014ID 390857198), the Davos Alzheimer\u2019s Collaborative, the VERUM Foundation, the Robert Vogel Memorial Foundation, the National Institutes for Health and Care Research (NIHR) Sheffield Biomedical Research Centre (NIHR203321), the University of Cambridge\u2013Ludwig-Maximilians-University Munich Strategic Partnership within the framework of the German Excellence Initiative and Excellence Strategy and the European Commission under the Innovative Health Initiative program (project no. 101132356) R.R.-G. has been funded by Instituto de Salud Carlos III (ISCIII) through project no. PI23/00845, co-funded by European Regional Development Fund/European Social Fund (ERDF/ESF), \u2018A way to make Europe\u2019/\u2018Investing in your future\u2019. M.A.S.-S. is supported by funding from the ISCIII (Juan Rod\u00E9s research grant no. JR18-00018; Fondo de investigaci\u00F3n sanitaria grant no. PI19/00882), the Alzheimer\u2019s Association clinician scientist fellowship (AACSF-22-972945), and the National Institutes of Health (R01AG080470). D.A. received research grants from ISCIII, Spain PI18/00435, PI22/00611, INT19/00016, INT23/00048, and from the Department of Health Generalitat de Catalunya PERIS program SLT006/17/12. I.I.-G. is a senior Atlantic Fellow for Equity in Brain Health at the Global Brain Health Institute (GBHI), and receives funding from the GBHI, the Alzheimer\u2019s Association and the Alzheimer\u2019s Society (GBHI ALZ UK-21-720973 and AACSF-21-850193). I.I.-G. was also supported by the Juan Rod\u00E9s Contract (JR20/0018) and PI21/00791 from ISCIII. O.D.-I. is funded by The Association for Frontotemporal Degeneration (Clinical Research Postdoctoral Fellowship, AFTD 2019\u20132021). This work was supported by research grants from FUNDELA (\u2018Por un mundo sin ELA\u2019) and ISCIII, Spain PI18/00326 and PI21/01395 to O.D.-I. S.R.-G. received funding from Alzheimer\u2019s Association (grant no. AACSF-21-850193). G.H. was funded by the DFG under Germany\u2019s Excellence Strategy within the framework of the Munich Cluster for Systems Neurology (EXC 2145 SyNergy\u2014ID 390857198), DFG (HO2402/18-1 MSAomics). A. Hermann is supported by the Hermann und Lilly Schilling Stiftung f\u00FCr medizinische Forschung im Stifterverband.All authors had access to the data in the study and accepted responsibility for submitting the paper for publication. A. Schneider serves in a scientific advisory board for and receives honoraria from Biogen. She additionally received funding for a scientific collaboration from Eisai and honoraria for presentations from Eisai. M.C. is currently an employee of uniQure Biopharma B.V. and recipient of employee stock options. F.H. receives author fees from Thieme medical publishers and W. Kohlhammer GmbH medical publishers. P.H. is an employee and owns stock in Alector LLC. K. Brockmann is a consultant for F. Hoffmann-La Roche Ltd, Vanqua Bio and the Michael J. Fox Foundation for Parkinson\u2019s Research and has received speaker honoraria from AbbVie, Lundbeck, UCB (Union Chimique Belge) and Zambon. N.H. has received travel support from Eli Lilly. A. Hermann has received honoraria for presentations and participation in advisory boards from Amylyx and IFT Pharma. He has received royalities from Elsevier Press and Kohlhammer. Washington University and R.J.B. have equity ownership interest in C2N Diagnostics and R.J.B. receives income from C2N Diagnostics for serving on the scientific advisory board. R.J.B. and N.R.B. may receive income based on technology (methods to detect microtubule binding region (MTBR) tau isoforms and use thereof) licensed by Washington University to C2N Diagnostics. R.J.B. has received research funding from Avid Radiopharmaceuticals, Janssen, Roche/Genentech, Eli Lilly, Eisai, Biogen, AbbVie, Bristol Myers Squibb and Novartis. R.J.B. serves on the Roche Gantenerumab Steering Committee as an unpaid member. R.G. received speaker fees and nonfinancial support from Biogen, Roche, Zambon and research support from Biogen, ITF Pharma and Zambon outside this work. D.A. participated in advisory boards from Fujirebio-Europe, Roche Diagnostics, Grifols S.A. and Lilly, and received speaker honoraria from Fujirebio-Europe, Roche Diagnostics, Nutricia, Krka Farmac\u00E9utica S.L., Zambon S.A.U. and Esteve Pharmaceuticals S.A. D.A. declares a filed patent application (WO2019175379 A1 Markers of synaptopathy in neurodegenerative disease). J.W. received lecture honoraria from Beeijing Yibai Science and Technology Ltd, Gloryren, Janssen Cilag, Pfizer, Med Update GmbH, Roche Pharma, Lilly and serves on advisory boards for Biogen, Abbott, Boehringer Ingelheim, Lilly, MSD Sharp & Dohme and Roche. M. Brandt received speaker honoraria from Idorsia, Eisai and Bristol Myers Squibb. All other authors state no competing interests.
Y.A. Abramzon P. Fratta B.J. Traynor R. Chia The overlapping genetics of amyotrophic lateral sclerosis and frontotemporal dementia. Front. Neurosci. 2020 14 42 32116499 7012787
L. Chare et al. New criteria for frontotemporal dementia syndromes: clinical and pathological diagnostic implications J. Neurol. Neurosurg. Psychiatry 2014 85 865 870 24421286
D.M.A. Mann J.S. Snowden Frontotemporal lobar degeneration: pathogenesis, pathology and pathways to phenotype Brain Pathol. 2017 27 723 736 1:CAS:528:DC%2BC2sXhslCnurbF 28100023 8029341
E. Mandelkow E.M. Mandelkow Microtubules and microtubule-associated proteins Curr. Opin. Cell Biol. 1995 7 72 81 1:CAS:528:DyaK2MXjsVyktrk%3D 7755992
I.R. Mackenzie M. Neumann Molecular neuropathology of frontotemporal dementia: insights into disease mechanisms from postmortem studies J. Neurochem. 2016 138 54 70 1:CAS:528:DC%2BC28XpvFChsb8%3D 27306735
D. Richards J.A. Morren E.P. Pioro Time to diagnosis and factors affecting diagnostic delay in amyotrophic lateral sclerosis J. Neurol. Sci. 2020 417 32763509
M. Mamarabadi H. Razjouyan L.I. Golbe Is the latency from progressive supranuclear palsy onset to diagnosis improving? Mov. Disord. Clin. Pract. 2018 5 603 606 30637280 6277372
P. Tsoukra et al. The diagnostic challenge of young-onset dementia syndromes and primary psychiatric diseases: results from a retrospective 20-year cross-sectional study J. Neuropsychiatry Clin. Neurosci. 2022 34 44 52 34538074
K.A.Q. Cousins et al. Distinguishing frontotemporal lobar degeneration tau from TDP-43 using plasma biomarkers JAMA Neurol. 2022 79 1155 1164 36215050 9552044
M. Suarez-Calvet et al. Plasma phosphorylated TDP-43 levels are elevated in patients with frontotemporal dementia carrying a C9orf72 repeat expansion or a GRN mutation J. Neurol. Neurosurg. Psychiatry 2014 85 684 691 24309270
Y. Ren et al. TDP-43 and phosphorylated TDP-43 levels in paired plasma and CSF samples in amyotrophic lateral sclerosis Front. Neurol. 2021 12 34194383 8236522
K. Katisko et al. Serum total TDP-43 levels are decreased in frontotemporal dementia patients with C9orf72 repeat expansion or concomitant motoneuron disease phenotype Alzheimers Res. Ther. 2022 14 151 1:CAS:528:DC%2BB38Xis1OntL3F 36217158 9552448
C. Scialo et al. TDP-43 real-time quaking induced conversion reaction optimization and detection of seeding activity in CSF of amyotrophic lateral sclerosis and frontotemporal dementia patients Brain Commun. 2020 2 33094285 7566418
L. Beyer et al. TDP-43 as structure-based biomarker in amyotrophic lateral sclerosis Ann. Clin. Transl. Neurol. 2021 8 271 277 1:CAS:528:DC%2BB3MXit12lu7g%3D 33263951
W.T. Hu et al. Reduced CSF p-Tau181 to Tau ratio is a biomarker for FTLD-TDP Neurology 2013 81 1945 1952 1:CAS:528:DC%2BC3sXhvVGmsLfP 24174584 3843382
K.E. Irwin et al. A fluid biomarker reveals loss of TDP-43 splicing repression in presymptomatic ALS-FTD Nat. Med. 2024 30 382 393 1:CAS:528:DC%2BB2cXit1Slt7o%3D 38278991 10878965
C. Luk et al. Development and assessment of sensitive immuno-PCR assays for the quantification of cerebrospinal fluid three- and four-repeat tau isoforms in tauopathies J. Neurochem. 2012 123 396 405 1:CAS:528:DC%2BC38XhsVKhurfF 22862741
J.E. Meredith Jr et al. Characterization of novel CSF Tau and ptau biomarkers for Alzheimer’s disease PLoS ONE 2013 8 e76523 1:CAS:528:DC%2BC3sXhs1WktrnN 24116116
K. Horie et al. CSF tau microtubule-binding region identifies pathological changes in primary tauopathies Nat. Med. 2022 28 2547 2554 1:CAS:528:DC%2BB38XivFClt73K 36424467 9800273
G. van Niel G. D’Angelo G. Raposo Shedding light on the cell biology of extracellular vesicles Nat. Rev. Mol. Cell Biol. 2018 19 213 228 29339798
M. Perez J. Avila F. Hernandez Propagation of tau via extracellular vesicles Front. Neurosci. 2019 13 698 31312118 6614378
E. Leroux et al. Extracellular vesicles: major actors of heterogeneity in tau spreading among human tauopathies Mol. Ther. 2022 30 782 797 1:CAS:528:DC%2BB3MXitlyktLnK 34563677
Y. Wang et al. The release and trans-synaptic transmission of Tau via exosomes Mol. Neurodegener. 2017 12 5 28086931 5237256
H. Asai et al. Depletion of microglia and inhibition of exosome synthesis halt tau propagation Nat. Neurosci. 2015 18 1584 1593 1:CAS:528:DC%2BC2MXhs1Wls7bJ 26436904 4694577
Y. Iguchi et al. Exosome secretion is a key pathway for clearance of pathological TDP-43 Brain 2016 139 3187 3201 27679482 5840881
A. Stuendl et al. Alpha-synuclein in plasma-derived extracellular vesicles is a potential biomarker of Parkinson’s disease Mov. Disord. 2021 36 2508 2518 1:CAS:528:DC%2BB3MXhs1Cmsb3F 34002893
A. Lionnet et al. Characterisation of tau in the human and rodent enteric nervous system under physiological conditions and in tauopathy Acta Neuropathol. Commun. 2018 6 65 30037345 6055332
E.B. Mukaetova-Ladinska et al. Platelet Tau protein as a potential peripheral biomarker in Alzheimer’s disease: an explorative study Curr. Alzheimer Res. 2018 15 800 808 1:CAS:528:DC%2BC1cXhtlKhsLzK 29623842
I.M. Kvetnoy et al. Tau-protein expression in human blood lymphocytes: a promising marker and suitable sample for life-time diagnosis of Alzheimer’s disease Neuro. Endocrinol. Lett. 2000 21 313 318 1:CAS:528:DC%2BD3cXmsVWgsLw%3D 11455366
M. Norman et al. L1CAM is not associated with extracellular vesicles in human cerebrospinal fluid or plasma Nat. Methods 2021 18 631 634 1:CAS:528:DC%2BB3MXht1Ghu7rF 34092791 9075416
B. Boyarko V. Hook Human tau isoforms and proteolysis for production of toxic tau fragments in neurodegeneration Front. Neurosci. 2021 15 34744602 8566764
M. Neumann et al. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis Science 2006 314 130 133 1:CAS:528:DC%2BD28XhtVCiurrL 17023659
M.F. Folstein S.E. Folstein P.R. McHugh ‘Mini-Mental State’. A practical method for grading the cognitive state of patients for the clinician J. Psychiatr. Res. 1975 12 189 198 1:STN:280:DyaE28%2FntFKjtw%3D%3D 1202204
Z.S. Nasreddine et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment J. Am. Geriatr. Soc. 2005 53 695 699 15817019
L.I. Golbe P.A. Ohman-Strickland A clinical rating scale for progressive supranuclear palsy Brain 2007 130 1552 1565 17405767
I. Piot et al. The Progressive Supranuclear Palsy Clinical Deficits Scale Mov. Disord. 2020 35 650 661 31951049
Schwab R. S England, A. Projection technique for evaluating surgery in Parkinson’s disease. in Third Symposium on Parkinson’s Disease (eds Billingham, F. H. & Donaldson, M. C.) 152–157 (Churchill, 1969).
Guy, W. in ECDEU Assessment Manual for Psychopharmacology—Revised. DHEW Publ No ADM 76-338. (U.S. Dept. of Health, Education, and Welfare, Public Health Service, Alcohol, Drug Abuse, and Mental Health Administration, National Institute of Mental Health, Psychopharmacology Research Branch, Division of Extramural Research Programs, 1976).
C.G. Goetz et al. Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): process, format, and clinimetric testing plan Mov. Disord. 2007 22 41 47 17115387
S.E. Starkstein et al. Reliability, validity, and clinical correlates of apathy in Parkinson’s disease J. Neuropsychiatry Clin. Neurosci. 1992 4 134 139 1:STN:280:DyaK38zjtVCqsQ%3D%3D 1627973
A. Schrag et al. Measuring quality of life in PSP: the PSP-QoL Neurology 2006 67 39 44 1:STN:280:DC%2BD28vhtFektw%3D%3D 16832075
R.I. Pfeffer T.T. Kurosaki C.H. Harrah Jr. J.M. Chance S. Filos Measurement of functional activities in older adults in the community J. Gerontol. 1982 37 323 329 1:STN:280:DyaL387mvVKktg%3D%3D 7069156
C.P. Hughes L. Berg W.L. Danziger L.A. Coben R.L. Martin A new clinical scale for the staging of dementia Br. J. Psychiatry 1982 140 566 572 1:STN:280:DyaL383lsl2mtA%3D%3D 7104545
D.S. Knopman S. Weintraub V.S. Pankratz Language and behavior domains enhance the value of the Clinical Dementia Rating Scale Alzheimers Dement. 2011 7 293 299 21575870
J.L. Cummings et al. The Neuropsychiatric Inventory: comprehensive assessment of psychopathology in dementia Neurology 1994 44 2308 2314 1:STN:280:DyaK2M%2FotlWisw%3D%3D 7991117
H.J. Wear et al. The Cambridge Behavioural Inventory revised Dement. Neuropsychol. 2008 2 102 107 29213551 5619578
M. Neumann et al. TDP-43 in the ubiquitin pathology of frontotemporal dementia with VCP gene mutations J. Neuropathol. Exp. Neurol. 2007 66 152 157 17279000
I. Gijselinck et al. Loss of TBK1 is a frequent cause of frontotemporal dementia in a Belgian cohort Neurology 2015 85 2116 2125 1:CAS:528:DC%2BC2MXitVCrtr3J 26581300 4691687
D. Alcolea et al. The Sant Pau Initiative on Neurodegeneration (SPIN) cohort: a data set for biomarker discovery and validation in neurodegenerative disorders Alzheimers Dement. (N Y) 2019 5 597 609 31650016
J. Vaquer-Alicea M.I. Diamond L.A. Joachimiak Tau strains shape disease Acta Neuropathol. 2021 142 57 71 1:CAS:528:DC%2BB3MXhtFWgtrzN 33830330 8217038
D. Ritz et al. Endolysosomal sorting of ubiquitylated caveolin-1 is regulated by VCP and UBXD1 and impaired by VCP disease mutations Nat. Cell Biol. 2011 13 1116 1123 1:CAS:528:DC%2BC3MXhtFWls7%2FF 21822278 3246400
Y. Zhang et al. Cerebellar Kv3.3 potassium channels activate TANK-binding kinase 1 to regulate trafficking of the cell survival protein Hax-1 Nat. Commun. 2021 12 1:CAS:528:DC%2BB3MXntl2qsrk%3D 33741962 7979925
M. Schwickart I. Vainshtein R. Lee A. Schneider M. Liang Interference in immunoassays to support therapeutic antibody development in preclinical and clinical studies Bioanalysis 2014 6 1939 1951 1:CAS:528:DC%2BC2cXhsVeqsbfI 24806787
K. O’Brien S. Ughetto S. Mahjoum A.V. Nair X.O. Breakefield Uptake, functionality, and re-release of extracellular vesicle-encapsulated cargo Cell Rep. 2022 39 35417683 9074118
H.M. Ramos-Zaldivar et al. Extracellular vesicles through the blood–brain barrier: a review Fluids Barriers CNS 2022 19 60 35879759 9310691
N. Riva et al. Phosphorylated TDP-43 aggregates in peripheral motor nerves of patients with amyotrophic lateral sclerosis Brain 2022 145 276 284 35076694 8967102
B.D. James et al. TDP-43 stage, mixed pathologies, and clinical Alzheimer’s-type dementia Brain 2016 139 2983 2993 27694152 5091047
P.T. Nelson et al. Frequency of LATE neuropathologic change across the spectrum of Alzheimer’s disease neuropathology: combined data from 13 community-based or population-based autopsy cohorts Acta Neuropathol. 2022 144 27 44 1:CAS:528:DC%2BB38XhvVars7rE 35697880 9552938
P.T. Nelson et al. Limbic-predominant age-related TDP-43 encephalopathy (LATE): consensus working group report Brain 2019 142 1503 1527 31039256 6536849
J.D. Rohrer et al. Serum neurofilament light chain protein is a measure of disease intensity in frontotemporal dementia Neurology 2016 87 1329 1336 1:CAS:528:DC%2BC28XhsF2ru7bE 27581216 5047041
T.F. Gendron et al. Comprehensive cross-sectional and longitudinal analyses of plasma neurofilament light across FTD spectrum disorders Cell Rep. Med. 2022 3 1:CAS:528:DC%2BB38XhsFCls77F 35492244 9044101
K. Katisko et al. GFAP as a biomarker in frontotemporal dementia and primary psychiatric disorders: diagnostic and prognostic performance J. Neurol. Neurosurg. Psychiatry 2021 92 1305 1312 34187866
N. Zhu et al. Plasma glial fibrillary acidic protein and neurofilament light chain for the diagnostic and prognostic evaluation of frontotemporal dementia Transl. Neurodegener. 2021 10 50 1:CAS:528:DC%2BB38XpsVOgtrk%3D 34893073 8662866
C.R. Jack Jr et al. NIA-AA research framework: toward a biological definition of Alzheimer’s disease Alzheimers Dement. 2018 14 535 562 29653606
A. Ludolph et al. A revision of the El Escorial criteria - 2015 Amyotroph. Lateral Scler. Frontotemporal Degener. 2015 16 291 292 26121170
J.M. Cedarbaum et al. The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS Study Group (Phase III) J. Neurol. Sci. 1999 169 13 21 1:STN:280:DC%2BD3c%2FgvFKqtg%3D%3D 10540002
S. Abrahams J. Newton E. Niven J. Foley T.H. Bak Screening for cognition and behaviour changes in ALS Amyotroph. Lateral Scler. Frontotemporal Degener. 2014 15 9 14 23781974
K. Rascovsky et al. Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia Brain 2011 134 2456 2477 21810890 3170532
R. Lemos D. Duro M.R. Simoes I. Santana The free and cued selective reminding test distinguishes frontotemporal dementia from Alzheimer’s disease Arch. Clin. Neuropsychol. 2014 29 670 679 25062746 4263917
K.A. Welsh et al. The Consortium to Establish a Registry for Alzheimer’s Disease (CERAD). Part V. A normative study of the neuropsychological battery Neurology 1994 44 609 614 1:STN:280:DyaK2c3hslyrsQ%3D%3D 8164812
M. Bertoux et al. Social cognition and emotional assessment differentiates frontotemporal dementia from depression J. Neurol. Neurosurg. Psychiatry 2012 83 411 416 22291219
Scogin, F., Rohen, N. & Bailey, E. in Handbook of Psychological Assessment in Primary Care Settings (ed. Maruish M. E.) 491–508 (Erlbaum, 2000).
M.L. Gorno-Tempini et al. Classification of primary progressive aphasia and its variants Neurology 2011 76 1006 1014 21325651 3059138
S. Bozeat M.A. Lambon Ralph K. Patterson P. Garrard J.R. Hodges Non-verbal semantic impairment in semantic dementia Neuropsychologia 2000 38 1207 1215 1:STN:280:DC%2BD3cvjvFCrsA%3D%3D 10865096
O.V. Billette S.A. Sajjadi K. Patterson P.J. Nestor SECT and MAST: new tests to assess grammatical abilities in primary progressive aphasia Aphasiology 2015 29 1135 1151
Huber, W., Poeck, K., Weniger, D. &; Willmes, K. Der Aachener Aphasie Test (AAT) (Hogrefe, 1983).
Ziegler, W., Aichert, I., Staiger, A. & Schimeczek, M. HWL-kompakt. https://neurophonetik.de/sprechapraxie-wortlisten (2019).
J.R. Hodges M. Martinos A.M. Woollams K. Patterson A.L. Adlam Repeat and point: differentiating semantic dementia from progressive non-fluent aphasia Cortex 2008 44 1265 1270 18761140
G. Respondek G.U. Hoglinger DescribePSP and ProPSP: German multicenter networks for standardized prospective collection of clinical data, imaging data, and biomaterials of patients with progressive supranuclear palsy Front. Neurol. 2021 12 644064 34113306 8186498
I. Litvan et al. Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele–Richardson–Olszewski syndrome): report of the NINDS-SPSP international workshop Neurology 1996 47 1 9 1:STN:280:DyaK283ptFSjtA%3D%3D 8710059
G.U. Hoglinger et al. Clinical diagnosis of progressive supranuclear palsy: The movement disorder society criteria Mov. Disord. 2017 32 853 864 28467028 5516529
M. Neumann et al. Phosphorylation of S409/410 of TDP-43 is a consistent feature in all sporadic and familial forms of TDP-43 proteinopathies Acta Neuropathol. 2009 117 137 149 1:CAS:528:DC%2BD1MXhtVCltLw%3D 19125255 2693625
T.J. Montine et al. National Institute on Aging–Alzheimer’s Association guidelines for the neuropathologic assessment of Alzheimer’s disease: a practical approach Acta Neuropathol. 2012 123 1 11 1:CAS:528:DC%2BC38Xkt1eqtQ%3D%3D 22101365
J. Attems et al. Neuropathological consensus criteria for the evaluation of Lewy pathology in post-mortem brains: a multi-centre study Acta Neuropathol. 2021 141 159 172 1:CAS:528:DC%2BB3MXjvVKqu7k%3D 33399945 7847437
I.R. Mackenzie et al. A harmonized classification system for FTLD-TDP pathology Acta Neuropathol. 2011 122 111 113 21644037 3285143
B.R. Brooks R.G. Miller M. Swash T.L. Munsat World Federation of Neurology Research Group on Motor Neuron Diseases El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis Amyotroph. Lateral Scler. Other Motor Neuron Disord. 2000 1 293 299 1:STN:280:DC%2BD3Mvhs1Ghsg%3D%3D 11464847
T.S. Campos et al. Spanish adaptation of the revised Amyotrophic Lateral Sclerosis Functional Rating Scale (ALSFRS-R) Amyotroph. Lateral Scler. 2010 11 475 477 20509746
E. Eren et al. Neuronal-derived EV biomarkers track cognitive decline in Alzheimer’s disease cells Cells 2022 11 436 1:CAS:528:DC%2BB38XnsVKmt7w%3D 35159246 8834433
D. Oender et al. Evolution of clinical outcome measures and biomarkers in sporadic adult-onset degenerative ataxia Mov. Disord. 2023 38 654 664 1:CAS:528:DC%2BB3sXhvVyisbo%3D 36695111
J.A. Hanley B.J. McNeil A method of comparing the areas under receiver operating characteristic curves derived from the same cases Radiology 1983 148 839 843 1:STN:280:DyaL3s3nsVKgtg%3D%3D 6878708
Boyd, K. et al. (eds) in ECML PKDD 2013, Part III, LNAI 8190, 451–466 (Springer, 2013).
Y. Barer et al. Epidemiology of progressive supranuclear Palsy: Real world data from the second largest health plan in Israel. Brain. Sci. 2022 12 1126 36138862 9496895
C.A. Brown C. Lally V. Kupelian W.D. Flanders Estimated Prevalence and Incidence of Amyotrophic Lateral Sclerosis and SOD1 and C9orf72 genetic variants Neuroepidemiology 2021 55 342 353 34247168
C.U. Onyike J. Diehl-Schmid The epidemiology of frontotemporal dementia Int Rev. Psychiatry 2013 25 130 137 23611343 3932112