European intersocietal recommendations for the biomarker-based diagnosis of neurocognitive disorders

Giovanni B Frisoni¹, Cristina Festari², Federico Massa³, Matteo Cotta Ramusino⁴, Stefania Orini⁵, Dag Aarsland⁶, Federica Agosta⁷, Claudio Babiloni⁸, Barbara Borroni⁹, Stefano F Cappa¹⁰, Kristian S Frederiksen¹¹, Lutz Froelich¹², Valentina Garibotto¹³, Alexander Haliassos¹⁴, Frank Jessen¹⁵, Anita Kamondi¹⁶, Roy Pc Kessels¹⁷, Silvia D Morbelli¹⁸, John T O'Brien¹⁹, Markus Otto²⁰, Armand Perret-Liaudet²¹, Francesca B Pizzini²², Mathieu Vandenbulcke²³, Ritva Vanninen²⁴, Frans Verhey²⁵, Meike W Vernooij²⁶, Tarek Yousry²⁷, Mercè Boada Rovira²⁸, Bruno Dubois²⁹, Jean Georges³⁰, Oskar Hansson³¹, Craig W Ritchie³², Philip Scheltens³³, Wiesje M van der Flier³⁴, Flavio Nobili³

Affiliations

¹ Laboratory of Neuroimaging of Aging (LANVIE), University of Geneva, Geneva, Switzerland; Geneva Memory Center, Department of Rehabilitation and Geriatrics, Geneva University Hospitals, Geneva, Switzerland. Electronic address: giovanni.frisoni@unige.ch.
² Laboratory of Alzheimer's Neuroimaging and Epidemiology, IRCCS Istituto Centro San Giovanni di Dio Fatebenefratelli, Brescia, Italy.
³ Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health (DINOGMI), University of Genoa, Genoa, Italy; IRCCS Ospedale Policlinico San Martino, Genoa, Italy.
⁴ Unit of Behavioral Neurology and Dementia Research Center (DRC), IRCCS Mondino Foundation, Pavia, Italy.
⁵ Alzheimer's Unit-Memory Clinic, IRCCS Istituto Centro San Giovanni di Dio Fatebenefratelli, Brescia, Italy; Department of Clinical and Experimental Sciences, University of Brescia, Brescia, Italy.
⁶ Centre for Age-Related Medicine, Stavanger University Hospital, Stavanger, Norway; UK Dementia Research Institute, Department of Psychological Medicine, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
⁷ Neuroimaging Research Unit, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy; Vita-Salute San Raffaele University, Milan, Italy.
⁸ Department of Physiology and Pharmacology "V Erspamer", Sapienza University of Rome, Rome, Italy; Hospital San Raffaele of Cassino, Cassino, Italy.
⁹ Department of Clinical and Experimental Sciences, University of Brescia, Brescia, Italy; Department of Continuity of Care and Frailty, ASST Spedali Civili, Brescia, Italy.
¹⁰ Centro Ricerca sulle Demenze, IRCCS Mondino Foundation, Pavia, Italy; University Institute for Advanced Studies (IUSS), Pavia, Italy.
¹¹ Danish Dementia Research Centre, Department of Neurology, Copenhagen University Hospital Rigshospitalet, Copenhagen, Denmark; Department of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark.
¹² Department of Geriatric Psychiatry, Central Institute of Mental Health Mannheim, Medical Faculty Mannheim, University of Heidelberg, Heidelberg, Germany.
¹³ Laboratory of Neuroimaging and Innovative Molecular Tracers (NIMTlab), Geneva University Neurocenter and Faculty of Medicine, University of Geneva, Geneva, Switzerland; Division of Nuclear Medicine and Molecular Imaging, Geneva University Hospitals, Geneva, Switzerland; CIBM Center for Biomedical Imaging, Geneva, Switzerland.
¹⁴ ESEAP-Proficiency Testing Scheme for Clinical Laboratories, Athens, Greece.
¹⁵ German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany; Department of Psychiatry, University of Cologne, Medical Faculty, Cologne, Germany; Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), University of Cologne, Cologne, Germany.
¹⁶ National Institute of Mental Health, Neurology and Neurosurgery, Budapest, Hungary; Department of Neurology, Semmelweis University, Budapest, Hungary.
¹⁷ Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, Netherlands; Radboud UMC Alzheimer Center and Department of Medical Psychology, Radboud University Medical Center, Nijmegen, Netherlands; Vincent van Gogh Institute for Psychiatry, Venray, Netherlands.
¹⁸ Department of Health Sciences (DISSAL), University of Genoa, Genoa, Italy; IRCCS Ospedale Policlinico San Martino, Genoa, Italy.
¹⁹ Department of Psychiatry, School of Clinical Medicine, University of Cambridge, Cambridge, UK.
²⁰ Department of Neurology, Martin Luther University of Halle-Wittenberg, Halle (Saale), Germany.
²¹ Neurobiology, Hospices Civils de Lyon, Lyon, France.
²² Department of Diagnostic and Public Health, Verona University Hospital, Verona University, Verona, Italy.
²³ Department of Neurosciences, KU Leuven, Leuven, Belgium; Department of Geriatric Psychiatry, University Psychiatric Centre KU Leuven, Leuven-Kortenberg, Belgium.
²⁴ University of Eastern Finland and Kuopio University Hospital, Kuopio, Finland.
²⁵ Department of Psychiatry and Neuropsychology-Alzheimer Centre Limburg, School for Mental Health and Neuroscience, Maastricht University, Maastricht, Netherlands.
²⁶ Department of Epidemiology and Department of Radiology and Nuclear Medicine Erasmus MC University Medical Center, Rotterdam, Netherlands.
²⁷ Lysholm Department of Neuroradiology and the Neuroradiological Academic Unit, Department of Brain Repair and Rehabilitation, University College London Hospitals NHS Foundation Trust National Hospital for Neurology and Neurosurgery, London, UK.
²⁸ Fundació ACE, Institut Català de Neurociències Aplicades, Barcelona, Spain.
²⁹ Institut de La Mémoire et de La Maladie d'Alzheimer, Neurology Department, Salpêtrière Hospital, Assistance Publique-Hôpital de Paris, Paris, France; Sorbonne University, Paris, France.
³⁰ Alzheimer Europe, Luxembourg.
³¹ Clinical Memory Research Unit, Department of Clinical Sciences, Lund University, Malmö, Sweden; Memory Clinic, Skåne University Hospital, Malmö, Sweden.
³² Edinburgh Dementia Prevention, Centre for Clinical Brain Sciences, Western General Hospital, University of Edinburgh, Edinburgh, UK; Brain Health Scotland, Edinburgh, UK.
³³ Alzheimer Center Amsterdam, Department of Neurology, Amsterdam Neuroscience, Amsterdam UMC, Amsterdam, Netherlands.
³⁴ Alzheimer Center Amsterdam, Department of Neurology, Amsterdam Neuroscience, Amsterdam UMC, Amsterdam, Netherlands; Amsterdam Neuroscience-Neurodegeneration, Amsterdam, Netherlands; Epidemiology and Data Science, Vrije Universiteit Amsterdam, Amsterdam UMC location VUmc, Amsterdam, Netherlands.

PMID: 38365381
DOI: 10.1016/S1474-4422(23)00447-7

Review

European intersocietal recommendations for the biomarker-based diagnosis of neurocognitive disorders

Giovanni B Frisoni et al. Lancet Neurol. 2024 Mar.

. 2024 Mar;23(3):302-312.

doi: 10.1016/S1474-4422(23)00447-7.

Authors

Affiliations

¹ Laboratory of Neuroimaging of Aging (LANVIE), University of Geneva, Geneva, Switzerland; Geneva Memory Center, Department of Rehabilitation and Geriatrics, Geneva University Hospitals, Geneva, Switzerland. Electronic address: giovanni.frisoni@unige.ch.
² Laboratory of Alzheimer's Neuroimaging and Epidemiology, IRCCS Istituto Centro San Giovanni di Dio Fatebenefratelli, Brescia, Italy.
³ Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health (DINOGMI), University of Genoa, Genoa, Italy; IRCCS Ospedale Policlinico San Martino, Genoa, Italy.
⁴ Unit of Behavioral Neurology and Dementia Research Center (DRC), IRCCS Mondino Foundation, Pavia, Italy.
⁵ Alzheimer's Unit-Memory Clinic, IRCCS Istituto Centro San Giovanni di Dio Fatebenefratelli, Brescia, Italy; Department of Clinical and Experimental Sciences, University of Brescia, Brescia, Italy.
⁶ Centre for Age-Related Medicine, Stavanger University Hospital, Stavanger, Norway; UK Dementia Research Institute, Department of Psychological Medicine, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
⁷ Neuroimaging Research Unit, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy; Vita-Salute San Raffaele University, Milan, Italy.
⁸ Department of Physiology and Pharmacology "V Erspamer", Sapienza University of Rome, Rome, Italy; Hospital San Raffaele of Cassino, Cassino, Italy.
⁹ Department of Clinical and Experimental Sciences, University of Brescia, Brescia, Italy; Department of Continuity of Care and Frailty, ASST Spedali Civili, Brescia, Italy.
¹⁰ Centro Ricerca sulle Demenze, IRCCS Mondino Foundation, Pavia, Italy; University Institute for Advanced Studies (IUSS), Pavia, Italy.
¹¹ Danish Dementia Research Centre, Department of Neurology, Copenhagen University Hospital Rigshospitalet, Copenhagen, Denmark; Department of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark.
¹² Department of Geriatric Psychiatry, Central Institute of Mental Health Mannheim, Medical Faculty Mannheim, University of Heidelberg, Heidelberg, Germany.
¹³ Laboratory of Neuroimaging and Innovative Molecular Tracers (NIMTlab), Geneva University Neurocenter and Faculty of Medicine, University of Geneva, Geneva, Switzerland; Division of Nuclear Medicine and Molecular Imaging, Geneva University Hospitals, Geneva, Switzerland; CIBM Center for Biomedical Imaging, Geneva, Switzerland.
¹⁴ ESEAP-Proficiency Testing Scheme for Clinical Laboratories, Athens, Greece.
¹⁵ German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany; Department of Psychiatry, University of Cologne, Medical Faculty, Cologne, Germany; Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), University of Cologne, Cologne, Germany.
¹⁶ National Institute of Mental Health, Neurology and Neurosurgery, Budapest, Hungary; Department of Neurology, Semmelweis University, Budapest, Hungary.
¹⁷ Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, Netherlands; Radboud UMC Alzheimer Center and Department of Medical Psychology, Radboud University Medical Center, Nijmegen, Netherlands; Vincent van Gogh Institute for Psychiatry, Venray, Netherlands.
¹⁸ Department of Health Sciences (DISSAL), University of Genoa, Genoa, Italy; IRCCS Ospedale Policlinico San Martino, Genoa, Italy.
¹⁹ Department of Psychiatry, School of Clinical Medicine, University of Cambridge, Cambridge, UK.
²⁰ Department of Neurology, Martin Luther University of Halle-Wittenberg, Halle (Saale), Germany.
²¹ Neurobiology, Hospices Civils de Lyon, Lyon, France.
²² Department of Diagnostic and Public Health, Verona University Hospital, Verona University, Verona, Italy.
²³ Department of Neurosciences, KU Leuven, Leuven, Belgium; Department of Geriatric Psychiatry, University Psychiatric Centre KU Leuven, Leuven-Kortenberg, Belgium.
²⁴ University of Eastern Finland and Kuopio University Hospital, Kuopio, Finland.
²⁵ Department of Psychiatry and Neuropsychology-Alzheimer Centre Limburg, School for Mental Health and Neuroscience, Maastricht University, Maastricht, Netherlands.
²⁶ Department of Epidemiology and Department of Radiology and Nuclear Medicine Erasmus MC University Medical Center, Rotterdam, Netherlands.
²⁷ Lysholm Department of Neuroradiology and the Neuroradiological Academic Unit, Department of Brain Repair and Rehabilitation, University College London Hospitals NHS Foundation Trust National Hospital for Neurology and Neurosurgery, London, UK.
²⁸ Fundació ACE, Institut Català de Neurociències Aplicades, Barcelona, Spain.
²⁹ Institut de La Mémoire et de La Maladie d'Alzheimer, Neurology Department, Salpêtrière Hospital, Assistance Publique-Hôpital de Paris, Paris, France; Sorbonne University, Paris, France.
³⁰ Alzheimer Europe, Luxembourg.
³¹ Clinical Memory Research Unit, Department of Clinical Sciences, Lund University, Malmö, Sweden; Memory Clinic, Skåne University Hospital, Malmö, Sweden.
³² Edinburgh Dementia Prevention, Centre for Clinical Brain Sciences, Western General Hospital, University of Edinburgh, Edinburgh, UK; Brain Health Scotland, Edinburgh, UK.
³³ Alzheimer Center Amsterdam, Department of Neurology, Amsterdam Neuroscience, Amsterdam UMC, Amsterdam, Netherlands.
³⁴ Alzheimer Center Amsterdam, Department of Neurology, Amsterdam Neuroscience, Amsterdam UMC, Amsterdam, Netherlands; Amsterdam Neuroscience-Neurodegeneration, Amsterdam, Netherlands; Epidemiology and Data Science, Vrije Universiteit Amsterdam, Amsterdam UMC location VUmc, Amsterdam, Netherlands.

PMID: 38365381
DOI: 10.1016/S1474-4422(23)00447-7

Abstract

The recent commercialisation of the first disease-modifying drugs for Alzheimer's disease emphasises the need for consensus recommendations on the rational use of biomarkers to diagnose people with suspected neurocognitive disorders in memory clinics. Most available recommendations and guidelines are either disease-centred or biomarker-centred. A European multidisciplinary taskforce consisting of 22 experts from 11 European scientific societies set out to define the first patient-centred diagnostic workflow that aims to prioritise testing for available biomarkers in individuals attending memory clinics. After an extensive literature review, we used a Delphi consensus procedure to identify 11 clinical syndromes, based on clinical history and examination, neuropsychology, blood tests, structural imaging, and, in some cases, EEG. We recommend first-line and, if needed, second-line testing for biomarkers according to the patient's clinical profile and the results of previous biomarker findings. This diagnostic workflow will promote consistency in the diagnosis of neurocognitive disorders across European countries.

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Conflict of interest statement

Declaration of interests DA has received research support or honoraria from Roche Diagnostics, Sanofi, and Eli Lilly; has served as a paid consultant for Roche Diagnostics and Takeda; and is a member of the Dementia Management steering committee for the European Association of Neurology. FA has acquired research support (for their institution) from the Italian Ministry of Health, AriSLA (Fondazione Italiana di Ricerca per la SLA), European Research Council, and Alzheimer's Research Foundation; and has served as a speaker for Biogen, Idec, Italfarmaco, Roche, and Zambon. BB has served as a consultant for PIAM; has a patent on neurophysiological markers and neurophysiological treatment approaches in Alzheimer's disease; and has participated on a data safety monitoring board or advisory board for Alector, UCB, Wave, AviadoBio, Lilly/Prevail, and Denali. SFC has received honoraria for lectures or presentations from Biogen, Roche, and Nutrucia, and has served as a consultant for Brain Control. CF has received funding through her institution from the Alzheimer's Association and Italian Ministry of Health. GBF has received funding through the Private Foundation of Geneva University Hospitals from APRA (Association Suisse pour la Recherche sur la Maladie d’Alzheimer), Fondation Segré, Ivan Pictet, Race Against Dementia Foundation, Fondation Child Care, Fondation Edmond J Safra, Fondation Minkoff, Fondazione Agusta, McCall Macbain Foundation, Nicole et René Keller, and Fondation AETAS; has received funding through the University of Geneva or Geneva University Hospitals for investigator-initiated sponsored studies from Roche, OM Pharma, Eisai, Biogen, and Novo Nordisk; has received funding for competitive research projects from EU-Horizon2020, Innovative Medicines Initiative (IMI), IMI2, Swiss National Science Foundation, and VELUX Foundation; and via their institution has served as a consultant or speaker for Biogen, Diadem, Roche, Novo Nordisk, and GE HealthCare. LF has acquired research support through his institution from Hector Foundation (FRAILBRAIN), EU-Horizon2020 (RECAGE, 2D-BioPAD), and EU-IMI2 (RADAR-AD); has received consultancy or speaker fees from Biogen, Eisai, Grifols, Neurimmune, Noselab, NovoNordisk, Roche, Schwabe, and TauRX; has served as an advisory board member for Avanir-Otsuka, Pharmatrophix, Forschungszentrum Jülich, Charité Berlin, Neurimmune, Neurokine Therapeutics, NSC Therapeutics, reMYND NV, Vivoryon, and European Alzheimer's Disease Consortium; and has served on the Alzheimer Europe Expert Advisory Panel (unpaid). VG was supported by the Swiss National Science Foundation (projects 320030_169876, 320030_185028 and IZSEZ0_188355), Velux Foundation (project 1123), Schmidheiny Foundation, and Aetas Foundation; and has received financial support for research or speaker fees through her institution from Siemens Healthineers, GE HealthCare, and Novo Nordisk. JG is an employee of Alzheimer Europe, which has received grants from the EU's Health, Horizon Europe, and Citizens, Equality, Rights and Values programmes, the Innovative Health Initiative, Joint Programme for Neurodegenerative Disease Research, and Luxembourg Fonds National de la Recherche; and has received sponsorship and support from AbbVie, Biogen, Eisai, Essity, Fujirebio, GE HealthCare, Grifols, Janssen, Lilly, MSD, Novo Nordisk, Nutricia, Prothena, Roche, and TauRx. OH has acquired research support (for their institution) from ADx, Avid Radiopharmaceuticals, Biogen, Eli Lilly, Eisai, Fujirebio, GE HealthCare, Pfizer, and Roche; and in the past 2 years has received consultancy or speaker fees from AC Immune, Amylyx, Alzpath, BioArctic, Biogen, Cerveau, Eisai, Eli Lilly, Fujirebio, Merck, Novartis, Novo Nordisk, Roche, Sanofi, and Siemens. AK has received through the National Institute of Mental Health, Neurology and Neurosurgery grants from the National Brain Research Program, Hungary I, II (KTIA_NAP_13-1-2013-0001; 2017-1.2.1-NKP-2017-00002); and she is Secretary and Treasurer of the European, Middle East, and Africa Chapter of the International Society of Clinical Neurophysiology (unpaid). RPCK has received royalties from Hogrefe Test Publishing, Bohn Stafleu Van Loghum, LannooCampus Publishers, and Taylor & Francis; honoraria from Benecke Education Lecture and RINO Utrecht; has served as a consultant for University of Michigan Consultancy, Pearson Assessment, and Europees Fonds voor Regionale Ontwikkeling OP-Oost EU Grant Consultancy (fee paid to university). FM has received a speaker honorarium from Roche Diagnostics. SDM has received grants through her institution from the Italian Ministry of Health; and consulting fees, honoraria, or support for attending meetings from Eli Lilly, GE HealthCare, and Life Molecular Imaging. JTO has received academic support or grants from Avid-Lilly, Merck, and Alliance Medical; has received (for his institution) consulting fees from TauRx, Novo Nordisk, Biogen, Roche, Lilly, and GE HealthCare. SO has received support for attending meetings from PIAM, Alector, and MSD. PS has acquired research support through his institution from Novo Nordisk (co-chair of EVOKE programme), Toyama (Principle Investigator of phase 2b study), UCB (Principle Investigator of phase 1b study), AC Immune (Principle Investigator of phase 1b study), and Alzheon (Principle Investigator of phase 2a study); has served as a consultant for Immunobrain Checkpoint (paid to university); is a member of a data safety and monitoring board of a phase 3 study for AB Science; and is chair of the World Dementia Council (unpaid). WMvdF has conducted research programmes funded by ZonMW, Nederlandse Organisatie voor Wetenschappelijk Onderzoek, European Union–Seventh Framework Programme, European Joint Programme on Neurodegenerative Diseases, Alzheimer Nederland, Hersenstichting CardioVascular Onderzoek Nederland, Health∼Holland, Topsector Life Sciences & Health, Stichting Dioraphte, Gieskes-Strijbis Fonds, Stichting Equilibrio, Edwin Bouw Fonds, Pasman Stichting, Alzheimer & Neuropsychiatrie Foundation, Philips, Biogen MA, Amprion, Novartis-NL, Life Molecular Imaging, Avid, Roche, Fujifilm, Eisai, and Combinostics. WMvdF holds the Pasman chair; is a recipient of ABOARD, which is a public–private partnership receiving funding from ZonMW (#73305095007) and Health∼Holland, Topsector Life Sciences & Health (PPP-allowance; #LSHM20106), all funding is paid to her institution; she is a recipient of TAP-dementia, receiving funding from ZonMw (#10510032120003) in the context of Onderzoeksprogramma Dementie, part of the Dutch National Dementia Strategy; Gieskes Strijbis Fonds also contributes to TAP-dementia. WMvdF is a consultant for the Oxford Health Policy Forum community interest company, Roche, Eisai, and Biogen MA; has been an invited speaker at Boehringer Ingelheim, Biogen MA, Danone, Eisai, WebMD Neurology (Medscape), NovoNordisk, Springer Healthcare, and the European Brain Council; and has participated in advisory boards for Biogen MA, Roche, and Eli Lilly. FV has served as consultant for Biogen (payment to Maastricht University). MV is a recipient of ABOARD, which is a public–private partnership receiving funding from ZonMW (#73305095007) and Health∼Holland, Topsector Life Sciences & Health (PPP-allowance; #LSHM20106); is a recipient of TAP-dementia, a ZonMw funded project (#10510032120003) in the context of the Dutch National Dementia Strategy; and is Chair of the Diagnostic Committee and Member of the Executive Committee of the European Society of Neuroradiology, which is an unpaid position. All other authors declare no competing interests.

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European intersocietal recommendations for the biomarker-based diagnosis of neurocognitive disorders

Affiliations

European intersocietal recommendations for the biomarker-based diagnosis of neurocognitive disorders

Authors

Affiliations

Abstract

Conflict of interest statement

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