Performance evaluation of automated white matter hyperintensity segmentation algorithms in a multicenter cohort on cognitive impairment and dementia.

Alzheimer’s disease FLAIR aging deep learning evaluation white matter hyperintensities segmentation

Journal

Frontiers in psychiatry
ISSN: 1664-0640
Titre abrégé: Front Psychiatry
Pays: Switzerland
ID NLM: 101545006

Informations de publication

Date de publication:
2022
Historique:
received: 02 08 2022
accepted: 07 12 2022
entrez: 30 1 2023
pubmed: 31 1 2023
medline: 31 1 2023
Statut: epublish

Résumé

White matter hyperintensities (WMH), a biomarker of small vessel disease, are often found in Alzheimer's disease (AD) and their advanced detection and quantification can be beneficial for research and clinical applications. To investigate WMH in large-scale multicenter studies on cognitive impairment and AD, appropriate automated WMH segmentation algorithms are required. This study aimed to compare the performance of segmentation tools and provide information on their application in multicenter research. We used a pseudo-randomly selected dataset ( Across tools, segmentation performance was moderate for global WMH volume and number of detected lesions. After retraining on a DELCODE subset, the deep learning algorithm sysu_media showed the highest performances with an average Dice's coefficient of 0.702 (±0.109 SD) for volume and a mean F1-score of 0.642 (±0.109 SD) for the number of lesions. The intra-class correlation was excellent for all algorithms (>0.9) but BIANCA (0.835). Performance improved with high WMH burden and varied across brain regions. To conclude, the deep learning algorithm, when retrained, performed well in the multicenter context. Nevertheless, the performance was close to traditional methods. We provide methodological recommendations for future studies using automated WMH segmentation to quantify and assess WMH along the continuum of cognitive impairment and AD dementia.

Sections du résumé

Background UNASSIGNED
White matter hyperintensities (WMH), a biomarker of small vessel disease, are often found in Alzheimer's disease (AD) and their advanced detection and quantification can be beneficial for research and clinical applications. To investigate WMH in large-scale multicenter studies on cognitive impairment and AD, appropriate automated WMH segmentation algorithms are required. This study aimed to compare the performance of segmentation tools and provide information on their application in multicenter research.
Methods UNASSIGNED
We used a pseudo-randomly selected dataset (
Results UNASSIGNED
Across tools, segmentation performance was moderate for global WMH volume and number of detected lesions. After retraining on a DELCODE subset, the deep learning algorithm sysu_media showed the highest performances with an average Dice's coefficient of 0.702 (±0.109 SD) for volume and a mean F1-score of 0.642 (±0.109 SD) for the number of lesions. The intra-class correlation was excellent for all algorithms (>0.9) but BIANCA (0.835). Performance improved with high WMH burden and varied across brain regions.
Conclusion UNASSIGNED
To conclude, the deep learning algorithm, when retrained, performed well in the multicenter context. Nevertheless, the performance was close to traditional methods. We provide methodological recommendations for future studies using automated WMH segmentation to quantify and assess WMH along the continuum of cognitive impairment and AD dementia.

Identifiants

pubmed: 36713907
doi: 10.3389/fpsyt.2022.1010273
pmc: PMC9877422
doi:

Types de publication

Journal Article

Langues

eng

Pagination

1010273

Investigateurs

Amthauer Holger (A)
Cetindag Arda Can (CA)
Cosma Nicoleta Carmen (CN)
Diesing Dominik (D)
Ehrlich Marie (E)
Fenski Frederike (F)
Freiesleben Silka Dawn (FS)
Fuentes Manuel (F)
Hauser Dietmar (H)
Hujer Nicole (H)
Incesoy Enise Irem (IE)
Kainz Christian (K)
Lange Catharina (L)
Lindner Katja (L)
Megges Herlind (M)
Peters Oliver (P)
Preis Lukas (P)
Altenstein Slawek (A)
Lohse Andrea (L)
Franke Christiana (F)
Priller Josef (P)
Spruth Eike (S)
Villar Munoz Irene (VM)
Barkhoff Miriam (B)
Boecker Henning (B)
Brosseron Frederic (B)
Daamen Marcel (D)
Engels Tanja (E)
Faber Jennifer (F)
Fließbach Klaus (F)
Frommann Ingo (F)
Grobe-Einsler Marcus (GE)
Hennes Guido (H)
Herrmann Gabi (H)
Jost Lorraine (J)
Kalbhen Pascal (K)
Kimmich Okka (K)
Kobeleva Xenia (K)
Kofler Barbara (K)
McCormick Cornelia (M)
Miebach Lisa (M)
Miklitz Carolin (M)
Müller Anna (M)
Oender Demet (O)
Polcher Alexandra (P)
Purrer Veronika (P)
Röske Sandra (R)
Schneider Christine (S)
Schneider Anja (S)
Spottke Annika (S)
Vogt Ina (V)
Wagner Michael (W)
Wolfsgruber Steffen (W)
Yilmaz Sagik (Y)
Bartels Claudia (B)
Dechent Peter (D)
Hansen Niels (H)
Hassoun Lina (H)
Hirschel Sina (H)
Nuhn Sabine (N)
Pfahlert Ilona (P)
Rausch Lena (R)
Schott Björn (S)
Timäus Charles (T)
Werner Christine (W)
Wiltfang Jens (W)
Zabel Lioba (Z)
Zech Heike (Z)
Bader Abdelmajid (B)
Baldermann Juan Carlos (BJ)
Dölle Britta (D)
Drzezga Alexander (D)
Escher Claus (E)
Ghiasi Nasim Roshan (GN)
Hardenacke Katja (H)
Jessen Frank (J)
Lützerath Hannah (L)
Maier Franziska (M)
Marquardt Benjamin (M)
Martikke Anja (M)
Meiberth Dix (M)
Petzler Snjezana (P)
Rostamzadeh Ayda (R)
Sannemann Lena (S)
Schild Ann-Katrin (S)
Sorgalla Susanne (S)
Stockter Simone (S)
Thelen Manuela (T)
Tscheuschler Maike (T)
Uhle Franziska (U)
Zeyen Philip (Z)
Bittner Daniel (B)
Cardenas-Blanco Arturo (CB)
Dobisch Laura (D)
Düzel Emrah (D)
Grieger-Klose Doreen (GK)
Hartmann Deike (H)
Metzger Coraline (M)
Nestor Peter (N)
Ruß Christin (R)
Schulze Franziska (S)
Speck Oliver (S)
Wenzel Glanz (W)
Yakupov Renat (Y)
Ziegler Gabriel (Z)
Brauneis Christine (B)
Bürger Katharina (B)
Catak Cihan (C)
Coloma Andrews Lisa (CA)
Dichgans Martin (D)
Dörr Angelika (D)
Ertl-Wagner Birgit (EW)
Frimmer Daniela (F)
Huber Brigitte (H)
Janowitz Daniel (J)
Kreuzer Max (K)
Markov Eva (M)
Müller Claudia (M)
Rominger Axel (R)
Schmid Ehemals Spreider Jennifer (SES)
Seegerer Anna (S)
Stephan Julia (S)
Zollver Adelgunde (Z)
Burow Lena (B)
de Jonge Sylvia (J)
Falkai Peter (F)
Garcia Angarita Natalie (GA)
Görlitz Thomas (G)
Gürsel Selim Üstün (GS)
Horvath Ildiko (H)
Kurz Carolin (K)
Meisenzahl-Lechner Eva (ML)
Perneczky Robert (P)
Utecht Julia (U)
Dyrba Martin (D)
Janecek-Meyer Heike (JM)
Kilimann Ingo (K)
Lappe Chris (L)
Lau Esther (L)
Pfaff Henrike (P)
Raum Heike (R)
Sabik Petr (S)
Schmidt Monika (S)
Schulz Heike (S)
Schwarzenboeck Sarah (S)
Teipel Stefan (T)
Weber Marc-Andre (W)
Buchmann Martina (B)
Heger Tanja (H)
Hinderer Petra (H)
Kuder-Buletta Elke (KB)
Laske Christoph (L)
Munk Matthias (M)
Mychajliw Christian (M)
Soekadar Surjo (S)
Sulzer Patricia (S)
Trunk Theresia (T)

Informations de copyright

Copyright © 2023 Gaubert, Dell’Orco, Lange, Garnier-Crussard, Zimmermann, Dyrba, Duering, Ziegler, Peters, Preis, Priller, Spruth, Schneider, Fliessbach, Wiltfang, Schott, Maier, Glanz, Buerger, Janowitz, Perneczky, Rauchmann, Teipel, Kilimann, Laske, Munk, Spottke, Roy, Dobisch, Ewers, Dechent, Haynes, Scheffler, Düzel, Jessen and Wirth.

Déclaration de conflit d'intérêts

MDu received fees for consultation and lectures from Roche, Bayer, Hovid Berhad, and Sanofi. OP received fees for consultation and lectures from Biogen, Eisai, Griffols, MSD, Roche, and Schwabe. JP received fees for consultation, lectures, patents from Neurimmune, Axon, Desitin, and Epomedics. JW was an honorary speaker for Actelion, Amgen, Beeijing Yibai Science and Technology Ltd., Janssen Cilag, Med Update GmbH, Pfizer, Roche Pharma, and was a member of the advisory boards of Abbott, Biogen, Boehringer Ingelheim, Lilly, MSD Sharp & Dohme, and Roche Pharma and received fees as a consultant for Immungenetics and Roboscreen. FJ received fees for consultation from Eli Lilly, Novartis, Roche, BioGene, MSD, Piramal, Janssen, and Lundbeck. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Références

Neuroimage Clin. 2020;27:102357
pubmed: 32739882
J Chiropr Med. 2016 Jun;15(2):155-63
pubmed: 27330520
Neuroimage. 2021 Aug 15;237:118140
pubmed: 33957235
Med Image Anal. 2008 Aug;12(4):514-523
pubmed: 18381247
Neuroimage. 2018 Dec;183:650-665
pubmed: 30125711
Alzheimers Res Ther. 2021 Jan 18;13(1):29
pubmed: 33461618
J Am Heart Assoc. 2015 Jun 23;4(6):001140
pubmed: 26104658
Neuroimage. 2017 Jul 15;155:159-168
pubmed: 28435096
Neuroimage. 2016 Nov 1;141:191-205
pubmed: 27402600
Alzheimers Res Ther. 2018 Feb 07;10(1):15
pubmed: 29415768
Sci Rep. 2018 Sep 12;8(1):13650
pubmed: 30209345
Alzheimers Dement. 2022 Mar;18(3):422-433
pubmed: 34322985
Front Neurol. 2019 Mar 26;10:238
pubmed: 30972001
Annu Int Conf IEEE Eng Med Biol Soc. 2016 Aug;2016:3342-3345
pubmed: 28269019
Lancet Neurol. 2013 Aug;12(8):822-38
pubmed: 23867200
Hum Brain Mapp. 2003 Aug;19(4):224-47
pubmed: 12874777
Front Neuroinform. 2011 Aug 22;5:13
pubmed: 21897815
Neuroimage. 2012 Feb 15;59(4):3774-83
pubmed: 22119648
Magn Reson Imaging. 1996;14(5):495-505
pubmed: 8843362
AJNR Am J Neuroradiol. 2006 Oct;27(9):1964-8
pubmed: 17032876
Neuroimage Clin. 2013 Oct 14;3:462-9
pubmed: 24273728
Hum Brain Mapp. 2002 Nov;17(3):143-55
pubmed: 12391568
Nat Rev Neurol. 2015 Mar;11(3):157-65
pubmed: 25686760
BMC Med Imaging. 2015 Aug 12;15:29
pubmed: 26263899
Psychol Bull. 1979 Mar;86(2):420-8
pubmed: 18839484
Magn Reson Imaging. 1998 Apr;16(3):311-8
pubmed: 9621972
IEEE Trans Med Imaging. 2019 Nov;38(11):2556-2568
pubmed: 30908194
Sci Rep. 2019 Nov 14;9(1):16742
pubmed: 31727919
Neuroinformatics. 2015 Jul;13(3):261-76
pubmed: 25649877
Neuroimage. 2010 Dec;53(4):1181-96
pubmed: 20637289
Hum Brain Mapp. 2021 Jun 15;42(9):2734-2745
pubmed: 33783933
J Neurol Sci. 2012 Nov 15;322(1-2):211-6
pubmed: 22921728

Auteurs

Malo Gaubert (M)

German Center for Neurodegenerative Diseases, Dresden, Germany.
Department of Neuroradiology, Rennes University Hospital (CHU), Rennes, France.

Andrea Dell'Orco (A)

German Center for Neurodegenerative Diseases, Dresden, Germany.
Department of Neuroradiology, Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany.

Catharina Lange (C)

German Center for Neurodegenerative Diseases, Dresden, Germany.
Department of Nuclear Medicine, Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany.

Antoine Garnier-Crussard (A)

Clinical and Research Memory Center of Lyon, Lyon Institute for Elderly, Hospices Civils de Lyon, Lyon, France.
Normandie Univ, UNICAEN, INSERM, U1237, PhIND "Physiopathology and Imaging of Neurological Disorders," Institut Blood and Brain @ Caen-Normandie, Caen, France.
Neuroscience Research Centre of Lyon, INSERM 1048, CNRS 5292, Lyon, France.

Isabella Zimmermann (I)

German Center for Neurodegenerative Diseases, Dresden, Germany.

Martin Dyrba (M)

German Center for Neurodegenerative Diseases, Rostock, Germany.

Marco Duering (M)

Department of Biomedical Engineering, Medical Image Analysis Center (MIAC) and qbig, University of Basel, Basel, Switzerland.

Gabriel Ziegler (G)

German Center for Neurodegenerative Diseases, Magdeburg, Germany.

Oliver Peters (O)

German Center for Neurodegenerative Diseases, Berlin, Germany.
Department of Psychiatry, Charité - Universitätsmedizin Berlin, Berlin, Germany.

Lukas Preis (L)

Department of Psychiatry, Charité - Universitätsmedizin Berlin, Berlin, Germany.

Josef Priller (J)

German Center for Neurodegenerative Diseases, Berlin, Germany.
Department of Psychiatry and Psychotherapy, Charité - Universitätsmedizin Berlin, Berlin, Germany.
Centre for Clinical Brain Sciences, University of Edinburgh and UK Dementia Research Institute (DRI), Edinburgh, United Kingdom.
Department of Psychiatry and Psychotherapy, School of Medicine, Technical University of Munich, Munich, Germany.

Eike Jakob Spruth (EJ)

German Center for Neurodegenerative Diseases, Berlin, Germany.
Department of Psychiatry and Psychotherapy, Charité - Universitätsmedizin Berlin, Berlin, Germany.

Anja Schneider (A)

German Center for Neurodegenerative Diseases, Bonn, Germany.
Department of Neurodegenerative Disease and Geriatric Psychiatry, University of Bonn Medical Center, Bonn, Germany.

Klaus Fliessbach (K)

German Center for Neurodegenerative Diseases, Bonn, Germany.
Department of Neurodegenerative Disease and Geriatric Psychiatry, University of Bonn Medical Center, Bonn, Germany.

Jens Wiltfang (J)

German Center for Neurodegenerative Diseases, Göttingen, Germany.
Department of Psychiatry and Psychotherapy, University Medical Center Göttingen, University of Göttingen, Göttingen, Germany.
Department of Medical Sciences, Neurosciences and Signaling Group, Institute of Biomedicine (iBiMED), University of Aveiro, Aveiro, Portugal.

Björn H Schott (BH)

German Center for Neurodegenerative Diseases, Göttingen, Germany.
Department of Psychiatry and Psychotherapy, University Medical Center Göttingen, University of Göttingen, Göttingen, Germany.
Leibniz Institute for Neurobiology, Magdeburg, Germany.

Franziska Maier (F)

Department of Psychiatry, Medical Faculty, University of Cologne, Cologne, Germany.

Wenzel Glanz (W)

German Center for Neurodegenerative Diseases, Magdeburg, Germany.

Katharina Buerger (K)

German Center for Neurodegenerative Diseases, Munich, Germany.
Department of Psychiatry and Psychotherapy, University Hospital, Ludwig Maximilian University of Munich (LMU), Munich, Germany.

Daniel Janowitz (D)

Department of Psychiatry and Psychotherapy, University Hospital, Ludwig Maximilian University of Munich (LMU), Munich, Germany.

Robert Perneczky (R)

German Center for Neurodegenerative Diseases, Munich, Germany.
Department of Psychiatry and Psychotherapy, University Hospital, Ludwig Maximilian University of Munich (LMU), Munich, Germany.
Munich Cluster for Systems Neurology (SyNergy) Munich, Munich, Germany.
Ageing Epidemiology Research Unit (AGE), School of Public Health, Imperial College London, London, United Kingdom.
Sheffield Institute for Translational Neuroscience (SITraN), University of Sheffield, Sheffield, United Kingdom.

Boris-Stephan Rauchmann (BS)

Department of Psychiatry and Psychotherapy, University Hospital, Ludwig Maximilian University of Munich (LMU), Munich, Germany.

Stefan Teipel (S)

German Center for Neurodegenerative Diseases, Rostock, Germany.
Department of Psychosomatic Medicine, Rostock University Medical Center, Rostock, Germany.

Ingo Kilimann (I)

German Center for Neurodegenerative Diseases, Rostock, Germany.
Department of Psychosomatic Medicine, Rostock University Medical Center, Rostock, Germany.

Christoph Laske (C)

German Center for Neurodegenerative Diseases, Tübingen, Germany.
Department of Psychiatry and Psychotherapy, University of Tübingen, Tübingen, Germany.

Matthias H Munk (MH)

German Center for Neurodegenerative Diseases, Tübingen, Germany.
Department of Psychiatry and Psychotherapy, University of Tübingen, Tübingen, Germany.

Annika Spottke (A)

German Center for Neurodegenerative Diseases, Bonn, Germany.
Department of Neurology, University of Bonn, Bonn, Germany.

Nina Roy (N)

German Center for Neurodegenerative Diseases, Bonn, Germany.

Laura Dobisch (L)

German Center for Neurodegenerative Diseases, Magdeburg, Germany.

Michael Ewers (M)

German Center for Neurodegenerative Diseases, Munich, Germany.

Peter Dechent (P)

MR-Research in Neurosciences, Department of Cognitive Neurology, Georg-August-University of Göttingen, Göttingen, Germany.

John Dylan Haynes (JD)

Bernstein Center for Computational Neuroscience, Charité - Universitätsmedizin, Berlin, Germany.

Klaus Scheffler (K)

Department for Biomedical Magnetic Resonance, University of Tübingen, Tübingen, Germany.

Emrah Düzel (E)

German Center for Neurodegenerative Diseases, Magdeburg, Germany.
Institute of Cognitive Neurology and Dementia Research (IKND), Otto-von-Guericke University, Magdeburg, Germany.

Frank Jessen (F)

German Center for Neurodegenerative Diseases, Bonn, Germany.
Department of Psychiatry, Medical Faculty, University of Cologne, Cologne, Germany.
Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), University of Cologne, Köln, Germany.

Miranka Wirth (M)

German Center for Neurodegenerative Diseases, Dresden, Germany.

Classifications MeSH