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Prognostic value of global deep white matter DTI metrics for 1-year outcome prediction in ICU traumatic brain injury patients: an MRI-COMA and CENTER-TBI combined study

Intensive Care Medicine volume 48, pages 201–212 (2022)Cite this article

A Correction to this article was published on 20 January 2022

This article has been updated

Abstract

Purpose

A reliable tool for outcome prognostication in severe traumatic brain injury (TBI) would improve intensive care unit (ICU) decision-making process by providing objective information to caregivers and family. This study aimed at designing a new classification score based on magnetic resonance (MR) diffusion metrics measured in the deep white matter between day 7 and day 35 after TBI to predict 1-year clinical outcome.

Methods

Two multicenter cohorts (29 centers) were used. MRI-COMA cohort (NCT00577954) was split into MRI-COMA-Train (50 patients enrolled between 2006 and mid-2014) and MRI-COMA-Test (140 patients followed up in clinical routine from 2014) sub-cohorts. These latter patients were pooled with 56 ICU patients (enrolled from 2014 to 2020) from CENTER-TBI cohort (NCT02210221). Patients were dichotomised depending on their 1-year Glasgow outcome scale extended (GOSE) score: GOSE 1–3, unfavorable outcome (UFO); GOSE 4–8, favorable outcome (FO). A support vector classifier incorporating fractional anisotropy and mean diffusivity measured in deep white matter, and age at the time of injury was developed to predict whether the patients would be either UFO or FO.

Results

The model achieved an area under the ROC curve of 0.93 on MRI-COMA-Train training dataset, and 49% sensitivity for 96.8% specificity in predicting UFO and 58.5% sensitivity for 97.1% specificity in predicting FO on the pooled MRI-COMA-Test and CENTER-TBI validation datasets.

Conclusion

The model successfully identified, with a specificity compatible with a personalized decision-making process in ICU, one in two patients who had an unfavorable outcome at 1 year after the injury, and two-thirds of the patients who experienced a favorable outcome.

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Acknowledgements

We would like to thank patients, relatives, and clinical and research staff at all trial sites. The members of MRI-COMA investigators are: Charlène Aubinet, Manon Carrière, Carol Di Perri, Steven Laureys, Andrea Soddu, Audrey Vanhaudenhuyse: Cyclotron Research Center and Department of Neurology, University of Liège, Liège, Belgium. Julien Amour: Department of Anesthesiology and Critical Care, Institut de cardiologie, Groupe Hospitalier Pitié-Salpêtrière, Paris, France. Charlotte Arbelot, Jean-Jacques Rouby, Corine Vezinet: Department of Intensive Care, Groupe Hospitalier Pitié-Salpêtrière, Paris, France. Laurent Barral, Jean-Paul Roustan: Department of Intensive Care, University Hospital of Montpellier, Montpellier, France. Nicolas Bruder: Department of Anesthesiology and Critical Care, University Hospital Timone Adultes, Marseille, France. Russel Chabanne, Jean-Michel Constantin: Department of Anesthesiology and Critical Care, University Hospital of Clermont-Ferrand, Clermont-Ferrand, France. Leila Chamard: Department of Neuroradiology, Neurological Hospital, Hospices civils de Lyon, Lyon, France. Jean Chastre, Charles-Edouard Luyt: Department of Medical Intensive Care, Institut de cardiologie, Groupe Hospitalier Pitié-Salpêtrière, Paris, France. Vincent Cottenceau, François Sztark, Olivier Verdonck: Department of Anesthesiology and Critical Care, University Hospital Pellegrin, Bordeaux, France. David Couret: Department of Intensive Care, University Hospital Sud Réunion, Saint-Pierre, France. Frédéric Dailler, Thomas Ritzenthaler: Department of Intensive Care, Neurological Hospital, Hospices civils de Lyon, Lyon, France. Vincent Degos, Louis Puybasset: Department of Neuro Critical Care, Groupe Hospitalier Pitié-Salpêtrière, Paris Francis Bolgert , Nicolas Weiss, Sophie Demeret, Alexandre Demoule, Alexandre Duguet, Thomas Similowski: Department of Respiratory and Critical Care Medicine, Groupe Hospitalier Pitié-Salpêtrière, Paris, France. Pierre-Guy Durand: Department of Intensive Care, Saint-Jean Hospital, Perpignan, France. Damien Galanaud: Department of Neuroradiology, Groupe Hospitalier Pitié-Salpêtrière, Paris, France. Michèle Génestal, Stein Silva: Department of Anesthesiology and Critical Care, University Hospital Purpan, Toulouse, France. Nadine Girard: Department of Neuroradiology, University Hospital Timone Adultes, Marseille, France. Betty Jean: Department of Neuroradiology, University Hospital of Clermont-Ferrand, Clermont-Ferrand, France. Stéphane Kremer: Department of Neuroradiology, University Hospital of Strasbourg, Strasbourg, France. Olivier Langeron, Mathieu Raux: Department of Anesthesiology and Critical Care, Groupe Hospitalier Pitié-Salpêtrière, Paris, France. Nathalie Laquay: Department of Intensive Care, Saint-Anne Hospital, Paris, France. Jean-Albert Lotterie: Neuro-Campus Baudot, Institut des Sciences du Cerveau, Toulouse, France. Nicolas Menjot de Champfleur: Department of Neuroradiology, University Hospital of Montpellier, Montpellier, France. Sandrine Molinier, Thomas Tourdias: Department of Neuroradiology, University Hospital Pellegrin, Bordeaux, France. Sandrine Mons: Department of Intensive Care, Hospital of Papeete, Papeete, France. Catherine Oppenheim: Department of Neuroradiology, Saint-Anne Hospital, Paris, France. Julien Pottecher: Department of Intensive Care, University Hospital of Strasbourg, Strasbourg, France. Benjamin Rohaut: Neurological Intensive Care Unit, Institut de Neurosciences, Groupe Hospitalier Pitié-Salpêtrière, Paris, France.Gustavo Sotoares: Department of Neuroradiology, University Hospital Roger Salengro, Lille, France. Eléonore Tollard: Department of Neuroradiology, University Hospital of Rouen, Rouen, France. Benoît Veber: Department of Intensive Care, University Hospital of Rouen, Rouen, France. Emmanuel Vega: Department of Intensive Care, University Hospital Roger Salengro, Lille, France. Cristina Agostinis: Department of Neuroradiology, Hospital Papa Giovanni XXIII, Bergamo, Italy. Mariagiulia Anglani: Department of Neuroradiology, University Hospital of Padova, Padova, Italy. Giuseppe Citerio, Alessia Vargiolu: School of Medicine, University of Milano - Bicocca, Monza, Italy. Moreno Curti, Francesco Della Corte, Francesca Grossi: Department of Anesthesia and Critical Care, Maggiore della Carita-Emergenza, Novara, Italy. Roberto Alberto De Blasi, Livia Errico: Department of Anesthesia and Critical Care, Sant’Andrea Hospital, Roma, Italy. Paolo Gritti: Department of Anesthesia and Critical Care, Hospital Papa Giovanni XXIII, Bergamo, Italy. Marina Munari: Department of Anesthesia and Critical Care, University Hospital of Padova, Padova, Italy. Mirko Patassini: Department of Neuroscience, Hospital San Gerardo, Monza, Italy. The members of CENTER-TBI MRI participants and MRI only investigators: Véronique De Keyser, Andrew I.R. Maas, Tomas Menovsky, Gregory Van der Steen: Department of Neurosurgery, Antwerp University Hospital and University of Antwerp, Edegem, Belgium. Bart Depreitere: Department of Neurosurgery, University Hospitals Leuven, Leuven, Belgium. Alexandre Ghuysen, Emergency Department, CHU, Liège, Belgium. Steven Laureys, Didier Ledoux, Benoit Misset: Cyclotron Research Center, University of Liège, Liège, Belgium. Paul M. Parizel: Department of Radiology, University of Antwerp, Edegem, Belgium. Wim Van Hecke, Thijs Vande Vyvere, Jan Verheyden: icoMetrix NV, Leuven, Belgium. Jussi P. Posti, Olli Tenovuo: Division of Clinical Neurosciences, Department of Neurosurgery and Turku Brain Injury Centre, Turku University Hospital and University of Turku, Turku, Finland. Riikka Takala: Perioperative Services, Intensive Care Medicine and Pain Management, Turku University Hospital and University of Turku, Turku, Finland. Peter Ylén: VTT Technical Research Centre, Tampere, Finland. Philippe Azouvi: Raymond Poincaré Hospital, Assistance Publique—Hôpitaux de Paris, Paris, France. Habib Benali, Vincent Degos, Damien Galanaud, Vincent Perlbarg, Louis Puybasset: Department of Anesthesiology and Critical Care, Pitié-Salpêtrière Teaching Hospital, Assistance Publique—Hôpitaux de Paris and Sorbonne Université, Paris; Laboratoire d’Imagerie Biomédicale, Sorbonne Université, Inserm, CNRS, Paris, France. Ana Kowark, Rolf Rossaint: Department of Anaesthesiology, University Hospital of Aachen, Aachen, Germany. Hans Clusmann: Department of Neurosurgery, Medical Faculty RWTH Aachen University, Aachen, Germany. Mark Coburn: Department of Anesthesiology and Intensive Care Medicine, University Hospital Bonn, Bonn, Germany. Krisztina Amrein, József Nyirádi: János Szentágothai Research Centre, University of Pécs, Pécs, Hungary. Andras Buki, Endre Czeiter: Department of Neurosurgery, Medical School, University of Pécs; Neurotrauma Research Group, János Szentágothai Research Centre, University of Pécs, Pécs, Hungary. Erzsébet Ezer, Zoltán Vámos: Department of Anaesthesiology and Intensive Therapy, University of Pécs, Pécs, Hungary. Noémi Kovács: Hungarian Brain Research Program—Grant No. KTIA_13_NAP-A-II/8, University of Pécs, Pécs, Hungary. Abayomi Sorinola, Viktória Tamás: Department of Neurosurgery, University of Pécs, Pécs, Hungary. Alessio Caccioppola, Emiliana Calappi, Marco Carbonara, Fabrizio Ortolano, Tommaso Zoerle: Neuro ICU, Fondazione IRCCS Cà Granda Ospedale Maggiore Policlinico, Milano, Italy. Giuseppe Citerio: School of Medicine and Surgery, Università Milano Bicocca, Milano, Italy, NeuroIntensive Care, ASST di Monza, Monza, Italy. Paolo Persona, Sandra Rossi: Department of Anesthesia and Intensive Care, Azienda Ospedaliera Università di Padova, Padova, Italy. Nino Stocchetti: Department of Pathophysiology and Transplantation, Milan University, and Neuroscience ICU, Fondazione IRCCS Cà Granda Ospedale Maggiore Policlinico, Milano, Italy. Nada Andelic: Division of Surgery and Clinical Neuroscience, Department of Physical Medicine and Rehabilitation, Oslo University Hospital and University of Oslo, Oslo, Norway. Lasse Andreassen: Department of Neurosurgery, University Hospital Northern Norway, Tromsø, Norway. Audny Anke: Department of Physical Medicine and Rehabilitation, University Hospital Northern Norway, Tromsø, Norway. Live Eikenes: Department of Circulation and Medical Imaging, Norwegian University of Science and Technology, NTNU, Trondheim, Norway. Shirin Frisvold: Department of Anesthesiology and Intensive care, University Hospital Northern Norway, Tromsø, Norway. Asta Haberg, Toril Skandsen: Department of Neuromedicine and Movement Science, Norwegian University of Science and Technology, NTNU, Trondheim; Department of Physical Medicine and Rehabilitation, St.Olavs Hospital, Trondheim University Hospital, Trondheim, Norway. Eirik Helseth: Department of Neurosurgery, Oslo University Hospital, Oslo, Norway. Ingeborg Nakken: Department of Radiology and Nuclear Medicine, St. Olavs Hospital, Trondheim University Hospital, Trondheim, Norway. Wibeke Nordhøy: Department of Diagnostic Physics, Clinic of Radiology and Nuclear Medicine, Oslo University Hospital, Oslo, Norway. Cecilie Roe: Department of Physical Medicine and Rehabilitation, Oslo University Hospital/University of Oslo, Oslo, Norway. Olav Roise: Division of Orthopedics, Oslo University Hospital, Oslo, Norway; Institute of Clinical Medicine, Faculty of medicine, University of Oslo, Oslo, Norway. Anne Vik: Department of Neuromedicine and Movement Science, Norwegian University of Science and Technology, NTNU, Trondheim; Department of Neurosurgery, St.Olavs Hospital, Trondheim University Hospital, Trondheim, Norway. Lars T. Westlye: Norwegian Centre for Mental Disorders Research (NORMENT), Division of Mental Health and Addiction, Oslo University Hospital and Institute of Clinical Medicine, University of Oslo and Department of Psychology, University of Oslo, Oslo, Norway. Bo-Michael Bellander: Department of Neurosurgery and Anesthesia and intensive care medicine, Karolinska University Hospital, Stockholm, Sweden. Visakh Muraleedharan: Karolinska Institutet, INCF International Neuroinformatics Coordinating Facility, Stockholm, Sweden. Kelly Foks: Department of Neurology, Erasmus MC, Rotterdam, The Netherlands. Iain Haitsma, Victor Volovici: Department of Neurosurgery, Erasmus MC, Rotterdam, The Netherlands. Hester Lingsma: Department of Public Health, Erasmus Medical Center-University Medical Center, Rotterdam, The Netherlands. Wilco Peul: Dept. of Neurosurgery, Leiden University Medical Center, Leiden, The Netherlands and Dept. of Neurosurgery, Medical Center Haaglanden, The Hague, The Netherlands. Ewout W. Steyerberg: Department of Public Health, Erasmus Medical Center-University Medical Center, Rotterdam; Department. of Department of Biomedical Data Sciences, Leiden University Medical Center, Leiden, The Netherlands. Jonathan Coles: Department of Anesthesia and Neurointensive Care, Cambridge University Hospital NHS Foundation Trust, Cambridge, UK. Marta Correia: Radiology/MRI department, MRC Cognition and Brain Sciences Unit, Cambridge, UK. Ben Glocker, Daniel Rueckert: Department of Computing, Imperial College London, London, UK. Peter J. Hutchinson: Division of Neurosurgery, Department of Clinical Neurosciences, Addenbrooke’s Hospital and University of Cambridge, Cambridge, UK. Evgenios Kornaropoulos, David K. Menon, Virginia Newcombe, Sophie Richter, Emmanuel Stamatakis, Guy Williams, Stefan Winzeck: Division of Anaesthesia, University of Cambridge, Addenbrooke’s Hospital, Cambridge, UK. Geoffrey Manley: Department of Neurological Surgery, University of California, San Francisco, CA, USA.

Funding

The MRI-COMA trial was funded by independent research grants from non-profit or governmental agencies: French Ministry of Health, Paris, France (Programme Hospitalier de Recherche Clinique 2005 #051061), and the French National Agency for Research (ANR) for the program “Investissements d’avenir” ANR-10-IAIHU-06 (to the Brain and Spine Institute); Italian Ministry of health and Regione Lombardia (Ricerca Finalizzata 2010-RF-2010-2319503). CENTER-TBI data used in preparation of this manuscript were obtained in the context of CENTER-TBI, a large collaborative project with the support of the European Union 7th Framework program (EC grant 602150). Additional funding was obtained from the Hannelore Kohl Stiftung (Germany), from OneMind (USA) and from Integra LifeSciences Corporation (USA).

Author information

Authors and Affiliations

  1. Neurosurgical Intensive Care Unit, APHP, Sorbonne Université, Hôpital Pitié-Salpêtrière, Paris, France

    Louis Puybasset, Jean Unrug, Grégory Torkomian & Valentine Battisti

  2. Laboratoire d’Imagerie Biomédicale (LIB), Sorbonne Université, CNRS, INSERM, Paris, France

    Louis Puybasset, Jean Unrug, Didier Cassereau, Damien Galanaud, Muriel Lefort, Éléonore Bayen & Mélanie Pelegrini-Issac

  3. Department of Anesthesiology and Intensive Care, Groupe Hospitalier Pitié-Salpêtrière, Assistance Publique-Hôpitaux de Paris, 47-83 Boulevard de l’Hôpital, 75013, Paris, France

    Louis Puybasset

  4. Clinical Research Group 29, Sorbonne Université, Paris, France

    Louis Puybasset & Vincent Degos

  5. BrainTale SAS, Paris, France

    Vincent Perlbarg

  6. Department of Neuroradiology, APHP, Sorbonne Université, Hôpital Pitié-Salpêtrière, Paris, France

    Damien Galanaud

  7. Department of Anesthesiology and Critical Care Medicine, University Hospital Timone, AP-HM, Aix Marseille University, Marseille, France

    Lionel Velly

  8. CNRS, Institute of Neuroscience Timone, UMR7289, Aix Marseille University, Marseille, France

    Lionel Velly

  9. Department of Anesthesia, Critical Care and Peri-Operative Medicine, APHP, Sorbonne Université, Hôpital Pitié-Salpêtrière, Paris, France

    Vincent Degos

  10. INSERM UMR 1141, Paris, France

    Vincent Degos

  11. Department of Medicine and Surgery, University of Milano-Bicocca, Monza, Italy

    Guiseppe Citerio

  12. Neurointensive Care Unit, Department of Emergency and Urgency, ASST-Monza, San Gerardo Hospital, Monza, Italy

    Guiseppe Citerio

  13. Rehabilitation Unit, APHP, Sorbonne Université, Hôpital Pitié-Salpêtrière, Paris, France

    Éléonore Bayen

Authors
  1. Louis Puybasset
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  2. Vincent Perlbarg
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  3. Jean Unrug
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  4. Didier Cassereau
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  5. Damien Galanaud
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  6. Grégory Torkomian
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  7. Valentine Battisti
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  8. Muriel Lefort
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  9. Lionel Velly
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  10. Vincent Degos
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  11. Guiseppe Citerio
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  12. Éléonore Bayen
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  13. Mélanie Pelegrini-Issac
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Consortia

the MRI-COMA Investigators CENTER-TBI MRI Participants and MRI Only Investigators

Contributions

Conceptualization: LP, VP, LV, EB, MPI. Methodology: MPI, VP, JU. Software: MPI, VP, JU. Validation: all. Formal analysis: MPI, VP, JU. Investigation: VB, GC, VD, DG, LP, GT. Resources: GC, VD, DG, LP. Data curation: VB, DC, ML, GT, JU. Writing—original draft: MPI, VP, EB, LP. Writing—review and editing: all. Visualization: MPI, JU. Supervision: LP, VD, VP, MPI. Project administration: LP, GT, MPI. Funding acquisition: LP. All approved the final version.

Corresponding author

Correspondence to Louis Puybasset.

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Conflicts of interest

DG, LP, and VP share together with institutions (APHP, INSERM, CNRS, and Sorbonne Université) the property of patent WO2012160316, which partly covers the research of the present study. DC, DG, LP, and VP are co-founders and members of the advisory board of Braintale SAS in terms approved by Sorbonne Université (Paris, France) in accordance with its policy on objectivity in research. GC is Editor in Chief of Intensive Care Medicine. The other authors do not have any conflict of interest to disclose.

Ethical approval

Both MRI-COMA (NCT00577954) and CENTER-TBI (NCT02210221) studies were conducted in accordance with all relevant laws of the EU if directly applicable or of direct effect and all relevant laws of the country where the Recruiting sites were located, including but not limited to, the relevant privacy and data protection laws and regulations (the “Privacy Law”), the relevant laws and regulations on the use of human materials, and all relevant guidance relating to clinical studies from time to time in force including, but not limited to, the ICH Harmonised Tripartite Guideline for Good Clinical Practice (CPMP/ICH/135/95) (“ICH GCP”) and the World Medical Association Declaration of Helsinki entitled “Ethical Principles for Medical Research Involving Human Subjects”. Ethical approval was obtained for each recruiting site. For details regarding MRI-COMA, the Direction de la Recherche Clinique et de l’Innovation (DRCI), Assistance Publique Hôpitaux de Paris (Paris, France) can be contacted: secretariat-direction.drc@aphp.fr. For CENTER-TBI, the list of sites, Ethical Committees, approval numbers and approval dates can be found on the website: https://www.center-tbi.eu/project/ethical-approval.

Consent to participate

CENTER-TBI: Informed Consent by the patients and/or the legal representative/next of kin was obtained, accordingly to the local legislations, for all patients recruited in the Core Dataset of CENTER-TBI and documented in the e-CRF. MRI-COMA: Informed Consent by the patients and/or the legal representative/next of kin was obtained, accordingly to the local legislations.

Consent for publication

Not applicable.

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The original online version of this article was revised: The copyright year for this article was incorrectly given as 2022 but should have been 2021.

The members of MRI-COMA Investigators and CENTER-TBI MRI Participants and MRI Only Investigators are listed in “Acknowledgements”.

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Puybasset, L., Perlbarg, V., Unrug, J. et al. Prognostic value of global deep white matter DTI metrics for 1-year outcome prediction in ICU traumatic brain injury patients: an MRI-COMA and CENTER-TBI combined study. Intensive Care Med 48, 201–212 (2022). https://doi.org/10.1007/s00134-021-06583-z

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Keywords

  • Traumatic brain injury
  • Outcome
  • Prognosis
  • Diffusion tensor imaging
  • Deep white matter