Long-term follow-up of neurodegenerative phenomenon in severe traumatic brain injury using MRI

Pierre Simeone; Guillaume Auzias; Julien Lefevre; Sylvain Takerkart; Olivier Coulon; Blandine Lesimple; Grégory Torkomian; Valentine Battisti; Alice Jacquens; David Couret; Lionel Naccache; Eleonore Bayen; Nicolas Bruder; Vincent Perlbarg; Louis Puybasset; Lionel Velly

doi:10.1016/j.rehab.2021.101599

Long-term follow-up of neurodegenerative phenomenon in severe traumatic brain injury using MRI

Ann Phys Rehabil Med. 2022 Nov;65(6):101599. doi: 10.1016/j.rehab.2021.101599. Epub 2022 Feb 15.

Authors

Pierre Simeone¹, Guillaume Auzias², Julien Lefevre², Sylvain Takerkart², Olivier Coulon², Blandine Lesimple³, Grégory Torkomian⁴, Valentine Battisti⁴, Alice Jacquens⁴, David Couret⁵, Lionel Naccache⁶, Eleonore Bayen⁷, Nicolas Bruder⁸, Vincent Perlbarg⁹, Louis Puybasset¹⁰, Lionel Velly¹¹

Affiliations

¹ Aix Marseille University, AP-HM, Department of Anesthesiology and Critical Care Medicine, University Hospital Timone, Marseille, France; Aix Marseille University, CNRS, Inst Neurosci Timone, UMR7289 Marseille, France.
² Aix Marseille University, CNRS, Inst Neurosci Timone, UMR7289 Marseille, France; Aix Marseille University, CNRS, Laboratoire des Sciences de l'Information et des Systèmes, UMR7296 Marseille, France.
³ Sorbonne Université, CNRS, INSERM, Laboratoire d'Imagerie Biomédicale, 75006, Paris, France.
⁴ Sorbonne Université, AP-HP, Department of Anesthesiology and Critical Care Medicine, Hôpital Pitié-Salpêtrière, 75006 Paris, France.
⁵ Réunion University, Neurocritical Care Unit, Hospital Saint-Pierre, BP350, Saint-Pierre, 97448 La Réunion, France.
⁶ Sorbonne Université, Institut du Cerveau et de la Moelle Epinière, PICNIC LAB, AP-HP, Hôpital Pitié-Salpêtrière, 75006 Paris, France.
⁷ Service de Médecine Physique et Réadaptation, Groupe Hospitalier Pitié-Salpêtrière, Assistance Publique-Hôpitaux de Paris (APHP), Paris, France.
⁸ Aix Marseille University, AP-HM, Department of Anesthesiology and Critical Care Medicine, University Hospital Timone, Marseille, France.
⁹ BrainTale SAS (V.P.), 75013 Paris, France.
¹⁰ Sorbonne Université, CNRS, INSERM, Laboratoire d'Imagerie Biomédicale, 75006, Paris, France; Sorbonne Université, AP-HP, Department of Anesthesiology and Critical Care Medicine, Hôpital Pitié-Salpêtrière, 75006 Paris, France.
¹¹ Aix Marseille University, AP-HM, Department of Anesthesiology and Critical Care Medicine, University Hospital Timone, Marseille, France; Aix Marseille University, CNRS, Inst Neurosci Timone, UMR7289 Marseille, France. Electronic address: lionel.velly@ap-hm.fr.

PMID: 34718191
DOI: 10.1016/j.rehab.2021.101599

Abstract

Background: Traumatic brain injury (TBI) lesions are known to evolve over time, but the duration and consequences of cerebral remodelling are unclear. Degenerative mechanisms occurring in the chronic phase after TBI could constitute "tertiary" lesions related to the neurological outcome.

Objective: The objective of this prospective study of severe TBI was to longitudinally evaluate the volume of white and grey matter structures and white matter integrity with 2 time-point multimodal MRI.

Methods: Longitudinal MRI follow-up was obtained for 11 healthy controls (HCs) and 22 individuals with TBI (mean [SD] 60 [15] months after injury) along with neuropsychological assessments. TBI individuals were classified in the "favourable" recovery group (Glasgow Outcome Scale Extended [GOSE] 6-8) and "unfavourable" recovery group (GOSE 3-5) at 5 years. Variation in brain volumes (3D T1-weighted image) and white matter integrity (diffusion tensor imaging [DTI]) were quantitatively assessed over time and used to predict neurological outcome.

Results: TBI individuals showed a marked decrease in volumes of whole white matter (median -11.4% [interquartile range -5.8; -14.6]; p < 0.001) and deep grey nuclear structures (-17.1% [-10.6; -20.5]; p < 0.001). HCs did not show any significant change over the same time period. Median volumetric loss in several brain regions was higher with GOSE 3-5 than 6-8. These lesions were associated with lower fractional anisotropy and higher mean diffusivity at baseline. Volumetric variations were positively correlated with normalized fractional anisotropy and negatively with normalized mean diffusivity at baseline and follow-up. A computed predictive model with baseline DTI showed good accuracy to predict neurological outcome (area under the receiver operating characteristic curve 0.82 [95% confidence interval 0.81-0.83]) CONCLUSIONS: We characterised the striking atrophy of deep brain structures after severe TBI. DTI imaging in the subacute phase can predict the occurrence and localization of these tertiary lesions as well as long-term neurological outcome.

Trial registration: ClinicalTrials.gov: NCT00577954. Registered on October 2006.

Keywords: Brain atrophy; Longitudinal; Magnetic resonance imaging; Neurodegeneration; Prognosis; Traumatic brain injury.

MeSH terms

Brain / pathology
Brain Injuries, Traumatic* / complications
Brain Injuries, Traumatic* / diagnostic imaging
Brain Injuries, Traumatic* / pathology
Case-Control Studies
Diffusion Tensor Imaging*
Follow-Up Studies
Humans
Magnetic Resonance Imaging
Prospective Studies

Associated data

ClinicalTrials.gov/NCT00577954