Cerebral perfusion using ASL in patients with COVID-19 and neurological manifestations: A retrospective multicenter observational study - 24/08/23
Doi : 10.1016/j.neurad.2023.01.005
François-Daniel Ardellier a, c, 1, ⁎ 
, Seyyid Baloglu a, 1, Magdalena Sokolska b, v, Vincent Noblet c, François Lersy a, Olivier Collange d, Jean-Christophe Ferré e, Adel Maamar f, Béatrice Carsin-Nicol e, Julie Helms g, h, Maleka Schenck i, Antoine Khalil j, Augustin Gaudemer k, Sophie Caillard h, l, Julien Pottecher m, Nicolas Lefèbvre n, Pierre-Emmanuel Zorn o, Muriel Matthieu o, Jean Christophe Brisset p, Clotilde Boulay q, Véronique Mutschler q, Yves Hansmann n, Paul-Michel Mertes d, Francis Schneider i, Samira Fafi-Kremer r, Mickael Ohana s, Ferhat Meziani g, t, Nicolas Meyer u, Tarek Yousry v, Mathieu Anheim q, w, François Cotton x, y, Hans Rolf Jäger v, Stéphane Kremer a, c
for the
, Seyyid Baloglu a, 1, Magdalena Sokolska b, v, Vincent Noblet c, François Lersy a, Olivier Collange d, Jean-Christophe Ferré e, Adel Maamar f, Béatrice Carsin-Nicol e, Julie Helms g, h, Maleka Schenck i, Antoine Khalil j, Augustin Gaudemer k, Sophie Caillard h, l, Julien Pottecher m, Nicolas Lefèbvre n, Pierre-Emmanuel Zorn o, Muriel Matthieu o, Jean Christophe Brisset p, Clotilde Boulay q, Véronique Mutschler q, Yves Hansmann n, Paul-Michel Mertes d, Francis Schneider i, Samira Fafi-Kremer r, Mickael Ohana s, Ferhat Meziani g, t, Nicolas Meyer u, Tarek Yousry v, Mathieu Anheim q, w, François Cotton x, y, Hans Rolf Jäger v, Stéphane Kremer a, cfor the
SFNR-COVID group2
SFNR-COVID group:Toulouse University Hospital (Toulouse) : Fabrice Bonneville, Gilles Adam, Guillaume Martin-Blondel, Jérémie Pariente, Thomas Geeraerts ; Louis Pasteur Hospital (Colmar) : Hélène Oesterlé, Federico Bolognini, Julien Messie ; Sainte-Anne Hospital (Paris) : Ghazi Hmeydia, Joseph Benzakoun, Catherine Oppenheim ; Amiens University Hospital (Amiens) : Jean-Marc Constans, Serge Metanbou, Adrien Heintz ; Henri-Mondor University Hospital (Créteil) : Blanche Bapst, Imen Megdiche ; CHIC Unisanté (Forbach) : Lavinia Jager, Patrick Nesser, Yannick Talla Mba ; Bordeaux University Hospital (Bordeaux) : Thomas Tourdias, Juliette Coutureau ; Emile Muller Hospital (Mulhouse) : Céline Hemmert, Philippe Feuerstein, Nathan Sebag ; Hospital of Haguenau (Haguenau) : Sophie Carre, Manel Alleg, Claire Lecocq ; Nancy University Hospital (Nancy) : Emmanuel Schmitt, René Anxionnat, François Zhu ; Limoges University Hospital (Limoges) : Géraud Forestier, Aymeric Rouchaud ; Dijon University Hospital (Dijon) : Pierre-Olivier Comby, Frederic Ricolfi, Pierre Thouant ; Grenoble Alpes University Hospital (Grenoble) : Sylvie Grand, Alexandre Krainik ; Antony Private Hospital (Antony) : Isaure de Beaurepaire, Grégoire Bornet ; Hospices Civils de Lyon (Lyon) : Audrey Lacalm, Patrick Miailhes, Julie Pique ; Saint-Etienne University Hospital (Saint-Etienne) : Claire Boutet, Xavier Fabre ; Clermont-Ferrand University Hospital (Clermont-Ferrand) : Béatrice Claise, Sonia Mirafzal, Laure Calvet ; French Neuroradiological Society (SFNR) board : Hubert Desal, Jérome Berge, Grégoire Boulouis, Apolline Kazemi, Nadya Pyatigorskaya, Augustin Lecler, Suzana Saleme, Myriam Edjlali-Goujon, Basile Kerleroux, Jean-Christophe Brisset ; UCIEC : Samir Chenaf
Fabrice Bonneville z, Gilles Adam z, Guillaume Martin-Blondel z, Jérémie Pariente z, Thomas Geeraerts z, Hélène Oesterlé aa, Federico Bolognini aa, Julien Messie aa, Ghazi Hmeydia ab, Joseph Benzakoun ab, Catherine Oppenheim ab, Jean-Marc Constans ac, Serge Metanbou ac, Adrien Heintz ac, Blanche Bapst ad, Imen Megdiche ad, Lavinia Jager ae, Patrick Nesser ae, Yannick Talla Mba ae, Thomas Tourdias af, Juliette Coutureau af, Céline Hemmert ag, Philippe Feuerstein ag, Nathan Sebag ag, Sophie Carre ah, Manel Alleg ah, Claire Lecocq ah, Emmanuel Schmitt ai, René Anxionnat ai, François Zhu ai, Géraud Forestier aj, Aymeric Rouchaud aj, Pierre-Olivier Comby ak, Frederic Ricolfi ak, Pierre Thouant ak, Sylvie Grand al, Alexandre Krainik al, Isaure de Beaurepaire am, Grégoire Bornet am, Audrey Lacalm an, Patrick Miailhes an, Julie Pique an, Claire Boutet ao, Xavier Fabre ao, Béatrice Claise ap, Sonia Mirafzal ap, Laure Calvet ap, Hubert Desal aq, Jérome Berge aq, Grégoire Boulouis aq, Apolline Kazemi aq, Nadya Pyatigorskaya aq, Augustin Lecler aq, Suzana Saleme aq, Myriam Edjlali-Goujon aq, Basile Kerleroux aq, Jean-Christophe Brisset aq, Samir Chenaf ar
z Toulouse University Hospital, Toulouse, France
aa Louis Pasteur Hospital, Colmar, France
ab Sainte-Anne Hospital, Paris, France
ac Amiens University Hospital, Amiens, France
ad Henri-Mondor University Hospital, Créteil, France
ae CHIC Unisanté, Forbach, France
af Bordeaux University Hospital, Bordeaux, France
ag Emile Muller Hospital, Mulhouse, France
ah Hospital of Haguenau, Haguenau, France
ai Nancy University Hospital, Nancy, France
aj Limoges University Hospital, Limoges, France
ak Dijon University Hospital, Dijon, France
al Grenoble Alpes University Hospital, Grenoble, France
am Antony Private Hospital, Antony, France
an Hospices Civils de Lyon, Lyon, France
ao Saint-Etienne University Hospital, Saint-Etienne, France
ap Clermont-Ferrand University Hospital, Clermont-Ferrand, France
aq French Neuroradiological Society (SFNR) Board, France
ar UCIEC, France
a Service D'imagerie 2, Hôpital de Hautepierre, Hôpitaux Universitaires de Strasbourg, Strasbourg, France
b Department of Medical Physics and Biomedical Engineering, University College London Hospitals NHS Foundation Trust, 235 Euston Road, London NW1 2BU, United Kingdom
c Engineering science, computer science and imaging laboratory (ICube), Integrative Multimodal Imaging in Healthcare, UMR 7357, University of Strasbourg-CNRS, Strasbourg, France
d Service d'Anesthésie-Réanimation, Nouvel Hôpital Civil, Hôpitaux universitaires de Strasbourg, Strasbourg, France
e Department of Neuroradiology, CHU Rennes, Rennes, France
f Medical Intensive Care Unit, CHU Rennes, Rennes, France
g Service de Médecine Intensive Réanimation, Nouvel Hôpital Civil, Hôpitaux Universitaires de Strasbourg, Strasbourg, France
h Immuno-Rhumatologie Moléculaire, INSERM UMR S1109, LabEx TRANSPLANTEX, Centre de Recherche d'Immunologie et d'Hématologie, Faculté de Médecine, Fédération Hospitalo-Universitaire (FHU) OMICARE, Fédération de Médecine Translationnelle de Strasbourg (FMTS), Université de Strasbourg (UNISTRA), Strasbourg, France
i Service de Médecine Intensive Réanimation, Hôpitaux universitaires de Strasbourg, Hautepierre, Strasbourg, France
j Department of Radiology, Assistance Publique–Hôpitaux de Paris (APHP), Denis Diderot University and Medical School, Bichat University Hospital, Paris, France
k Neuroradiology Unit, Department of Radiology, Assistance Publique-Hôpitaux de Paris (APHP), Bichat University Hospital, Paris, France
l Nephrology and Transplantation department, Hôpitaux Universitaires de Strasbourg. Inserm UMR S1109, LabEx Transplantex, Fédération de Médecine Translationnelle de Strasbourg (FMTS), Université de Strasbourg, Strasbourg, France
m Hôpital de Hautepierre, Service d'Anesthésie, Réanimation & Médecine Péri-Opératoire - Université de Strasbourg, Faculté de Médecine, FMTS, EA3072, Hôpitaux Universitaires de Strasbourg, Strasbourg, France
n Service de Maladies Infectieuses, NHC, CHU de Strasbourg, Strasbourg, France
o Hôpitaux Universitaires de Strasbourg, UCIEC, Pôle d'Imagerie, Strasbourg, France
p Brisset-Li Consulting, Valbonne-Sophia-Antipolis, France
q Service de Neurologie, Hôpitaux Universitaires de Strasbourg, Strasbourg, France
r Laboratoire de Virologie Médicale, Hôpitaux Universitaires de Strasbourg, Strasbourg, France
s Radiology Department, Nouvel Hôpital Civil, Strasbourg University Hospital, Strasbourg, France
t UMR 1260, Regenerative Nanomedicine (RNM), FMTS, INSERM (French National Institute of Health and Medical Research), Strasbourg, France
u Service de Santé Publique, GMRC, CHU de Strasbourg, Strasbourg F-67091 , France
v Neuroradiological Academic Unit, Department of Brain Repair and Rehabilitation, UCL Queen Square Institute of Neurology, Queen Square, London WC1N 3BG, United Kingdom
w INSERM-U964/CNRS-UMR7104/Université de Strasbourg, Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), Illkirch, France
x MRI center, Centre Hospitalier Lyon Sud, Hospices Civils de Lyon, Lyon, France
y CREATIS-LRMN, CNRS/UMR/5220-INSERM U630, Université Lyon 1, Villeurbanne, France
⁎Corresponding author at: Service D'imagerie 2, Hôpital de Hautepierre, Hôpitaux Universitaires de Strasbourg, Strasbourg, France.Service D'imagerie 2Hôpital de HautepierreHôpitaux Universitaires de StrasbourgStrasbourgFrance
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Highlights |
• | In a multicentric cohort of 59 patients suffering from severe COVID-19, ASL perfusion was abnormal in 53, hypoperfusion occurred in 48 (with a predominant fronto-temporo-polar pattern), whereas hyperperfusion occurred in 9. |
• | Post-contrast FLAIR leptomeningeal enhancement was the only parameter with a significant association with cerebral perfusion, as it was tightly linked to hyperperfusion. |
• | Frontotemporal hypoperfusion was also found in quantitative subgroup analysis compared to healthy subjects. |
Abstract |
Background and purpose |
Cerebral hypoperfusion has been reported in patients with COVID-19 and neurological manifestations in small cohorts. We aimed to systematically assess changes in cerebral perfusion in a cohort of 59 of these patients, with or without abnormalities on morphological MRI sequences.
Methods |
Patients with biologically-confirmed COVID-19 and neurological manifestations undergoing a brain MRI with technically adequate arterial spin labeling (ASL) perfusion were included in this retrospective multicenter study. ASL maps were jointly reviewed by two readers blinded to clinical data. They assessed abnormal perfusion in four regions of interest in each brain hemisphere: frontal lobe, parietal lobe, posterior temporal lobe, and temporal pole extended to the amygdalo-hippocampal complex.
Results |
Fifty-nine patients (44 men (75%), mean age 61.2 years) were included. Most patients had a severe COVID-19, 57 (97%) needed oxygen therapy and 43 (73%) were hospitalized in intensive care unit at the time of MRI. Morphological brain MRI was abnormal in 44 (75%) patients. ASL perfusion was abnormal in 53 (90%) patients, and particularly in all patients with normal morphological MRI. Hypoperfusion occurred in 48 (81%) patients, mostly in temporal poles (52 (44%)) and frontal lobes (40 (34%)). Hyperperfusion occurred in 9 (15%) patients and was closely associated with post-contrast FLAIR leptomeningeal enhancement (100% [66.4%-100%] of hyperperfusion with enhancement versus 28.6% [16.6%-43.2%] without, p = 0.002). Studied clinical parameters (especially sedation) and other morphological MRI anomalies had no significant impact on perfusion anomalies.
Conclusion |
Brain ASL perfusion showed hypoperfusion in more than 80% of patients with severe COVID-19, with or without visible lesion on conventional MRI abnormalities.
Le texte complet de cet article est disponible en PDF.Keywords : COVID-19, Neuroimaging, Magnetic resonance imaging, Cerebrovascular circulation, Multicenter study
Abbreviations : COVID-19, SARS-CoV-2, ICU, ASL, CBF, RT-PCR, EEG, PaO2, FiO2
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© 2023
Elsevier Masson SAS. Tous droits réservés.
Vol 50 - N° 5
P. 470-481 - septembre 2023 Retour au numéro
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