Cerebral perfusion using ASL in patients with COVID-19 and neurological manifestations: A retrospective multicenter observational study.
Journal of Neuroradiology. 2023-09-01; 50(5): 470-481
DOI: 10.1016/j.neurad.2023.01.005
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1. J Neuroradiol. 2023 Sep;50(5):470-481. doi: 10.1016/j.neurad.2023.01.005. Epub
2023 Jan 16.
Cerebral perfusion using ASL in patients with COVID-19 and neurological
manifestations: A retrospective multicenter observational study.
Ardellier FD(1), Baloglu S(2), Sokolska M(3), Noblet V(4), Lersy F(2), Collange
O(5), Ferré JC(6), Maamar A(7), Carsin-Nicol B(6), Helms J(8), Schenck M(9),
Khalil A(10), Gaudemer A(11), Caillard S(12), Pottecher J(13), Lefèbvre N(14),
Zorn PE(15), Matthieu M(15), Brisset JC(16), Boulay C(17), Mutschler V(17),
Hansmann Y(14), Mertes PM(5), Schneider F(9), Fafi-Kremer S(18), Ohana M(19),
Meziani F(20), Meyer N(21), Yousry T(22), Anheim M(23), Cotton F(24), Jäger
HR(22), Kremer S(25); SFNR-COVID group.
Collaborators: Bonneville F(26), Adam G(26), Martin-Blondel G(26), Pariente
J(26), Geeraerts T(26), Oesterlé H(27), Bolognini F(27), Messie J(27), Hmeydia
G(28), Benzakoun J(28), Oppenheim C(28), Constans JM(29), Metanbou S(29), Heintz
A(29), Bapst B(30), Megdiche I(30), Jager L(31), Nesser P(31), Mba YT(31),
Tourdias T(32), Coutureau J(32), Hemmert C(33), Feuerstein P(33), Sebag N(33),
Carre S(34), Alleg M(34), Lecocq C(34), Schmitt E(35), Anxionnat R(35), Zhu
F(35), Forestier G(36), Rouchaud A(36), Comby PO(37), Ricolfi F(37), Thouant
P(37), Grand S(38), Krainik A(38), de Beaurepaire I(39), Bornet G(39), Lacalm
A(40), Miailhes P(40), Pique J(40), Boutet C(41), Fabre X(41), Claise B(42),
Mirafzal S(42), Calvet L(42), Desal H(43), Berge J(43), Boulouis G(43), Kazemi
A(43), Pyatigorskaya N(43), Lecler A(43), Saleme S(43), Edjlali-Goujon M(43),
Kerleroux B(43), Brisset JC(43), Chenaf S(44).
Author information:
(1)Service D’imagerie 2, Hôpital de Hautepierre, Hôpitaux Universitaires de
Strasbourg, Strasbourg, France; Engineering science, computer science and
imaging laboratory (ICube), Integrative Multimodal Imaging in Healthcare, UMR
7357, University of Strasbourg-CNRS, Strasbourg, France. Electronic address:
.
(2)Service D’imagerie 2, Hôpital de Hautepierre, Hôpitaux Universitaires de
Strasbourg, Strasbourg, France.
(3)Department of Medical Physics and Biomedical Engineering, University College
London Hospitals NHS Foundation Trust, 235 Euston Road, London NW1 2BU, United
Kingdom; Neuroradiological Academic Unit, Department of Brain Repair and
Rehabilitation, UCL Queen Square Institute of Neurology, Queen Square, London
WC1N 3BG, United Kingdom.
(4)Engineering science, computer science and imaging laboratory (ICube),
Integrative Multimodal Imaging in Healthcare, UMR 7357, University of
Strasbourg-CNRS, Strasbourg, France.
(5)Service d’Anesthésie-Réanimation, Nouvel Hôpital Civil, Hôpitaux
universitaires de Strasbourg, Strasbourg, France.
(6)Department of Neuroradiology, CHU Rennes, Rennes, France.
(7)Medical Intensive Care Unit, CHU Rennes, Rennes, France.
(8)Service de Médecine Intensive Réanimation, Nouvel Hôpital Civil, Hôpitaux
Universitaires de Strasbourg, Strasbourg, France; 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.
(9)Service de Médecine Intensive Réanimation, Hôpitaux universitaires de
Strasbourg, Hautepierre, Strasbourg, France.
(10)Department of Radiology, Assistance Publique-Hôpitaux de Paris (APHP), Denis
Diderot University and Medical School, Bichat University Hospital, Paris,
France.
(11)Neuroradiology Unit, Department of Radiology, Assistance Publique-Hôpitaux
de Paris (APHP), Bichat University Hospital, Paris, France.
(12)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; 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.
(13)Hôpital de Hautepierre, Service d’Anesthésie, Réanimation & Médecine
Péri-Opératoire – Université de Strasbourg, Faculté de Médecine, FMTS, EA3072,
Hôpitaux Universitaires de Strasbourg, Strasbourg, France.
(14)Service de Maladies Infectieuses, NHC, CHU de Strasbourg, Strasbourg,
France.
(15)Hôpitaux Universitaires de Strasbourg, UCIEC, Pôle d’Imagerie, Strasbourg,
France.
(16)Brisset-Li Consulting, Valbonne-Sophia-Antipolis, France.
(17)Service de Neurologie, Hôpitaux Universitaires de Strasbourg, Strasbourg,
France.
(18)Laboratoire de Virologie Médicale, Hôpitaux Universitaires de Strasbourg,
Strasbourg, France.
(19)Radiology Department, Nouvel Hôpital Civil, Strasbourg University Hospital,
Strasbourg, France.
(20)Service de Médecine Intensive Réanimation, Nouvel Hôpital Civil, Hôpitaux
Universitaires de Strasbourg, Strasbourg, France; UMR 1260, Regenerative
Nanomedicine (RNM), FMTS, INSERM (French National Institute of Health and
Medical Research), Strasbourg, France.
(21)Service de Santé Publique, GMRC, CHU de Strasbourg, Strasbourg F-67091 ,
France.
(22)Neuroradiological Academic Unit, Department of Brain Repair and
Rehabilitation, UCL Queen Square Institute of Neurology, Queen Square, London
WC1N 3BG, United Kingdom.
(23)Service de Neurologie, Hôpitaux Universitaires de Strasbourg, Strasbourg,
France; INSERM-U964/CNRS-UMR7104/Université de Strasbourg, Institut de Génétique
et de Biologie Moléculaire et Cellulaire (IGBMC), Illkirch, France.
(24)MRI center, Centre Hospitalier Lyon Sud, Hospices Civils de Lyon, Lyon,
France; CREATIS-LRMN, CNRS/UMR/5220-INSERM U630, Université Lyon 1,
Villeurbanne, France.
(25)Service D’imagerie 2, Hôpital de Hautepierre, Hôpitaux Universitaires de
Strasbourg, Strasbourg, France; Engineering science, computer science and
imaging laboratory (ICube), Integrative Multimodal Imaging in Healthcare, UMR
7357, University of Strasbourg-CNRS, Strasbourg, France.
(26)Toulouse University Hospital, Toulouse, France.
(27)Louis Pasteur Hospital, Colmar, France.
(28)Sainte-Anne Hospital, Paris, France.
(29)Amiens University Hospital, Amiens, France.
(30)Henri-Mondor University Hospital, Créteil, France.
(31)CHIC Unisanté, Forbach, France.
(32)Bordeaux University Hospital, Bordeaux, France.
(33)Emile Muller Hospital, Mulhouse, France.
(34)Hospital of Haguenau, Haguenau, France.
(35)Nancy University Hospital, Nancy, France.
(36)Limoges University Hospital, Limoges, France.
(37)Dijon University Hospital, Dijon, France.
(38)Grenoble Alpes University Hospital, Grenoble, France.
(39)Antony Private Hospital, Antony, France.
(40)Hospices Civils de Lyon, Lyon, France.
(41)Saint-Etienne University Hospital, Saint-Etienne, France.
(42)Clermont-Ferrand University Hospital, Clermont-Ferrand, France.
(43)French Neuroradiological Society (SFNR) Board, France.
(44)UCIEC, France.
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.
Copyright © 2023 Elsevier Masson SAS. All rights reserved.
DOI: 10.1016/j.neurad.2023.01.005
PMCID: PMC9842391
PMID: 36657613 [Indexed for MEDLINE]
Conflict of interest statement: Declaration of Competing Interest The authors
declare that they have no known competing financial interests or personal
relationships that could have appeared to influence the work reported in this
paper.