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      Brain MRI Findings in Severe COVID-19: A Retrospective Observational Study

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      , MD * , , , MD * , , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , PhD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , MD, , PhD, , , MD, , MD, , MD, , PhD, , MD, , MD, , MD, , MD, , MD, , PharmD, , MD, , MD, , MD, , MD, , MD, , MD
      Radiology
      Radiological Society of North America

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          Abstract

          Background

          Brain MRI parenchymal signal abnormalities have been in association with SARS-CoV-2.

          Purpose

          Describe the neuroimaging findings (excluding ischemic infarcts) in patients with severe COVID-19 infection.

          Methods

          This was a retrospective study of patients evaluated from March 23th, 2020 to April 27th, 2020 at 16 hospitals. Inclusion criteria were: (i) positive nasopharyngeal or lower respiratory tract reverse transcriptase-polymerase chain reaction assays; (ii) severe COVID infection defined as requirement for hospitalization and oxygen therapy; (iii) neurologic manifestations; (iv) abnormal brain MRI. Exclusion criteria were patients with missing or non-contributory data regarding brain MRI or a brain MRI showing ischemic infarcts, cerebral venous thrombosis, or chronic lesions unrelated to the current event. Categorical data were compared using Fisher exact test. Quantitative data were compared using Student’s t-test or Wilcoxon test. A p-value lower than 0.05 was considered significant.

          Results

          Thirty men (81%) and 7 women (19%) met inclusion criteria, with a mean age of 61+/- 12 years (range: 8-78). The most common neurologic manifestations were alteration of consciousness (27/37, 73%), pathological wakefulness when the sedation was stopped (15/37, 41%), confusion (12/37, 32%), and agitation (7/37, 19%). The most frequent MRI findings were: signal abnormalities located in the medial temporal lobe in 16/37 (43%, 95% CI 27-59%) patients, non-confluent multifocal white matter hyperintense lesions on FLAIR and diffusion sequences, with variable enhancement, with associated hemorrhagic lesions in 11/37 patients (30%, 95% CI 15-45%), and extensive and isolated white matter microhemorrhages in 9/37 patients (24%, 95% CI 10-38%). A majority of patients (20/37, 54%) had intracerebral hemorrhagic lesions with a more severe clinical presentation: higher admission rate in intensive care units, 20/20 patients, 100% versus 12/17 patients, 71%, p=0.01; development of the acute respiratory distress syndrome in 20/20 patients, 100% versus 11/17 patients, 65%, p=0.005. Only one patient was positive for SARS-CoV-2 RNA in the cerebrospinal fluid.

          Conclusion

          Patients with severe COVID-19 and without ischemic infarcts had a wide range of neurologic manifestations that were be associated with abnormal brain MRIs. Eight distinctive neuroradiological patterns were described.

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          Most cited references19

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          A Novel Coronavirus from Patients with Pneumonia in China, 2019

          Summary In December 2019, a cluster of patients with pneumonia of unknown cause was linked to a seafood wholesale market in Wuhan, China. A previously unknown betacoronavirus was discovered through the use of unbiased sequencing in samples from patients with pneumonia. Human airway epithelial cells were used to isolate a novel coronavirus, named 2019-nCoV, which formed a clade within the subgenus sarbecovirus, Orthocoronavirinae subfamily. Different from both MERS-CoV and SARS-CoV, 2019-nCoV is the seventh member of the family of coronaviruses that infect humans. Enhanced surveillance and further investigation are ongoing. (Funded by the National Key Research and Development Program of China and the National Major Project for Control and Prevention of Infectious Disease in China.)
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            COVID-19–associated Acute Hemorrhagic Necrotizing Encephalopathy: CT and MRI Features

            Since its introduction to the human population in December 2019, the coronavirus disease 2019 (COVID-19) pandemic has spread across the world with over 330,000 reported cases in 190 countries (1). While patients typically present with fever, shortness of breath, and cough, neurologic manifestations have been reported, although to a much lesser extent (2). We report the first presumptive case of COVID-19–associated acute necrotizing hemorrhagic encephalopathy, a rare encephalopathy that has been associated with other viral infections but has yet to be demonstrated as a result of COVID-19 infection. A female airline worker in her late fifties presented with a 3-day history of cough, fever, and altered mental status. Initial laboratory work-up was negative for influenza, with the diagnosis of COVID-19 made by detection of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) viral nucleic acid in a nasopharyngeal swab specimen using the U.S. Centers for Disease Control and Prevention (CDC) 2019-Novel Coronavirus (2019-nCoV) Real-Time Reverse Transcriptase-Polymerase Chain Reaction assay. The assay was performed on a Roche thermocycler at our institution following “emergency use authorization” from the CDC. Cerebrospinal fluid (CSF) analysis was limited due to a traumatic lumbar puncture. However, CSF bacterial culture showed no growth after 3 days, and tests for herpes simplex virus 1 and 2, varicella zoster virus, and West Nile virus were negative. Testing for the presence of SARS-CoV-2 in the CSF was unable to be performed. Noncontrast head CT images demonstrated symmetric hypoattenuation within the bilateral medial thalami with a normal CT angiogram and CT venogram (Fig 1). Images from brain MRI demonstrated hemorrhagic rim enhancing lesions within the bilateral thalami, medial temporal lobes, and subinsular regions (Fig 2). The patient was started on intravenous immunoglobulin. High-dose steroids were not initiated due to concern for respiratory compromise. Figure 1a: A, Image from noncontrast head CT demonstrates symmetric hypoattenuation within the bilateral medial thalami (arrows). B, Axial CT venogram demonstrates patency of the cerebral venous vasculature, including the internal cerebral veins (arrows). C, Coronal reformat of aCT angiogram demonstrates normal appearance of the basilar artery and proximal posterior cerebral arteries. Figure 1b: A, Image from noncontrast head CT demonstrates symmetric hypoattenuation within the bilateral medial thalami (arrows). B, Axial CT venogram demonstrates patency of the cerebral venous vasculature, including the internal cerebral veins (arrows). C, Coronal reformat of aCT angiogram demonstrates normal appearance of the basilar artery and proximal posterior cerebral arteries. Figure 1c: A, Image from noncontrast head CT demonstrates symmetric hypoattenuation within the bilateral medial thalami (arrows). B, Axial CT venogram demonstrates patency of the cerebral venous vasculature, including the internal cerebral veins (arrows). C, Coronal reformat of aCT angiogram demonstrates normal appearance of the basilar artery and proximal posterior cerebral arteries. Figure 2a: MRI images demonstrate T2 FLAIR hyperintensity within the bilateral medial temporal lobes and thalami (A, B, E, F) with evidence of hemorrhage indicated by hypointense signal intensity on susceptibility-weighted images (C, G) and rim enhancement on postcontrast images (D, H). Figure 2b: MRI images demonstrate T2 FLAIR hyperintensity within the bilateral medial temporal lobes and thalami (A, B, E, F) with evidence of hemorrhage indicated by hypointense signal intensity on susceptibility-weighted images (C, G) and rim enhancement on postcontrast images (D, H). Figure 2c: MRI images demonstrate T2 FLAIR hyperintensity within the bilateral medial temporal lobes and thalami (A, B, E, F) with evidence of hemorrhage indicated by hypointense signal intensity on susceptibility-weighted images (C, G) and rim enhancement on postcontrast images (D, H). Figure 2d: MRI images demonstrate T2 FLAIR hyperintensity within the bilateral medial temporal lobes and thalami (A, B, E, F) with evidence of hemorrhage indicated by hypointense signal intensity on susceptibility-weighted images (C, G) and rim enhancement on postcontrast images (D, H). Figure 2e: MRI images demonstrate T2 FLAIR hyperintensity within the bilateral medial temporal lobes and thalami (A, B, E, F) with evidence of hemorrhage indicated by hypointense signal intensity on susceptibility-weighted images (C, G) and rim enhancement on postcontrast images (D, H). Figure 2f: MRI images demonstrate T2 FLAIR hyperintensity within the bilateral medial temporal lobes and thalami (A, B, E, F) with evidence of hemorrhage indicated by hypointense signal intensity on susceptibility-weighted images (C, G) and rim enhancement on postcontrast images (D, H). Figure 2g: MRI images demonstrate T2 FLAIR hyperintensity within the bilateral medial temporal lobes and thalami (A, B, E, F) with evidence of hemorrhage indicated by hypointense signal intensity on susceptibility-weighted images (C, G) and rim enhancement on postcontrast images (D, H). Figure 2h: MRI images demonstrate T2 FLAIR hyperintensity within the bilateral medial temporal lobes and thalami (A, B, E, F) with evidence of hemorrhage indicated by hypointense signal intensity on susceptibility-weighted images (C, G) and rim enhancement on postcontrast images (D, H). Acute necrotizing encephalopathy (ANE) is a rare complication of influenza and other viral infections and has been related to intracranial cytokine storms, which result in blood-brain-barrier breakdown, but without direct viral invasion or parainfectious demyelination (3). Accumulating evidence suggests that a subgroup of patients with severe COVID-19 might have a cytokine storm syndrome (4). While predominantly described in the pediatric population, ANE is known to occur in adults as well. The most characteristic imaging feature includes symmetric, multifocal lesions with invariable thalamic involvement (5). Other commonly involved locations include the brain stem, cerebral white matter, and cerebellum (5). Lesions appear hypoattenuating on CT images and MRI demonstrates T2 FLAIR hyperintense signal with internal hemorrhage. Postcontrast images may demonstrate a ring of contrast enhancement (5). This is the first reported case of COVID-19–associated acute necrotizing hemorrhagic encephalopathy. As the number of patients with COVID-19 increases worldwide, clinicians and radiologists should be watching for this presentation among patients presenting with COVID-19 and altered mental status.
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              Brain MRI Findings in Patients in the Intensive Care Unit with COVID-19 Infection

              Online supplemental material is available for this article.
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                Author and article information

                Contributors
                Journal
                Radiology
                Radiology
                Radiology
                Radiology
                Radiological Society of North America
                0033-8419
                1527-1315
                16 June 2020
                : 202222
                Affiliations
                [1]Hôpitaux Universitaires de Strasbourg, Service d’imagerie 2, Hôpital de Hautepierre, Strasbourg, France (S.K., F.L., S.B., F.D.A., T.W.); Engineering science, computer science and imaging laboratory (ICube), Integrative Multimodal Imaging in Healthcare, UMR 7357, University of Strasbourg-CNRS, Strasbourg, France (S.K.,); Service de Neurologie, Hôpitaux Universitaires de Strasbourg, Strasbourg, France (J.S., C.B., V.M., M.A.); CHU Rennes, Department of Neuroradiology, Rennes, France (J.C.F., B.C.N.); Service de maladies infectieuses et réanimation médicale. CHU Rennes, France (A.M.); Hôpitaux universitaires de Strasbourg, Service d’Anesthésie-Réanimation, Nouvel Hôpital Civil, Strasbourg, France (O.C., P.M.M.); Service de Neuroradiologie, CHU Toulouse, Toulouse, France (F.B., G.A.); Department of infectious and tropical diseases, Toulouse University Hospital, Toulouse, France (G.M.B.); Department of Neurology, Toulouse University Hospital, Toulouse, France (M.R.); Department of Anesthesia and Critical Care, Toulouse University Hospital University Toulouse 3-Paul Sabatier, Toulouse, France (T.G., L.D.); Service de neuroradiologie diagnostique et interventionnelle, Centre Hospitalier Universitaire des Alpes, Grenoble, France (S.G., A.K.); 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 (S.C.); EA CHIMERE 7516, Université de Picardie Jules Verne, Amiens, France; Service de NeuroRadiologie, pôle Imagerie Médicale, Centre Hospitalo-Universitaire d'Amiens, Amiens, France (J.M.C., A.H.); Service de Neuro Radiologie, pôle Imagerie Médicale, Centre Hospitalo-Universitaire d'Amiens, Amiens, France (S.M.); Hôpitaux universitaires de Strasbourg, Service de Médecine Intensive Réanimation, Nouvel Hôpital Civil, Strasbourg, France (J.H., F.M.); 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 (J.H.); Hôpitaux universitaires de Strasbourg, Service de Médecine Intensive Réanimation, Hautepierre, Strasbourg, France (M.S., F.C.); Service de Maladies infectieuses, NHC, CHU de Strasbourg, Strasbourg, France (N.L., Y.H.); Service de Radiologie, CHU de Saint-Etienne, Saint-Etienne, France (C.B.); Service de Réanimation, CH de Roanne, Roanne, France (X.F.); University Hospital of Limoges, Neuroradiology Department, Limoges, France (G.F., S.S.); Radiology Department, Hôpital Privé d’Antony, Antony, France (I.B., G.B.); Service d’imagerie Pédiatrique et Fœtale, Hôpital Femme Mère Enfant, HCL, Lyon, France (A.L.); Service de Neuroradiologie, Hôpitaux Civils de Colmar, Colmar, France (H.O., F.B., J.M.); INSERM U1266, Service d’imagerie morphologique et fonctionnelle, GHU Psychiatrie et Neurosciences, site Sainte-Anne, Paris, France (G.H., J.B., C.O., G.B., M.E.G., B.K.); service de Neuroradiologie, CHU Henri Mondor, Créteil, France (B.B., I.M.); Neuroradiology Unit, Department of Radiology, Assistance Publique–Hôpitaux de Paris (APHP), Bichat University Hospital, Paris, France (M.H.F., A.G.); Department of Radiology, Assistance Publique–Hôpitaux de Paris (APHP), Denis Diderot University and Medical School, Bichat University Hospital, Paris, France (A.K.); CHIC Unisanté, Hôpital Marie Madeleine, Forbach, France (L.J., P.N., Y.T.M.); service de Radiologie 1, GHR Mulhouse Sud Alsace, Hôpital Mère Enfants, Mulhouse, France (C.H., P.F., N.S.); Service de Neurologie, Centre Hospitalier de Haguenau, Haguenau, France (S.C., C.L.); Service de Radiologie, Centre Hospitalier de Haguenau, Haguenau, France (M.A.); Service de Neuroradiologie, Hôpital Central, CHU de Nancy, Nancy, France (E.S., R.A., F.Z.); Department of Neuroradiology, University Hospital of Dijon, Hôpital François Mitterrand, Dijon, France (P.C., F.R., P.T.); Department of Diagnostic and Interventional Neuroradiology, University Hospital, Nantes, France (H.D.); Neuroradiology department - CHU de Bordeaux, Bordeaux, France (J.B.); Service de Neuroradiologie, CHU de Lille, Lille, France (A.K.); Assistance Publique Hôpitaux de Paris, Service de Neuroradiologie, Hôpital Pitié-Salpêtrière, Paris, France Sorbonne Université, Univ Paris 06, UMR S 1127, CNRS UMR 7225, ICM, F-75013, Paris, France (N.P.); Neuroradiology department, Fondation A.Rothschild Hospital, Paris, France (A.L.); Hôpitaux Universitaires de Strasbourg, UCIEC, Pôle d’Imagerie, Strasbourg, France (P.E.Z., M.M.); Observatoire Français de la Sclérose en Plaques, Lyon, France (J.C.B.); Hôpitaux universitaires de Strasbourg, Laboratoire de Virologie Médicale, Strasbourg, France (S.F.K.); Radiology Department, Nouvel Hôpital Civil, Strasbourg University Hospital, Strasbourg, France (M.O.); INSERM (French National Institute of Health and Medical Research), UMR 1260, Regenerative Nanomedicine (RNM), FMTS, Strasbourg, France (F.M.); Department of Anaesthesia and Intensive Care, Lyon-Sud Hospital, Hospices Civils de Lyon, F-69495 Pierre Benite; University Claude Bernard Lyon 1, Lyon, France (J.S.D.); CHU de Strasbourg, Service de Santé Publique, GMRC, F-67091 Strasbourg, France (N.M.); Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), INSERM-U964/CNRSUMR7104/Université de Strasbourg, Illkirch, France (M.A.); MRI center, Centre Hospitalier Lyon Sud, Hospices Civils de Lyon, Lyon, France (F.C.); Université Lyon 1, CREATIS-LRMN, CNRS/UMR/5220-INSERM U630, Villeurbanne, France (F.C.).
                Author notes
                Corresponding author: S.K (email: stephane.kremer@ 123456chru-strasbourg.fr )

                Contributions: SK, FC, FL, JDS, and MA were responsible for the conception of the study. SK, FC, FL, JDS and MA collected the epidemiological, clinical, laboratory, and radiological data, and had full access to all data in the study and take responsibility for the accuracy of the data analysis. NM contributed to the statistical analysis. SK, FC, FL, JDS, and MA contributed to the writing and revision of the present report.

                All other authors contributed to the acquisition, analysis, or interpretation of data, and revised and approved the final manuscript.

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                Article
                202222
                10.1148/radiol.2020202222
                7301613
                32544034
                d4963e9b-6ae0-4bbf-823d-090b3dc6de67
                2020 by the Radiological Society of North America, Inc.

                This article is made available via the PMC Open Access Subset for unrestricted re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for the duration of the COVID-19 pandemic or until permissions are revoked in writing. Upon expiration of these permissions, PMC is granted a perpetual license to make this article available via PMC and Europe PMC, consistent with existing copyright protections.

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