Retrospective Observational Study of Brain Magnetic Resonance Imaging Findings in Patients with Acute SARS-CoV-2 Infection and Neurological Manifestations

Chougar, Lydia; Shor, Natalia; Weiss, Nicolas; Galanaud, Damien; Leclercq, Delphine; Mathon, Bertrand; Belkacem, Samia; Ströer, Sebastian; Burrel, Sonia; Boutolleau, David; Demoule, Alexandre; Rosso, Charlotte; Delorme, Cécile; Seilhean, Danielle; Dormont, Didier; Morawiec, Elise; Raux, Mathieu; Demeret, Sophie; Gerber, Sophie; Trunet, Stéphanie; Similowski, Thomas; Degos, Vincent; Rufat, Pierre; Corvol, Jean-Christophe; Lehéricy, Stéphane; Pyatigorskaya, Nadya

doi:10.1148/radiol.2020202422

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Retrospective Observational Study of Brain Magnetic Resonance Imaging Findings in Patients with Acute SARS-CoV-2 Infection and Neurological Manifestations

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Author(s): Lydia Chougar , MD , Natalia Shor , MD, Nicolas Weiss , MD, PhD, Damien Galanaud , MD, PhD, Delphine Leclercq , MD, Bertrand Mathon , MD, Samia Belkacem , MD, Sebastian Stroër , MD, Sonia Burrel , MD, PhD, David Boutolleau , MD, PhD, Alexandre Demoule , MD, PhD, Charlotte Rosso , MD, PhD, Cécile Delorme , MD, Danielle Seilhean , MD, PhD, Didier Dormont , MD, PhD, Elise Morawiec , MD, Mathieu Raux , MD, PhD, Sophie Demeret , MD, Sophie Gerber , MD, Stéphanie Trunet , MD, Thomas Similowski , MD, PhD, Vincent Degos , MD, PhD, Pierre Rufat , MD, PhD, Jean-Christophe Corvol , MD, PhD, Stéphane Lehéricy , MD, PhD, Nadya Pyatigorskaya , MD, PhD, On behalf of the CoCo Neurosciences study group

Publication date (Electronic): 17 July 2020

Journal: Radiology

Publisher: Radiological Society of North America

Keywords: COVID-19, SARS-CoV-2, neurological manifestations, brain MRI, imaging patterns

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Abstract

Background

This study provides a detailed imaging assessment in a large series of COVID-19 patients with neurological manifestations.

Purpose

To review the MRI findings associated with acute neurological manifestations in COVID-19 patients.

Methods

This was a cross-sectional study conducted between March 23 and May 7, 2020 at the Pitié-Salpêtrière University Hospital, a reference center for COVID-19 in the Paris area. Inclusion criteria were: adult patients diagnosed with SARS-CoV-2 infection, presenting with acute neurological manifestations and referred for a brain MRI examination. Patients were excluded if they had a previous history of neurological disease. The characteristics and the frequency of different MRI features were investigated. The findings were analyzed separately in patients in intensive care units (ICU) and other departments (non-ICU).

Results

During the inclusion period, 1176 consecutive patients were hospitalized for suspected COVID-19. Out of 308 patients with acute neurological symptoms, 73 patients met the inclusion criteria (23.7%) and were included: 35 ICU patients (47.9%) and 38 non-ICU patients (52.1%). The mean age was 58.5 ± 15.6 years, with a male predominance (65.8% vs. 34.2%). Forty-three patients presented pathological MRI findings 2-4 weeks after symptom onset (58.9%), including 17 with acute ischemic infarct (23.3%), 1 with a deep venous thrombosis (1.4%), 8 with multiple microhemorrhages (11.3%), 22 with perfusion abnormalities (47.7%), 3 with restricted diffusion foci within the corpus callosum consistent with cytotoxic lesions of the corpus callosum (CLOCC, 4.1%). Multifocal white matter enhancing lesions were seen in 4 ICU patients (5%). Basal ganglia abnormalities were seen in 4 other patients (5%). The cerebrospinal fluid (CSF) analysis was negative for SARS-CoV-2 in all tested patients (n=39).

Conclusion

In addition to cerebrovascular lesions, perfusion abnormalities, CLOCC and ICU-related complications, we identified two patterns including white matter enhancing lesions and basal ganglia abnormalities that could be related to SARS-CoV-2 infection.

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Most cited references 38

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Endothelial cell infection and endotheliitis in COVID-19

Zsuzsanna Varga, Andreas J. Flammer, Peter Steiger … (2020)

Cardiovascular complications are rapidly emerging as a key threat in coronavirus disease 2019 (COVID-19) in addition to respiratory disease. The mechanisms underlying the disproportionate effect of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection on patients with cardiovascular comorbidities, however, remain incompletely understood.1, 2 SARS-CoV-2 infects the host using the angiotensin converting enzyme 2 (ACE2) receptor, which is expressed in several organs, including the lung, heart, kidney, and intestine. ACE2 receptors are also expressed by endothelial cells. 3 Whether vascular derangements in COVID-19 are due to endothelial cell involvement by the virus is currently unknown. Intriguingly, SARS-CoV-2 can directly infect engineered human blood vessel organoids in vitro. 4 Here we demonstrate endothelial cell involvement across vascular beds of different organs in a series of patients with COVID-19 (further case details are provided in the appendix). Patient 1 was a male renal transplant recipient, aged 71 years, with coronary artery disease and arterial hypertension. The patient's condition deteriorated following COVID-19 diagnosis, and he required mechanical ventilation. Multisystem organ failure occurred, and the patient died on day 8. Post-mortem analysis of the transplanted kidney by electron microscopy revealed viral inclusion structures in endothelial cells (figure A, B ). In histological analyses, we found an accumulation of inflammatory cells associated with endothelium, as well as apoptotic bodies, in the heart, the small bowel (figure C) and lung (figure D). An accumulation of mononuclear cells was found in the lung, and most small lung vessels appeared congested. Figure Pathology of endothelial cell dysfunction in COVID-19 (A, B) Electron microscopy of kidney tissue shows viral inclusion bodies in a peritubular space and viral particles in endothelial cells of the glomerular capillary loops. Aggregates of viral particles (arrow) appear with dense circular surface and lucid centre. The asterisk in panel B marks peritubular space consistent with capillary containing viral particles. The inset in panel B shows the glomerular basement membrane with endothelial cell and a viral particle (arrow; about 150 nm in diameter). (C) Small bowel resection specimen of patient 3, stained with haematoxylin and eosin. Arrows point to dominant mononuclear cell infiltrates within the intima along the lumen of many vessels. The inset of panel C shows an immunohistochemical staining of caspase 3 in small bowel specimens from serial section of tissue described in panel D. Staining patterns were consistent with apoptosis of endothelial cells and mononuclear cells observed in the haematoxylin-eosin-stained sections, indicating that apoptosis is induced in a substantial proportion of these cells. (D) Post-mortem lung specimen stained with haematoxylin and eosin showed thickened lung septa, including a large arterial vessel with mononuclear and neutrophilic infiltration (arrow in upper inset). The lower inset shows an immunohistochemical staining of caspase 3 on the same lung specimen; these staining patterns were consistent with apoptosis of endothelial cells and mononuclear cells observed in the haematoxylin-eosin-stained sections. COVID-19=coronavirus disease 2019. Patient 2 was a woman, aged 58 years, with diabetes, arterial hypertension, and obesity. She developed progressive respiratory failure due to COVID-19 and subsequently developed multi-organ failure and needed renal replacement therapy. On day 16, mesenteric ischaemia prompted removal of necrotic small intestine. Circulatory failure occurred in the setting of right heart failure consequent to an ST-segment elevation myocardial infarction, and cardiac arrest resulted in death. Post-mortem histology revealed lymphocytic endotheliitis in lung, heart, kidney, and liver as well as liver cell necrosis. We found histological evidence of myocardial infarction but no sign of lymphocytic myocarditis. Histology of the small intestine showed endotheliitis (endothelialitis) of the submucosal vessels. Patient 3 was a man, aged 69 years, with hypertension who developed respiratory failure as a result of COVID-19 and required mechanical ventilation. Echocardiography showed reduced left ventricular ejection fraction. Circulatory collapse ensued with mesenteric ischaemia, and small intestine resection was performed, but the patient survived. Histology of the small intestine resection revealed prominent endotheliitis of the submucosal vessels and apoptotic bodies (figure C). We found evidence of direct viral infection of the endothelial cell and diffuse endothelial inflammation. Although the virus uses ACE2 receptor expressed by pneumocytes in the epithelial alveolar lining to infect the host, thereby causing lung injury, the ACE2 receptor is also widely expressed on endothelial cells, which traverse multiple organs. 3 Recruitment of immune cells, either by direct viral infection of the endothelium or immune-mediated, can result in widespread endothelial dysfunction associated with apoptosis (figure D). The vascular endothelium is an active paracrine, endocrine, and autocrine organ that is indispensable for the regulation of vascular tone and the maintenance of vascular homoeostasis. 5 Endothelial dysfunction is a principal determinant of microvascular dysfunction by shifting the vascular equilibrium towards more vasoconstriction with subsequent organ ischaemia, inflammation with associated tissue oedema, and a pro-coagulant state. 6 Our findings show the presence of viral elements within endothelial cells and an accumulation of inflammatory cells, with evidence of endothelial and inflammatory cell death. These findings suggest that SARS-CoV-2 infection facilitates the induction of endotheliitis in several organs as a direct consequence of viral involvement (as noted with presence of viral bodies) and of the host inflammatory response. In addition, induction of apoptosis and pyroptosis might have an important role in endothelial cell injury in patients with COVID-19. COVID-19-endotheliitis could explain the systemic impaired microcirculatory function in different vascular beds and their clinical sequelae in patients with COVID-19. This hypothesis provides a rationale for therapies to stabilise the endothelium while tackling viral replication, particularly with anti-inflammatory anti-cytokine drugs, ACE inhibitors, and statins.7, 8, 9, 10, 11 This strategy could be particularly relevant for vulnerable patients with pre-existing endothelial dysfunction, which is associated with male sex, smoking, hypertension, diabetes, obesity, and established cardiovascular disease, all of which are associated with adverse outcomes in COVID-19.

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Neurologic Manifestations of Hospitalized Patients With Coronavirus Disease 2019 in Wuhan, China

Ling Mao, Huijuan Jin, Mengdie Wang … (2020)

The outbreak of coronavirus disease 2019 (COVID-19) in Wuhan, China, is serious and has the potential to become an epidemic worldwide. Several studies have described typical clinical manifestations including fever, cough, diarrhea, and fatigue. However, to our knowledge, it has not been reported that patients with COVID-19 had any neurologic manifestations.

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High risk of thrombosis in patients with severe SARS-CoV-2 infection: a multicenter prospective cohort study

Julie Helms, Charles Tacquard, François Séverac … (2020)

Little evidence of increased thrombotic risk is available in COVID-19 patients. Our purpose was to assess thrombotic risk in severe forms of SARS-CoV-2 infection.

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Author and article information

Contributors

Lydia Chougar:

ORCID: https://orcid.org/0000-0001-9306-5687

Journal

Journal ID (nlm-ta): Radiology

Journal ID (iso-abbrev): Radiology

Journal ID (publisher-id): Radiology

Title: Radiology

Publisher: Radiological Society of North America

ISSN (Print): 0033-8419

ISSN (Electronic): 1527-1315

Publication date (Electronic): 17 July 2020

Electronic Location Identifier: 202422

Affiliations

[1]Sorbonne Université, Inserm, CNRS, Institut du Cerveau - Paris Brain Institute - ICM, F-75013, Paris, France (L.C., D.G., B.M., C.R., D.D., J.C., S.L., N.P.); Sorbonne Université, 75013, Paris, France (L.C., N.S., N.W., D.G., B.M., S.B., D.B., A.D., C.R., D.S., D.D., E.M., M.R., T.S., V.D., J.C., S.L., N.P.); ICM, “Movement Investigations and Therapeutics” Team (MOV’IT), Paris, France (L.C., S.L., N.P.); ICM, Centre de NeuroImagerie de Recherche – CENIR, Paris, France (L.C., D.G., S.L., N.P.); Assistance Publique Hôpitaux de Paris, Hôpital Pitié-Salpêtrière, Service de neuroradiologie, Paris, France (L.C., N.S., D.G., D.L., S.B., S.S., D.D., S.G., S.T., S.L., N.P.); Brain Liver Pitié-Salpêtrière (BLIPS) Study Group, INSERM UMR_S 938, Centre de recherche Saint-Antoine, Maladies métaboliques, biliaires et fibro-inflammatoire du foie, Institute of Cardiometabolism and Nutrition (ICAN) (N.W., S.D.); Assistance Publique Hôpitaux de Paris, Hôpital Pitié-Salpêtrière, Médecine Intensive Réanimation Neurologique, Paris, France (N.W.); Assistance Publique Hôpitaux de Paris, Hôpital Pitié-Salpêtrière, Service de neurochirurgie, Paris, France (B.M.); Assistance Publique Hôpitaux de Paris, Hôpital Pitié-Salpêtrière, Service de virologie, Centre d’Investigation Clinique Neurosciences, Paris, France (S.B., D.B.); CNR Herpèsvirus (laboratoire associé HSV), SU-INSERM UMR_S 1136 Team 3 THERAVIR IPLESP (S.B., D.B.); Assistance Publique Hôpitaux de Paris, Hôpital Pitié-Salpêtrière, Service de Pneumologie, Médecine Intensive et Réanimation, Paris, France (A.D., E.M., T.S.); Assistance Publique Hôpitaux de Paris, Hôpital Pitié-Salpêtrière, Urgences Cérébro-Vasculaires, Paris, France (C.R.); ICM, stroke network, STAR team, Paris, France (C.R.); Assistance Publique Hôpitaux de Paris, Hôpital Pitié-Salpêtrière, Département de Neurologie, Centre d’Investigation Clinique Neurosciences, Paris, France (C.D., J.C.); Assistance Publique Hôpitaux de Paris, Hôpital Pitié-Salpêtrière, Département de Neuropathologie, Paris, France (D.S.); ICM, INRIA, ARAMIS project-team, Paris, France (D.D., M.R., M.R.); Assistance Publique Hôpitaux de Paris, Hôpital Pitié-Salpêtrière, Department of Anesthesia, Critical Care and Peri-Operative Medicine, Paris, France (M.R., V.D.); Clinical Research Group ARPE, Sorbonne University, Paris, France (V.D.); INSERM UMR 1141, Paris France (V.D.); Assistance Publique Hôpitaux de Paris, DMU ESPRIT, Paris, France(P.R.)

Author notes

Corresponding Author Contact Details: C.L Email: chougar.lydia@ 123456gmail.com

Author information

Lydia Chougar https://orcid.org/0000-0001-9306-5687

Natalia Shor https://orcid.org/0000-0003-0693-1829

Nicolas Weiss https://orcid.org/0000-0001-5155-196X

Damien Galanaud https://orcid.org/0000-0002-9285-8121

Delphine Leclercq https://orcid.org/0000-0003-1110-3833

Bertrand Mathon https://orcid.org/0000-0002-9182-5846

Samia Belkacem https://orcid.org/0000-0002-3634-912X

Sonia Burrel https://orcid.org/0000-0002-7783-2601

David Boutolleau https://orcid.org/0000-0001-9401-4662

Alexandre Demoule https://orcid.org/0000-0002-0432-7217

Charlotte Rosso https://orcid.org/0000-0001-7236-1508

Cécile Delorme https://orcid.org/0000-0002-5838-9077

Danielle Seilhean https://orcid.org/0000-0003-3498-4602

Didier Dormont https://orcid.org/0000-0002-6080-1286

Elise Morawiec https://orcid.org/0000-0002-1323-6819

Mathieu Raux https://orcid.org/0000-0003-2493-9146

Sophie Demeret https://orcid.org/0000-0002-0523-6472

Sophie Gerber https://orcid.org/0000-0002-1901-8126

Stéphanie Trunet https://orcid.org/0000-0003-3825-7699

Thomas Similowski https://orcid.org/0000-0003-2868-9279

Vincent Degos https://orcid.org/0000-0002-6540-5725

Pierre Rufat https://orcid.org/0000-0002-2222-4369

Jean-Christophe Corvol https://orcid.org/0000-0001-7325-0199

Stéphane Lehéricy https://orcid.org/0000-0002-5802-3518

Nadya Pyatigorskaya https://orcid.org/0000-0002-2070-1299

Article

Publisher-manuscript ID: 202422

DOI: 10.1148/radiol.2020202422

PMC ID: 7370354

PubMed ID: 32677875

SO-VID: 1e288654-e70c-41d8-a66d-f977f0e6571e

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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.

Retrospective Observational Study of Brain Magnetic Resonance Imaging Findings in Patients with Acute SARS-CoV-2 Infection and Neurological Manifestations

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Abstract

Background

Purpose

Methods

Results

Conclusion

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Novel Coronavirus Disease COVID-19

Most cited references 38

Endothelial cell infection and endotheliitis in COVID-19

Neurologic Manifestations of Hospitalized Patients With Coronavirus Disease 2019 in Wuhan, China

High risk of thrombosis in patients with severe SARS-CoV-2 infection: a multicenter prospective cohort study

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