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Cerebrovascular disease in patients with COVID-19: neuroimaging, histological and clinical description
Open accessAbstract
Since the appearance of the first case of coronavirus disease 2019 (COVID-19) a pandemic has emerged affecting millions of individuals worldwide. Although the main clinical manifestations are respiratory, an increase in neurological conditions, specifically acute cerebrovascular disease, has been detected. We present cerebrovascular disease case incidence in hospitalized patients with SARS-CoV-2 infection. Patients were confirmed by microbiological/serological testing, or on chest CT semiology. Available data on co-morbidity, laboratory parameters, treatment administered, neuroimaging, neuropathological studies and clinical evolution during hospitalization, measured by the modified Rankin scale, were analysed. A bivariate study was also designed to identify differences between ischaemic and haemorrhagic subtypes. A statistical model of binary logistic regression and sensitivity analysis was designed to study the influence of independent variables over prognosis. In our centre, there were 1683 admissions of patients with COVID-19 over 50 days, of which 23 (1.4%) developed cerebrovascular disease. Within this group of patients, cerebral and chest CT scans were performed in all cases, and MRI in six (26.1%). Histological samples were obtained in 6/23 cases (two brain biopsies, and four arterial thrombi). Seventeen patients were classified as cerebral ischaemia (73.9%, with two arterial dissections), five as intracerebral haemorrhage (21.7%), and one leukoencephalopathy of posterior reversible encephalopathy type. Haemorrhagic patients had higher ferritin levels at the time of stroke (1554.3 versus 519.2, P = 0.004). Ischaemic strokes were unexpectedly frequent in the vertebrobasilar territory (6/17, 35.3%). In the haemorrhagic group, a characteristic radiological pattern was identified showing subarachnoid haemorrhage, parieto-occipital leukoencephalopathy, microbleeds and single or multiple focal haematomas. Brain biopsies performed showed signs of thrombotic microangiopathy and endothelial injury, with no evidence of vasculitis or necrotizing encephalitis. The functional prognosis during the hospital period was unfavourable in 73.9% (17/23 modified Rankin scale 4-6), and age was the main predictive variable (odds ratio = 1.5; 95% confidence interval 1.012-2.225; P = 0.043). Our series shows cerebrovascular disease incidence of 1.4% in patients with COVID-19 with high morbidity and mortality. We describe pathological and radiological data consistent with thrombotic microangiopathy caused by endotheliopathy with a haemorrhagic predisposition.
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“Consistent with several other reports,23, 24 the risk of cerebrovascular events (ischaemic stroke and intracranial haemorrhage) was elevated after COVID-19, with the incidence of ischaemic stroke rising to almost one in ten (or three in 100 for a first stroke) in patients with encephalopathy.”
From 6-month neurological and psychiatric outcomes in 236 379 survivors of COVID-19: a retrospective cohort study using electronic health records (2021) · cites this paper as [24]
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Calderón‐Garcidueñas, L., Torres‐Jardón, R., Franco-Lira, M., Kulesza, R. J., González-Maciel, A., Reynoso-Robles, R., Brito-Aguilar, R., García-Arreola, B., Revueltas-Ficachi, P., Barrera-Velázquez, J. A., et al. (2020) · Journal of Alzheimer s Disease · doi:10.3233/jad-200891 · Cited by 40
Cerebrovascular Complications and Vessel Wall Imaging in COVID-19 Encephalopathy—A Pilot Study
Uginet, M., Bréville, G., Hofmeister, J., Machi, P., Lalive, P. H., Rosi, A., Fitsiori, A., Vargas, M. I., Assal, F., Allali, G., et al. (2021) · Clinical Neuroradiology · doi:10.1007/s00062-021-01008-2 · Cited by 37
Post-COVID-19 Syndrome Mechanisms, Prevention and Management
Najafi, M. B., & Javanmard, S. (2023) · International Journal of Preventive Medicine · doi:10.4103/ijpvm.ijpvm_508_21 · Cited by 38
Zhang, B., Wu, H., Kim, H., Welch, P. J., Cornett, A. M., Stocker, G. E., Nogueira, R. G., Kim, J., Owens, G. E., Dayton, P. A., et al. (2023) · Research · doi:10.34133/research.0048 · Cited by 36
Central Nervous System Manifestations of COVID-19: A Critical Review and Proposed Research Agenda
Hewitt, K. C., Marra, D. E., Block, C. K., Cysique, L. A., Drane, D. L., Haddad, M. M., Łojek, E., McDonald, C. R., Reyes, A., Eversole, K., et al. (2021) · Journal of the International Neuropsychological Society · doi:10.1017/s1355617721000345 · Cited by 36
Andriuta, D., Si-Ahmed, C., Roussel, M., Constans, J., Makki, M., Aarabi, A., Basille, D., Andréjak, C., & Godefroy, O. (2022) · Journal of Alzheimer s Disease · doi:10.3233/jad-215506 · Cited by 40
Neurologic complications of coronavirus and other respiratory viral infections
Cavallieri, F., Sellner, J., Zedde, M., & Moro, E. (2022) · Handbook of clinical neurology · doi:10.1016/b978-0-323-91532-8.00004-5 · Cited by 32
Neuroimaging Findings in Patients with COVID-19: A Systematic Review and Meta-Analysis
Kim, P. H., Kim, M., Suh, C. H., Chung, S. R., Park, J. E., Kim, S. C., Choi, Y. J., Lee, J. H., Kim, H. S., Baek, J. H., et al. (2021) · Korean Journal of Radiology · doi:10.3348/kjr.2021.0127 · Cited by 33
Wang, Y., Luu, L. D. W., Liu, S., Zhu, X., Huang, S., Li, F., Huang, X., Guo, L., Zhang, J., Ge, H., et al. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01641-y · Cited by 35
Marto, J. P., Strambo, D., Ntaios, G., Nguyen, T. N., Herzig, R., Członkowska, A., Demeestere, J., Mansour, O. Y., Salerno, A., Wegener, S., et al. (2022) · Neurology · doi:10.1212/wnl.0000000000201537 · Cited by 32
Nobleza, C. O. S. (2021) · CONTINUUM Lifelong Learning in Neurology · doi:10.1212/con.0000000000001018 · Cited by 30
Li, R., Liu, G., Zhang, X., Zhang, M., Lu, J., & Li, H. (2023) · BMC Infectious Diseases · doi:10.1186/s12879-023-08331-8 · Cited by 30
A review of ischemic stroke in COVID-19: currently known pathophysiological mechanisms
Tang, X., & Zheng, F. (2021) · Neurological Sciences · doi:10.1007/s10072-021-05679-0 · Cited by 28
COVID-19-Related Brain Injury: The Potential Role of Ferroptosis
Zhang, R., Sun, C., Chen, X., Han, Y., Zang, W., Jiang, C., Wang, J., & Wang, J. (2022) · Journal of Inflammation Research · doi:10.2147/jir.s353467 · Cited by 27
Neurological complications after COVID-19: A narrative review
Molaverdi, G., Kamal, Z., Safavi, M., Shafiee, A., Mozhgani, S., Ghobadi, M. Z., & Goudarzvand, M. (2023) · eNeurologicalSci · doi:10.1016/j.ensci.2023.100485 · Cited by 27
Intracranial hemorrhage in critically ill patients hospitalized for COVID-19
Fayed, I., Pivazyan, G., Conte, A. G., Chang, J. J., & Mai, J. C. (2020) · Journal of Clinical Neuroscience · doi:10.1016/j.jocn.2020.08.026 · Cited by 26
Khan, S., Siddique, R., Xiao, H., Lin, Y., Liu, Y., Wang, X., Hua, L., & Nabi, G. (2021) · International Journal of Biological Sciences · doi:10.7150/ijbs.66906 · Cited by 26
Trevino, T. N., Almousawi, A. A., Robinson, K. F., Fogel, A., Class, J., Minshall, R. D., Tai, L. M., Richner, J. M., & Lutz, S. E. (2024) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2024.578309 · Cited by 25
Neurological Implications of COVID-19: Role of Redox Imbalance and Mitochondrial Dysfunction
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Trigger Factors for Spontaneous Intracerebral Hemorrhage: A Case-Crossover Study
van Etten, E. S., Kaushik, K., Jolink, W. M. T., Koemans, E. A., Ekker, M. S., Rasing, I., Voigt, S., Schreuder, F. H. B. M., Cannegieter, S. C., Rinkel, G. J. E., et al. (2021) · Stroke · doi:10.1161/strokeaha.121.036233 · Cited by 24
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Retinal imaging study diagnoses in COVID-19: a case report
Ortiz-Egea, J. M., Ruiz‐Medrano, J., & Ruiz‐Moreno, J. M. (2021) · Journal of Medical Case Reports · doi:10.1186/s13256-020-02620-5 · Cited by 23
The squirrel monkey model in clinical neuroscience
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Acute ischemic stroke outcomes in patients with COVID-19: a systematic review and meta-analysis
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Mechanical Thrombectomy Outcomes in COVID-19 Patients With Acute Ischemic Stroke
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Phytochemicals targeting lncRNAs: A novel direction for neuroprotection in neurological disorders
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Parsay, S., Vosoughi, A., Khabbaz, A., & Sadigh‐Eteghad, S. (2020) · Journal of Stroke and Cerebrovascular Diseases · doi:10.1016/j.jstrokecerebrovasdis.2020.105552 · Cited by 20
Neuropathogenesis of acute coronavirus disease 2019
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Neuroinvasion and neurotropism of severe acute respiratory syndrome coronavirus 2 infection
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Colonna, S., Sciumè, L., Giarda, F., Innocenti, A., Beretta, G., & Costa, D. D. (2021) · Frontiers in Neurology · doi:10.3389/fneur.2020.602554 · Cited by 19
Metadata
- Authors
- Hernández-Fernández, F., Sandoval Valencia, H., Barbella-Aponte, R. A., Collado-Jiménez, R., Ayo-Martín, Ó., Barrena, C., Molina-Nuevo, J. D., García-García, J., Lozano-Setién, E., Alcahut-Rodriguez, C., Martínez-Martín, Á., Sánchez-López, A., & Segura, T.
- Affiliations
- Department of Neurology, Hospital General Universitario de Albacete, Albacete, Spain
- Department of Neurosurgery, Hospital General Universitario de Albacete, Albacete, Spain
- Hospital General Universitario de Albacete (ES)
- Department of Radiology, Hospital General Universitario de Albacete, Albacete, Spain
- Anaesthesia Intensive Care Unit, Hospital General Universitario de Albacete, Albacete, Spain
- ORCID
- Venue
- Brain
- Publisher
- Oxford University Press (OUP)
- Published
- 2020-07-09
- Volume
- 143
- Issue
- 10
- Pages
- 3089-3103
- ISSN
- 0006-8950 (ISSN-L)
- 1460-2156
- PMC
- PMC7454411
- OpenAlex
- W3041271257
- Cited by
- 280
- References
- 47
- Citations by year
- 2026: 5 · 2025: 11 · 2024: 20 · 2023: 41 · 2022: 48 · 2021: 105 · 2020: 49
- FWCI
- 26.29
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
- Locations
- Brain (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Clinical Neurology › Long-Term Effects of COVID-19
- Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
- Health Sciences › Medicine › Clinical Neurology › Acute Ischemic Stroke Management
- Keywords
- COVID-19 pandemic, SARS-CoV-2, cerebrovascular disease, stroke, ischemic stroke, intracerebral hemorrhage, posterior circulation stroke, cerebral microbleeds, subarachnoid hemorrhage, leukoencephalopathy, posterior reversible encephalopathy syndrome, thrombotic microangiopathy, endothelial injury, ferritin, brain biopsy, arterial thrombus, age as prognostic factor
- MeSH terms
- Betacoronavirus, COVID-19, SARS-CoV-2, Age Factors, Aged, Brain, Cerebral Hemorrhage, Brain Ischemia, Female, Ferritins, Humans, Magnetic Resonance Imaging, Male, Pneumonia, Viral, Spain, Tomography, X-Ray Computed, Comorbidity, Incidence, Coronavirus Infections, Leukoencephalopathies, Pandemics, Neuroimaging
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