Morphological, cellular and molecular basis of brain infection in COVID-19 patients
Open accessAbstract
Although increasing evidence confirms neuropsychiatric manifestations associated mainly with severe COVID-19 infection, the long-term neuropsychiatric dysfunction has been frequently observed after mild infection. Here we show the spectrum of the cerebral impact of SARS-CoV-2 infection ranging from long-term alterations in mildly infected individuals (orbitofrontal cortical atrophy, neurocognitive impairment, excessive fatigue and anxiety symptoms) to severe acute damage confirmed in brain tissue samples extracted from the orbitofrontal region (via endonasal trans-ethmoidal approach) from individuals who died of COVID-19. We used surface-based analyses of 3T MRI and identified orbitofrontal cortical atrophy in a group of 81 mildly infected patients (77% referred anosmia or dysgeusia during acute stage) compared to 145 healthy volunteers; this atrophy correlated with symptoms of anxiety and cognitive dysfunction. In an independent cohort of 26 individuals who died of COVID-19, we used histopathological signs of brain damage as a guide for possible SARS-CoV-2 brain infection, and found that among the 5 individuals who exhibited those signs, all of them had genetic material of the virus in the brain. Brain tissue samples from these 5 patients also exhibited foci of SARS-CoV-2 infection and replication, particularly in astrocytes. Supporting the hypothesis of astrocyte infection, neural stem cell-derived human astrocytes in vitro are susceptible to SARS-CoV-2 infection through a non-canonical mechanism that involves spike-NRP1 interaction. SARS-CoV-2-infected astrocytes manifested changes in energy metabolism and in key proteins and metabolites used to fuel neurons, as well as in the biogenesis of neurotransmitters. Moreover, human astrocyte infection elicits a secretory phenotype that reduces neuronal viability. Our data support the model in which SARS-CoV-2 reaches the brain, infects astrocytes and consequently leads to neuronal death or dysfunction. These deregulated processes are also likely to contribute to the structural and functional alterations seen in the brains of COVID-19 patients.
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SARS-CoV-2 infection is associated with a non-negligible incidence of neurological and psychiatric manifestations.
“Recent reports highlighting the risk for neuropsychiatric impairments secondary to COVID-19 showed that SARS-CoV-2 infection is associated with non-negligible incidence of neurological and psychiatric manifestations”
From Cognitive decline following acute viral infections: literature review and projections for post-COVID-19 (2022) · cites this paper as [17]
Neuropsychiatric and cognitive symptoms may arise as a direct CNS infection by SARS-CoV-2.
“provided evidence that neuropsychiatric and cognitive symptoms may arise as a direct CNS infection by the virus also [17, 136].”
From Cognitive decline following acute viral infections: literature review and projections for post-COVID-19 (2022) · cites this paper as [17]
Cognitive impairment, mainly attention and executive dysfunctions, has been reported in 28-56% of patients with mild or asymptomatic COVID-19.
“Another study showed that cognitive impairment (mainly attention and executive dysfunctions) has been reported in 28–56% of patients with mild or asymptomatic COVID-19”
From Cognitive decline following acute viral infections: literature review and projections for post-COVID-19 (2022) · cites this paper as [17]
The cognitive impairment in mild or asymptomatic COVID-19 was correlated with decreased cortical thickness in the right gyrus rectus and in language-associated areas.
“which was correlated with decreased cortical thickness in the right gyrus rectus, and in language associated areas [17].”
From Cognitive decline following acute viral infections: literature review and projections for post-COVID-19 (2022) · cites this paper as [17]
The brain may be a sanctuary for SARS-CoV-2.
“Additionally, SARS-CoV-2 was found in astrocytes of all deceased patients with brain damage, underscoring the fact that brain may be a sanctuary for SARS-CoV-2 [17].”
From Cognitive decline following acute viral infections: literature review and projections for post-COVID-19 (2022) · cites this paper as [17]
SARS-CoV-2 was found in astrocytes of all deceased patients with brain damage.
“Additionally, SARS-CoV-2 was found in astrocytes of all deceased patients with brain damage, underscoring the fact that brain may be a sanctuary for SARS-CoV-2 [17].”
From Cognitive decline following acute viral infections: literature review and projections for post-COVID-19 (2022) · cites this paper as [17]
The finding that SARS-CoV-2 infects astrocytes and its role with amyloid-β deposition underscores a possible link between COVID-19 infection and Alzheimer's disease.
“The finding that SARS-CoV-2 infects astrocytes [17] and its role with amyloid-β (Aβ) deposition, underscores a possible link between COVID-19 infection and AD.”
From Cognitive decline following acute viral infections: literature review and projections for post-COVID-19 (2022) · cites this paper as [17]
Once the virus enters the CNS, it affects neurons, microglia, oligodendrocytes, and especially astrocytes, undermining neuron viability.
“Once the virus enters the CNS, it affects neurons, microglia, oligodendrocytes, and especially astrocytes, undermining neurons viability [17, 179, 180].”
From Cognitive decline following acute viral infections: literature review and projections for post-COVID-19 (2022) · cites this paper as [17]
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Tropism of SARS-CoV-2 for human cortical astrocytes
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Self-citation
- Authors
- Crunfli, F., Carregari, V. C., Veras, F. P., Vendramini, P. H., Valença, A. G. F., Antunes, A. S. L. M., Brandão-Teles, C., da Silva Zuccoli, G., Reis-de-Oliveira, G., Silva-Costa, L. C., Saia-Cereda, V. M., Smith, B. J., Codo, A. C., de Souza, G. F., Muraro, S. P., Parise, P. L., Toledo-Teixeira, D. A., de Castro, Í. M. S., Melo, B. M. S., Almeida, G. M., Firmino, E. M. S., Paiva, I. M., Silva, B. M. S., Guimarães, R. M., Mendes, N. D., Ludwig, R. G., Ruiz, G. P., Knittel, T. L., Davanzo, G. G., Gerhardt, J. A., Rodrigues, P. B., Forato, J., Amorim, M. R., Silva, N. B., Martini, M. C., Benatti, M. N., Batah, S., Siyuan, L., João, R. B., Silva, L. S., Nogueira, M. H., Aventurato, Í. K., de Brito, M. R., Alvim, M. K. M., da Silva Júnior, J. R., Damião, L. L., de Sousa, I. M. P., da Rocha, E. D., Gonçalves, S. M., da Silva, L. H. L., Bettini, V., de Campos, B. M., Ludwig, G., Tavares, L. A., Pontelli, M. C., Viana, R. M. M., Martins, R., Vieira, A. S., Alves-Filho, J. C., Arruda, E., Podolski-Gondim, G., Santos, M. V., Neder, L., Cendes, F., Louzada-Junior, P., Oliveira, R. D., Cunha, F. Q., Damásio, A., Vinolo, M. A. R., Munhoz, C. D., Rehen, S. K., Nakaya, H. I., Mauad, T., Duarte-Neto, A. N., da Silva, L. F. F., Dolhnikoff, M., Saldiva, P., Farias, A. S., Moraes-Vieira, P. M. M., Fabro, A. T., Sebollela, A. S., Módena, J. L. P., Yasuda, C. L., Mori, M. A., Cunha, T. M., & Martins-de-Souza, D.
- Affiliations
- Universidade Estadual de Campinas (UNICAMP) (BR)
- Universidade de São Paulo (BR)
- Universidade Federal do Rio de Janeiro (BR)
- Corresponding author
- Yasuda, Clarissa Lin
- Mori, Marcelo A.
- Cunha, Thiago Mattar
- ORCID
- Crunfli, Fernanda
- Carregari, Victor Corasolla
- Veras, Flavio Protasio
- Vendramini, Pedro Henrique
- Valença, Aline Gazzola Fragnani
- Antunes, André Saraiva Leão Marcelo
- Brandão-Teles, Caroline
- da Silva Zuccoli, Giuliana
- Reis-de-Oliveira, Guilherme
- Silva-Costa, Lícia C.
- Saia-Cereda, Verônica Monteiro
- Smith, Bradley Joseph
- Codo, Ana Campos
- de Souza, Gabriela Fabiano
- Muraro, Stéfanie Primon
- Parise, Pierina Lorencini
- Toledo-Teixeira, Daniel A.
- Melo, Bruno Marcel Silva
- Almeida, Glaucia M.
- Firmino, Egidi Mayara Silva
- Paiva, Isadora Marques
- Guimarães, Rafaela Mano
- Mendes, Niele D.
- Ruiz, Gabriel Palermo
- Knittel, Thiago Leite
- Davanzo, Gustavo Gastão
- Gerhardt, Jaqueline Aline
- Rodrigues, Patrícia Brito
- Forato, Julia
- Amorim, Mariene Ribeiro
- Silva, Natália Brunetti
- Martini, Matheus Cavalheiro
- Benatti, Maíra Nilson
- Batah, Sabrina
- Siyuan, Li
- João, Rafael Batista
- Silva, Lucas Scardua
- Nogueira, Mateus Henrique
- Aventurato, Ítalo Karmann
- Alvim, Marina Koutsodontis Machado
- Gonçalves, Solange Maria
- Ludwig, Guilherme
- Tavares, Lucas Alves
- Pontelli, Marjorie Cornejo
- Viana, Rosa Maria Mendes
- Vieira, Andre S.
- Alves-Filho, José Carlos
- Arruda, Eurico
- Santos, Marcelo Volpon
- Neder, Luciano
- Cendes, Fernando
- Oliveira, Renê Donizeti
- Cunha, Fernando Queiroz
- Damásio, André
- Vinolo, Marco Aurélio Ramirez
- Munhoz, Carolina Demarchi
- Rehen, Stevens K.
- Nakaya, Helder I
- Duarte-Neto, Amaro Nunes
- Dolhnikoff, Marisa
- Saldiva, Paulo
- Farias, Alessandro S.
- Moraes-Vieira, Pedro Manoel M.
- Fabro, Alexandre Todorovic
- Sebollela, Adriano S.
- Módena, José Luiz Proença
- Yasuda, Clarissa Lin
- Mori, Marcelo A.
- Cunha, Thiago Mattar
- Martins-de-Souza, Daniel
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- openRxiv
- Published
- 2020-10-13
- Volume
- 119
- Issue
- 35
- Pages
- e2200960119-e2200960119
- ISSN
- 0027-8424 (ISSN-L)
- PMC
- PMC9436354
- OpenAlex
- W4291021482
- Cited by
- 331
- References
- 139
- Citations by year
- 2026: 36 · 2025: 56 · 2024: 80 · 2023: 99 · 2022: 40 · 2021: 17 · 2020: 2 · 2013: 1
- FWCI
- 36.31
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc-nd
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion, cc-by-nc-nd)
- medRxiv (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Funders
- Fundação de Amparo à Pesquisa do Estado de São Paulo (20/05601-6, #2013-07559-3, 2019/, 13/07607-8, 2014/, 2013/08216- 2, 2013/07607, 19/00098-7, 20/04860-8, 2013 07607-8, 2014/10 068–4, 13/08216-2, 20/04746-0, 17/25588-1, 2019/11457-8, 20/04919-2, 2013/08216)
- Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (2013/08216-2, 2013/07607-8)
- Conselho Nacional de Desenvolvimento Científico e Tecnológico (2013/07607-8, #2013/08216-2)
- Topics
- Health Sciences › Medicine › Neurology › Long-Term Effects of COVID-19
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
- Keywords
- COVID-19 pandemic, SARS-CoV-2, brain infection, long COVID, neuropsychiatric symptoms, orbitofrontal cortex, cortical atrophy, neurocognitive impairment, astrocyte energy metabolism, neuronal cell death, brain histopathology, postmortem brain
- MeSH terms
- COVID-19, SARS-CoV-2, Post-Acute COVID-19 Syndrome, Astrocytes, Brain, Humans, Central Nervous System Viral Diseases
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
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