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Research ArticleAdult Brain
Open Access

Brain and Lung Imaging Correlation in Patients with COVID-19: Could the Severity of Lung Disease Reflect the Prevalence of Acute Abnormalities on Neuroimaging? A Global Multicenter Observational Study

A. Mahammedi, A. Ramos, N. Bargalló, M. Gaskill, S. Kapur, L. Saba, H. Carrete, S. Sengupta, E. Salvador, A. Hilario, Y. Revilla, M. Sanchez, M. Perez-Nuñez, S. Bachir, B. Zhang, L. Oleaga, J. Sergio, L. Koren, P. Martin-Medina, L. Wang, M. Benegas, F. Ostos, G. Gonzalez-Ortega, P. Calleja, G. Udstuen, B. Williamson, V. Khandwala, S. Chadalavada, D. Woo and A. Vagal
American Journal of Neuroradiology March 2021, DOI: https://doi.org/10.3174/ajnr.A7072
A. Mahammedi
aFrom the Departments of Neuroradiology, (A.M., A.V., M.G., L.W., G.U., B.W., V.K.), Cardiopulmonary Imaging, (S.K.), Neurology (S.S., D.W.), and Department of Informatics and Interventional Radiology, (S.C.), University of Cincinnati Medical Center, Cincinnati, Ohio
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A. Ramos
bDepartments of Epidemiology and Biostatistics (B.Z.) and Pediatrics, (S.B.), Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio
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N. Bargalló
dDepartments of Neuroradiology (L.O., N.B.) and Cardiopulmonary Imaging (M.S., M.B., J.S.), Hospital Clínic de Barcelona, Sunyer Biomedical Research Institute, Barcelona, Spain
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M. Gaskill
aFrom the Departments of Neuroradiology, (A.M., A.V., M.G., L.W., G.U., B.W., V.K.), Cardiopulmonary Imaging, (S.K.), Neurology (S.S., D.W.), and Department of Informatics and Interventional Radiology, (S.C.), University of Cincinnati Medical Center, Cincinnati, Ohio
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S. Kapur
aFrom the Departments of Neuroradiology, (A.M., A.V., M.G., L.W., G.U., B.W., V.K.), Cardiopulmonary Imaging, (S.K.), Neurology (S.S., D.W.), and Department of Informatics and Interventional Radiology, (S.C.), University of Cincinnati Medical Center, Cincinnati, Ohio
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L. Saba
eDepartment of Neuroradiology (L.S.), Azienda Ospedaliero Universitaria di Cagliari, Monserrato (Cagliari), Italy
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H. Carrete Jr
fDepartment of Neuroradiology (H.C.), Escola Paulista de Medicina, Federal University of São Paulo, São Paulo, Brazil
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S. Sengupta
aFrom the Departments of Neuroradiology, (A.M., A.V., M.G., L.W., G.U., B.W., V.K.), Cardiopulmonary Imaging, (S.K.), Neurology (S.S., D.W.), and Department of Informatics and Interventional Radiology, (S.C.), University of Cincinnati Medical Center, Cincinnati, Ohio
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E. Salvador
cDepartments of Neuroradiology (A.R., E.S., A.H., L.K., P.M.-M.), Cardiopulmonary Imaging (Y.R., M.P.-N.) and Neurology (F.O., G.G.-O., P.C.), Hospital Universitario 12 de Octubre, Madrid, Spain
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A. Hilario
cDepartments of Neuroradiology (A.R., E.S., A.H., L.K., P.M.-M.), Cardiopulmonary Imaging (Y.R., M.P.-N.) and Neurology (F.O., G.G.-O., P.C.), Hospital Universitario 12 de Octubre, Madrid, Spain
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Y. Revilla
cDepartments of Neuroradiology (A.R., E.S., A.H., L.K., P.M.-M.), Cardiopulmonary Imaging (Y.R., M.P.-N.) and Neurology (F.O., G.G.-O., P.C.), Hospital Universitario 12 de Octubre, Madrid, Spain
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M. Sanchez
dDepartments of Neuroradiology (L.O., N.B.) and Cardiopulmonary Imaging (M.S., M.B., J.S.), Hospital Clínic de Barcelona, Sunyer Biomedical Research Institute, Barcelona, Spain
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M. Perez-Nuñez
cDepartments of Neuroradiology (A.R., E.S., A.H., L.K., P.M.-M.), Cardiopulmonary Imaging (Y.R., M.P.-N.) and Neurology (F.O., G.G.-O., P.C.), Hospital Universitario 12 de Octubre, Madrid, Spain
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S. Bachir
fDepartment of Neuroradiology (H.C.), Escola Paulista de Medicina, Federal University of São Paulo, São Paulo, Brazil
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B. Zhang
bDepartments of Epidemiology and Biostatistics (B.Z.) and Pediatrics, (S.B.), Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio
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L. Oleaga
dDepartments of Neuroradiology (L.O., N.B.) and Cardiopulmonary Imaging (M.S., M.B., J.S.), Hospital Clínic de Barcelona, Sunyer Biomedical Research Institute, Barcelona, Spain
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J. Sergio
dDepartments of Neuroradiology (L.O., N.B.) and Cardiopulmonary Imaging (M.S., M.B., J.S.), Hospital Clínic de Barcelona, Sunyer Biomedical Research Institute, Barcelona, Spain
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L. Koren
cDepartments of Neuroradiology (A.R., E.S., A.H., L.K., P.M.-M.), Cardiopulmonary Imaging (Y.R., M.P.-N.) and Neurology (F.O., G.G.-O., P.C.), Hospital Universitario 12 de Octubre, Madrid, Spain
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P. Martin-Medina
cDepartments of Neuroradiology (A.R., E.S., A.H., L.K., P.M.-M.), Cardiopulmonary Imaging (Y.R., M.P.-N.) and Neurology (F.O., G.G.-O., P.C.), Hospital Universitario 12 de Octubre, Madrid, Spain
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L. Wang
aFrom the Departments of Neuroradiology, (A.M., A.V., M.G., L.W., G.U., B.W., V.K.), Cardiopulmonary Imaging, (S.K.), Neurology (S.S., D.W.), and Department of Informatics and Interventional Radiology, (S.C.), University of Cincinnati Medical Center, Cincinnati, Ohio
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M. Benegas
dDepartments of Neuroradiology (L.O., N.B.) and Cardiopulmonary Imaging (M.S., M.B., J.S.), Hospital Clínic de Barcelona, Sunyer Biomedical Research Institute, Barcelona, Spain
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F. Ostos
cDepartments of Neuroradiology (A.R., E.S., A.H., L.K., P.M.-M.), Cardiopulmonary Imaging (Y.R., M.P.-N.) and Neurology (F.O., G.G.-O., P.C.), Hospital Universitario 12 de Octubre, Madrid, Spain
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G. Gonzalez-Ortega
cDepartments of Neuroradiology (A.R., E.S., A.H., L.K., P.M.-M.), Cardiopulmonary Imaging (Y.R., M.P.-N.) and Neurology (F.O., G.G.-O., P.C.), Hospital Universitario 12 de Octubre, Madrid, Spain
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P. Calleja
cDepartments of Neuroradiology (A.R., E.S., A.H., L.K., P.M.-M.), Cardiopulmonary Imaging (Y.R., M.P.-N.) and Neurology (F.O., G.G.-O., P.C.), Hospital Universitario 12 de Octubre, Madrid, Spain
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G. Udstuen
aFrom the Departments of Neuroradiology, (A.M., A.V., M.G., L.W., G.U., B.W., V.K.), Cardiopulmonary Imaging, (S.K.), Neurology (S.S., D.W.), and Department of Informatics and Interventional Radiology, (S.C.), University of Cincinnati Medical Center, Cincinnati, Ohio
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B. Williamson
aFrom the Departments of Neuroradiology, (A.M., A.V., M.G., L.W., G.U., B.W., V.K.), Cardiopulmonary Imaging, (S.K.), Neurology (S.S., D.W.), and Department of Informatics and Interventional Radiology, (S.C.), University of Cincinnati Medical Center, Cincinnati, Ohio
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V. Khandwala
aFrom the Departments of Neuroradiology, (A.M., A.V., M.G., L.W., G.U., B.W., V.K.), Cardiopulmonary Imaging, (S.K.), Neurology (S.S., D.W.), and Department of Informatics and Interventional Radiology, (S.C.), University of Cincinnati Medical Center, Cincinnati, Ohio
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S. Chadalavada
aFrom the Departments of Neuroradiology, (A.M., A.V., M.G., L.W., G.U., B.W., V.K.), Cardiopulmonary Imaging, (S.K.), Neurology (S.S., D.W.), and Department of Informatics and Interventional Radiology, (S.C.), University of Cincinnati Medical Center, Cincinnati, Ohio
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D. Woo
aFrom the Departments of Neuroradiology, (A.M., A.V., M.G., L.W., G.U., B.W., V.K.), Cardiopulmonary Imaging, (S.K.), Neurology (S.S., D.W.), and Department of Informatics and Interventional Radiology, (S.C.), University of Cincinnati Medical Center, Cincinnati, Ohio
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A. Vagal
aFrom the Departments of Neuroradiology, (A.M., A.V., M.G., L.W., G.U., B.W., V.K.), Cardiopulmonary Imaging, (S.K.), Neurology (S.S., D.W.), and Department of Informatics and Interventional Radiology, (S.C.), University of Cincinnati Medical Center, Cincinnati, Ohio
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  • FIG 1.
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    FIG 1.

    Flow chart of the study.

  • FIG 2.
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    FIG 2.

    Receiver operating characteristic curve showing the sensitivity and specificity of the CT lung severity score as a predictor of acute neuroimaging abnormalities in patients with COVID-19 with neurologic symptoms. The area under the curve corresponds to the accuracy. ROC indicates receiver operating characteristic.

  • FIG 3.
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    FIG 3.

    Acute leukoencephalopathy. A 48-year-old man without a history of seizures presented with convulsions and altered mental status. Extensive and confluent symmetric deep and subcortical white matter FLAIR hyperintensities in the bilateral centra semiovale (A) and periventricular frontal and parietal regions (B) with associated mild restricted diffusion on DWI/ADC images, most prominent in the centra semiovale (C and D) and peritrigonal regions (E and F). No associated enhancement or microbleed was seen on the T1 postcontrast and SWI (not shown). Coronal MPR and axial noncontrast images in lung windows demonstrate mixed ground-glass and consolidative opacities in all lobes with a lower lung and peripheral predominance (G–J). The CT lung severity score was 16 (right upper lobe, right lower lobe, left upper lobe, left lower lobe, 25%–49% and right middle lobe 50%–75%). The chest CT scan was obtained 8 days after the initial onset of respiratory symptoms.

  • FIG 4.
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    FIG 4.

    Acute infarct, multifocal microbleeds, and subcortical white matter FLAIR hyperintensity. A 65-year-old man presented with altered mental status and ischemic stroke. Available prior brain MR imaging findings from 1 month ago were normal. A and B, New punctate microbleeds on gradient-echo sequences in the right superior parietal lobule, left inferior parietal lobule, and right cerebellum. Note a small area of restricted diffusion in the anterior left cerebellum on DWI/ADC images (C–D) with FLAIR hyperintensities (E), consistent with acute infarct. New punctate deep and subcortical white matter FLAIR hyperintensities without associated hemorrhage or restricted diffusion in the left-greater-than-right frontal (F), parietal (G), and occipital lobes (H). Axial chest CT images show right apical GGOs and biapical paraseptal emphysema (I). Bilateral GGOs are right greater than left (J). Patchy consolidations in the apical segment of the lower lobe of the right lung (K). Extensive consolidation with an air bronchogram in the right lower lobe (L). The CT lung severity score was 14. The chest CT scan was obtained 10 days after initial onset of respiratory symptoms.

  • FIG 5.
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    FIG 5.

    PRES. A 25-year-old woman presented with altered mental status and ischemic stroke. A and B, Extensive cortical and subcortical areas of T2/FLAIR hyperintensity in the right frontal and bilateral parietal lobes. Associated patchy and confluent leptomeningeal enhancement is seen only on FLAIR postcontrast image (C) but not on T1 postcontrast image (D). Note no restriction diffusion or hemosiderin on DWI and gradient-echo sequences (E and F). Axial chest CT scans show new extensive bilateral patchy consolidations in the upper lobes with bilateral right-more-than-left pleural effusions (G and H). The CT lung severity score was 12. The chest CT scan was obtained 7 days after the initial onset of respiratory symptoms.

  • FIG 6.
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    FIG 6.

    Multifocal microbleeds and deep white matter FLAIR hyperintensities. A 63-year-old man presented with altered mental status. Available prior brain MR imaging findings from 3 months ago were normal. Note confluent periventricular white matter T2/FLAIR hyperintensities, most prominent in the peritrigonal regions (A and B), with new punctate microbleeds on gradient-echo sequences in the right frontoparietal regions (C) and left frontal lobe (D). No associated enhancement is seen on the T1 postcontrast image. Axial chest CT images in lung windows show bilateral, peripheral, predominant ground-glass opacities and dependent consolidations in the upper and lower lobes (F–I). Note air bronchograms in both lower lobes (H and I). The CT lung severity score was 18. The chest CT scan was obtained 11 days after the initial onset of respiratory symptoms.

  • FIG 7.
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    FIG 7.

    Left TIPIC (carotidynia). A 40-year-old man without significant medical history or known trauma presented with myoclonus and acute tenderness overlying the left carotid artery with increased pulsation. Axial T1 fat-saturated postcontrast image shows asymmetric enhancement and nonstenotic thickening of the left common carotid wall (A, arrows), with T1 precontrast hyperintensity of a crescent-shaped subintimal focus (C, arrow), which is also hyperintense on T2 fat-saturated and T2-weighted (B and D) images. Differential considerations include carotidynia or dissection. However, given the significantly improved symptoms after anti-inflammatory treatment, the lack of luminal stenosis, and the patient’s neck pain characteristics, findings are most consistent with carotidynia. No follow-up imaging was available.

Tables

  • Figures
  • Neuroimaging characteristics of hospitalized patients with COVID-19 with new onset of neurologic symptomsa

    Neuroimaging CharacteristicsAll Patients (n = 135), CT (n = 132) or MR imaging (n = 36)
    T2/FLAIR white matter signal abnormality
     Nonconfluent punctate deep and subcortical white matter disease22/36 (61)
     Isolated, nonspecific9/36 (25)
     Associated restricted diffusion onlyb6/36 (17)
     Associated microhemorrhage onlyb3/36 (8)
     Associated microhemorrhage and restricted diffusionb4/36 (11)
    Confluent symmetric T2 hyperintensity without restricted diffusion or hemorrhage2/36 (5)
    Confluent symmetric T2 hyperintensity with mild restricted diffusionc2/36 (5)
    Enhancement (MR imaging with and without IV contrast)LeptomeningealdParenchymale Cranial nerves2/17 (12)2/17 (12)0/17 (0)
    Acute ischemic infarctsVascular territorySmall/watershed infarctsCardioembolic36/135 (27)21/135 (15)10/135 (7)5/135 (4)
    Intracranial hemorrhagesParenchymalSubarachnoidMicrohemorrhage14/135 (10)3/135 (2)4/135 (3)7/36 (19)
    Acute leukoencephalopathyc4/36 (11)
    PRES3/36 (8)
    Hypoxic-ischemic encephalopathy2/36 (5)
    TIPICf2/7 (28)
    • ↵a Numbers in parentheses are percentages.

    • bThought to be most consistent with acute lacunar infarcts with a few associated microhemorrhages (Figs 4 and 6).

    • cAcute leukoencephalopathy. A 48-year-old man without a history of seizures presented with convulsion and altered mental status (Fig 3).

    • dSeen on FLAIR postcontrast only and likely related to PRES (Fig 5).

    • eSeptic emboli with atypical left parietal abscess. A 70-year-old woman with high blood pressure, chronic kidney disease, and type 2 diabetes mellitus. Long admission in the intensive care unit with intubation for COVID-19 and bilateral pneumonia. She presented with alteration of mental state and difficulty to progress in the weaning process. No history of malignancy (Online Supplemental Data).

    • fLeft TIPIC (carotidynia). A 40 -year-old man without significant medical history or known trauma presented with myoclonus and acute tenderness overlying the left carotid artery with increased pulsation. His symptoms significantly improved after steroid therapy (Fig 7).

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A. Mahammedi, A. Ramos, N. Bargalló, M. Gaskill, S. Kapur, L. Saba, H. Carrete, S. Sengupta, E. Salvador, A. Hilario, Y. Revilla, M. Sanchez, M. Perez-Nuñez, S. Bachir, B. Zhang, L. Oleaga, J. Sergio, L. Koren, P. Martin-Medina, L. Wang, M. Benegas, F. Ostos, G. Gonzalez-Ortega, P. Calleja, G. Udstuen, B. Williamson, V. Khandwala, S. Chadalavada, D. Woo, A. Vagal
Brain and Lung Imaging Correlation in Patients with COVID-19: Could the Severity of Lung Disease Reflect the Prevalence of Acute Abnormalities on Neuroimaging? A Global Multicenter Observational Study
American Journal of Neuroradiology Mar 2021, DOI: 10.3174/ajnr.A7072

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Brain and Lung Imaging Correlation in Patients with COVID-19: Could the Severity of Lung Disease Reflect the Prevalence of Acute Abnormalities on Neuroimaging? A Global Multicenter Observational Study
A. Mahammedi, A. Ramos, N. Bargalló, M. Gaskill, S. Kapur, L. Saba, H. Carrete, S. Sengupta, E. Salvador, A. Hilario, Y. Revilla, M. Sanchez, M. Perez-Nuñez, S. Bachir, B. Zhang, L. Oleaga, J. Sergio, L. Koren, P. Martin-Medina, L. Wang, M. Benegas, F. Ostos, G. Gonzalez-Ortega, P. Calleja, G. Udstuen, B. Williamson, V. Khandwala, S. Chadalavada, D. Woo, A. Vagal
American Journal of Neuroradiology Mar 2021, DOI: 10.3174/ajnr.A7072
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