Download PDF
CC BY 4.0 · Arq Neuropsiquiatr 2023; 81(11): 989-999
DOI: 10.1055/s-0043-1772834
View and Review

Intracranial hemorrhages in patients with COVID-19: a systematic review of the literature, regarding six cases in an Amazonian population

Hemorragias intracranianas em pacientes com COVID-19: uma revisão sistemática da literatura, a propósito de seis casos na população amazônica
William de Sousa Lima 
1   Universidade Federal do Pará, Faculdade de Medicina, Departamento de Neurologia do Hospital Universitário João de Barros Barreto, Belém PA, Brazil.
,
Marcelo Henrique Pereira Soares 
1   Universidade Federal do Pará, Faculdade de Medicina, Departamento de Neurologia do Hospital Universitário João de Barros Barreto, Belém PA, Brazil.
,
Eric Homero Albuquerque Paschoal 
1   Universidade Federal do Pará, Faculdade de Medicina, Departamento de Neurologia do Hospital Universitário João de Barros Barreto, Belém PA, Brazil.
,
Joelma Karin Sagica Fernandes Paschoal 
1   Universidade Federal do Pará, Faculdade de Medicina, Departamento de Neurologia do Hospital Universitário João de Barros Barreto, Belém PA, Brazil.
,
Fernando Mendes Paschoal  Jr.
1   Universidade Federal do Pará, Faculdade de Medicina, Departamento de Neurologia do Hospital Universitário João de Barros Barreto, Belém PA, Brazil.
,
Edson Bor-Seng-Shu 
2   Universidade de São Paulo, Faculdade de Medicina, Departamento de Neurologia do Hospital das Clínicas, São Paulo SP, Brazil.
› Author Affiliations
› Further Information
   Permissions and Reprints

Abstract

Background Coronavirus disease 2019 (COVID-19) has emerged as a public health emergency worldwide, predominantly affecting the respiratory tract. However, evidence supports the involvement of extrapulmonary sites, including reports of intracranial hemorrhages.

Objective To describe six original cases and review the literature on intracranial hemorrhages in patients diagnosed with COVID-19 by molecular methods.

Methods A systematic literature review was performed on MEDLINE, PubMed, and NCBI electronic databases to identify eligible studies. Of the total 1,624 articles retrieved, only 53 articles met the inclusion criteria.

Results The overall incidence of intracranial hemorrhage in patients hospitalized for COVID-19 was 0.26%. In this patient group, the mean age was 60 years, and the majority were male (68%) with initial respiratory symptoms (73%) and some comorbidity. Before the diagnosis of hemorrhage, 43% of patients were using anticoagulants, 47.3% at therapeutic doses. The intraparenchymal (50%) was the most affected compartment, followed by the subarachnoid (34%), intraventricular (11%), and subdural (7%). There was a predominance of lobar over non-lobar topographies. Multifocal or multicompartmental hemorrhages were described in 25% of cases. Overall mortality in the cohort studies was 44%, while around 55% of patients were discharged from hospital.

Conclusion Despite the unusual association, the combination of these two diseases is associated with high rates of mortality and morbidity, as well as more severe clinicoradiological presentations. Further studies are needed to provide robust evidence on the exact pathophysiology behind the occurrence of intracranial hemorrhages after COVID-19 infection.

Resumo

Antecedentes A COVID-19 emergiu como uma emergência de saúde pública em todo o mundo, proporcionando lesão principalmente do trato respiratório. No entanto, várias evidências apontam para acometimento de sítios extrapulmonares, incluindo relatos de hemorragias intracranianas.

Objetivo Descrever seis casos originais e revisar a literatura sobre hemorragias intracranianas em pacientes com diagnostico de COVID-19 por métodos moleculares.

Métodos A revisão sistemática da literatura foi feita nas bases de dados eletrônicas da MEDLINE, PubMed e NCBI para identificar os estudos elegíveis. Do total de 1.624 artigos recuperados, apenas 53 artigos preencheram os critérios de inclusão.

Resultados A incidência geral de hemorragia intracraniana nos pacientes internados por COVID-19 foi de 0,26%. A média de idade foi de 60 anos, e a maioria dos pacientes era do sexo masculino (68%) com sintomas respiratórios iniciais (73%) e alguma comorbidade. Antes do diagnóstico de hemorragia, 43% estavam em uso de anticoagulantes, 47,3% destes em doses terapêuticas. O compartimento mais acometido foi o intraparenquimatoso (50%), seguido do subaracnoideo (34%), intraventricular (11%) e subdural (7%). Houve predomínio de topografias lobares sobre as não-lobares. Hemorragias multifocais ou multicompartimentais foram descritas em 25% dos casos. A mortalidade geral nos estudos de coorte foi de 44%, enquanto houve alta hospitalar em cerca de 55% dos pacientes.

Conclusão Apesar da associação incomum, a combinação dessas doenças está relacionada com altas taxas de mortalidade e morbidade, bem como apresentações clínico-radiológicas mais graves. Mais estudos são necessários para oferecer evidências robustas sobre a fisiopatologia exata por trás da ocorrência de hemorragias intracranianas após infecção por COVID-19.

Keywords

COVID-19 - Intracranial Hemorrhages - Cerebral Hemorrhage - Hemorrhagic Stroke

Palavras-chave

COVID-19 - Hemorragias Intracranianas - Hemorragia Cerebral - Acidente Vascular Cerebral Hemorrágico

Authors' Contributions

WSL: conceptualization, data curation, formal analysis, funding acquisition, investigation, methodology, project administration, visualization, writing – original draft, and writing – review & editing; MHPS: data curation, formal analysis, investigation, methodology, project administration, writing – original draft, and writing – review & editing; EHAP: project administration, resources, software, supervision, validation, visualization, and writing – review & editing; JKSFP: Project administration, resources, supervision, validation, visualization, and writing – review & editing; FMPJ: conceptualization, funding acquisition, investigation, methodology, project administration, resources, software, supervision, validation, visualization, writing – original draft, and writing – review & editing; EBSS: project administration, resources, software, supervision, validation, visualization, and writing – review & editing.


Supplementary Material



Publication History

Received: 15 October 2022

Accepted: 01 May 2023

Article published online:
30 November 2023

© 2023. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution 4.0 International License, permitting copying and reproduction so long as the original work is given appropriate credit (https://creativecommons.org/licenses/by/4.0/)

Thieme Revinter Publicações Ltda.
Rua do Matoso 170, Rio de Janeiro, RJ, CEP 20270-135, Brazil

 

  • References

  • 1 World Health Organization. Coronavirus disease (COVID-19) outbreak [Internet]. 2021 [cited 2021 Mar 24]. Available from: https://www.who.int/emergencies/diseases/novel-coronavirus-2019
    PubMedGoogle Scholar
  • 2 Thakur V, Ratho RK, Kumar P. et al. Multi-Organ Involvement in COVID-19: Beyond Pulmonary Manifestations. J Clin Med 2021; 10 (03) 446
    CrossrefPubMedGoogle Scholar
  • 3 Sun BW, Zhang M, Wang PC, Song JT. A Clinical Analysis of Extrapulmonary Complications in Novel Coronavirus Pneumonia Patients. Int J Gen Med 2021; 14: 381-385
    CrossrefPubMedGoogle Scholar
  • 4 Mao L, Jin H, Wang M. et al. Neurologic Manifestations of Hospitalized Patients With Coronavirus Disease 2019 in Wuhan, China. JAMA Neurol 2020; 77 (06) 683-690
    CrossrefPubMedGoogle Scholar
  • 5 Tawakul AA, Alharbi AH, Basahal AM. et al. Neurological Symptoms and Complications of COVID-19 Among Patients in a Tertiary Hospital in Saudi Arabia. Cureus 2021; 13 (11) e19200
    PubMedGoogle Scholar
  • 6 Chowdhary A, Subedi R, Tandon M. et al. Relevance and clinical significance of magnetic resonance imaging of neurological manifestations in covid-19: A systematic review of case reports and case series. Vol. 10, Brain Sciences. MDPI AG; 2020: 1-15
    Google Scholar
  • 7 Mogensen MA, Wangaryattawanich P, Hartman J, Filippi CG, Hippe DS, Cross NM. RSNA COVID-19 task force. Special report of the RSNA COVID-19 task force: systematic review of outcomes associated with COVID-19 neuroimaging findings in hospitalized patients. Br J Radiol 2021; 94 (1127) 20210149
    CrossrefPubMedGoogle Scholar
  • 8 Mahammedi A, Ramos A, Bargalló N. et al. 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. AJNR Am J Neuroradiol 2021; 42 (06) 1008-1016
    CrossrefPubMedGoogle Scholar
  • 9 Kuo W, Hӓne C, Mukherjee P, Malik J, Yuh EL. Expert-level detection of acute intracranial hemorrhage on head computed tomography using deep learning. Proc Natl Acad Sci U S A 2019; 116 (45) 22737-22745
    CrossrefPubMedGoogle Scholar
  • 10 Naidech AM. Intracranial hemorrhage. Am J Respir Crit Care Med 2011; 184 (09) 998-1006
    CrossrefPubMedGoogle Scholar
  • 11 Baig AM, Khaleeq A, Ali U, Syeda H. Evidence of the COVID-19 Virus Targeting the CNS: Tissue Distribution, Host-Virus Interaction, and Proposed Neurotropic Mechanisms. ACS Chem Neurosci 2020; 11 (07) 995-998
    CrossrefPubMedGoogle Scholar
  • 12 Klingenstein M, Klingenstein S, Neckel PH. et al. Evidence of SARS-CoV2 Entry Protein ACE2 in the Human Nose and Olfactory Bulb. Cells Tissues Organs 2020; 209 (4-6): 155-164
    CrossrefPubMedGoogle Scholar
  • 13 Pedersen SF, Ho YC. SARS-CoV-2: a storm is raging. J Clin Invest 2020; 130 (05) 2202-2205
    CrossrefPubMedGoogle Scholar
  • 14 Wang Z, Yang Y, Liang X. et al. COVID-19 Associated Ischemic Stroke and Hemorrhagic Stroke: Incidence, Potential Pathological Mechanism, and Management. Front Neurol 2020; 11: 571996
    CrossrefPubMedGoogle Scholar
  • 15 Tang N, Li D, Wang X, Sun Z. Abnormal coagulation parameters are associated with poor prognosis in patients with novel coronavirus pneumonia. J Thromb Haemost 2020; 18 (04) 844-847
    CrossrefPubMedGoogle Scholar
  • 16 Valderrama EV, Humbert K, Lord A, Frontera J, Yaghi S. Severe Acute Respiratory Syndrome Coronavirus 2 Infection and Ischemic Stroke. Stroke 2020; 51 (07) e124-e127
    CrossrefPubMedGoogle Scholar
  • 17 Altschul DJ, Unda SR, de La Garza Ramos R. et al. Hemorrhagic presentations of COVID-19: Risk factors for mortality. Clin Neurol Neurosurg 2020; 198: 106112
    CrossrefPubMedGoogle Scholar
  • 18 Lersy F, Willaume T, Brisset JC. et al. Critical illness-associated cerebral microbleeds for patients with severe COVID-19: etiologic hypotheses. J Neurol 2021; 268 (08) 2676-2684
    CrossrefPubMedGoogle Scholar
  • 19 Rothstein A, Oldridge O, Schwennesen H, Do D, Cucchiara BL. Acute Cerebrovascular Events in Hospitalized COVID-19 Patients. Stroke 2020; 51 (09) e219-e222
    CrossrefPubMedGoogle Scholar
  • 20 John S, Hussain SI, Piechowski-Jozwiak B. et al. Clinical characteristics and admission patterns of stroke patients during the COVID 19 pandemic: A single center retrospective, observational study from the Abu Dhabi, United Arab Emirates. Clin Neurol Neurosurg 2020; 199: 106227
    CrossrefPubMedGoogle Scholar
  • 21 Al-Mufti F, Becker C, Kamal H. et al. Acute Cerebrovascular Disorders and Vasculopathies Associated with Significant Mortality in SARS-CoV-2 Patients Admitted to The Intensive Care Unit in The New York Epicenter. J Stroke Cerebrovasc Dis 2021; 30 (02) 105429
    CrossrefPubMedGoogle Scholar
  • 22 Migdady I, Shoskes A, Hasan LZ. et al. Timing of Acute Stroke in COVID-19-A Health System Registry Study. Neurohospitalist 2021; 11 (04) 285-294
    CrossrefPubMedGoogle Scholar
  • 23 Siegler JE, Cardona P, Arenillas JF. et al. Cerebrovascular events and outcomes in hospitalized patients with COVID-19: The SVIN COVID-19 Multinational Registry. Int J Stroke 2021; 16 (04) 437-447
    CrossrefPubMedGoogle Scholar
  • 24 Pavlov V, Beylerli O, Gareev I, Torres Solis LF, Solís Herrera A, Aliev G. COVID-19-Related Intracerebral Hemorrhage. Front Aging Neurosci 2020; 12: 600172
    CrossrefPubMedGoogle Scholar
  • 25 Qureshi AI, Baskett WI, Huang W. et al. Intracerebral Hemorrhage and Coronavirus Disease 2019 in a Cohort of 282,718 Hospitalized Patients. Neurocrit Care 2022; 36 (01) 259-265
    CrossrefPubMedGoogle Scholar
  • 26 Hernández-Fernández F, Sandoval Valencia H, Barbella-Aponte RA. et al. Cerebrovascular disease in patients with COVID-19: neuroimaging, histological and clinical description. Brain 2020; 143 (10) 3089-3103
    CrossrefPubMedGoogle Scholar
  • 27 Kvernland A, Kumar A, Yaghi S. et al. Anticoagulation use and Hemorrhagic Stroke in SARS-CoV-2 Patients Treated at a New York Healthcare System. Neurocrit Care 2021; 34 (03) 748-759
    CrossrefPubMedGoogle Scholar
  • 28 Melmed KR, Cao M, Dogra S. et al. Risk factors for intracerebral hemorrhage in patients with COVID-19. J Thromb Thrombolysis 2021; 51 (04) 953-960
    CrossrefPubMedGoogle Scholar
  • 29 Abbas R, El Naamani K, Sweid A. et al. Intracranial Hemorrhage in Patients with Coronavirus Disease 2019 (COVID-19): A Case Series. World Neurosurg 2021; 154: e473-e480
    CrossrefPubMedGoogle Scholar
  • 30 Fayed I, Pivazyan G, Conte AG, Chang J, Mai JC. Intracranial hemorrhage in critically ill patients hospitalized for COVID-19. J Clin Neurosci 2020; 81: 192-195
    CrossrefPubMedGoogle Scholar
  • 31 Keller E, Brandi G, Winklhofer S. et al. Large and Small Cerebral Vessel Involvement in Severe COVID-19: Detailed Clinical Workup of a Case Series. Stroke 2020; 51 (12) 3719-3722
    CrossrefPubMedGoogle Scholar
  • 32 Mousa-Ibrahim F, Berg S, Od TPDetola O, Teitcher M, Ruland S. Intracranial Hemorrhage in Hospitalized SARS-CoV-2 Patients: A Case Series. J Stroke Cerebrovasc Dis 2021; 30 (01) 105428
    CrossrefPubMedGoogle Scholar
  • 33 Ramos AD, Koyfman F, Byrns K. et al. Characterization of Hemorrhagic and Ischemic Stroke in a Diverse Cohort of COVID-19 Patients. Neurohospitalist 2021; 11 (04) 295-302
    CrossrefPubMedGoogle Scholar
  • 34 Sedova P, Brown Jr RD, Bryndziar T. et al. Treat covid-19, but not only covid-19: Stroke matters as well. Cerebrovasc Dis 2022; 51 (01) 52-59
    CrossrefPubMedGoogle Scholar
  • 35 Douiri A, Muruet W, Bhalla A. et al; SSNAP Collaboration. Stroke Care in the United Kingdom During the COVID-19 Pandemic. Stroke 2021; 52 (06) 2125-2133
    CrossrefPubMedGoogle Scholar
  • 36 Wu Y, Chen F, Wang Z. et al. Reductions in Hospital Admissions and Delays in Acute Stroke Care During the Pandemic of COVID-19. Front Neurol 2020; 11: 584734
    CrossrefPubMedGoogle Scholar
  • 37 Libruder C, Ram A, Hershkovitz Y. et al. Reduction in Acute Stroke Admissions during the COVID-19 Pandemic: Data from a National Stroke Registry. Neuroepidemiology 2021; 55 (05) 354-360
    CrossrefPubMedGoogle Scholar
  • 38 Balestrino M, Coccia A, Boffa AS. et al. Request of hospital care dropped for TIA but remained stable for stroke during COVID-19 pandemic at a large Italian university hospital. Intern Emerg Med 2021; 16 (03) 735-739
    CrossrefPubMedGoogle Scholar
  • 39 Diegoli H, Magalhães PSC, Martins SCO. et al. Decrease in Hospital Admissions for Transient Ischemic Attack, Mild, and Moderate Stroke During the COVID-19 Era. Stroke 2020; 51 (08) 2315-2321
    CrossrefPubMedGoogle Scholar
  • 40 Abdulazim A, Ebert A, Etminan N, Szabo K, Alonso A. Negative Impact of the COVID-19 Pandemic on Admissions for Intracranial Hemorrhage. Front Neurol 2020; 11: 584522
    CrossrefPubMedGoogle Scholar
  • 41 Nogueira RG, Abdalkader M, Qureshi MM. et al. Global impact of COVID-19 on stroke care. Int J Stroke 2021; 16 (05) 573-584
    CrossrefPubMedGoogle Scholar
  • 42 Tong X, King SMC, Asaithambi G. et al. COVID-19 Pandemic and Quality of Care and Outcomes of Acute Stroke Hospitalizations: the Paul Coverdell National Acute Stroke Program. Prev Chronic Dis 2021; 18: E82
    CrossrefPubMedGoogle Scholar
  • 43 Katz JM, Libman RB, Wang JJ. et al. Cerebrovascular Complications of COVID-19. Stroke 2020; 51 (09) e227-e231
    PubMedGoogle Scholar
  • 44 Jain R, Young M, Dogra S. et al. COVID-19 related neuroimaging findings: A signal of thromboembolic complications and a strong prognostic marker of poor patient outcome. J Neurol Sci 2020; 414: 116923
    CrossrefPubMedGoogle Scholar
  • 45 Mendes A, Herrmann FR, Genton L. et al. Incidence, characteristics and clinical relevance of acute stroke in old patients hospitalized with COVID-19. BMC Geriatr 2021; 21 (01) 52
    CrossrefPubMedGoogle Scholar
  • 46 Katsanos AH, Palaiodimou L, Zand R. et al. The Impact of SARS-CoV-2 on Stroke Epidemiology and Care: A Meta-Analysis. Ann Neurol 2021; 89 (02) 380-388
    CrossrefPubMedGoogle Scholar
  • 47 Syahrul S, Maliga HA, Ilmawan M. et al. Hemorrhagic and ischemic stroke in patients with coronavirus disease 2019: incidence, risk factors, and pathogenesis - a systematic review and meta-analysis. F1000 Res 2021; 10: 34
    CrossrefPubMedGoogle Scholar
  • 48 Nannoni S, de Groot R, Bell S, Markus HS. Stroke in COVID-19: A systematic review and meta-analysis. Int J Stroke 2021; 16 (02) 137-149
    CrossrefPubMedGoogle Scholar
  • 49 Tan YK, Goh C, Leow AST. et al. COVID-19 and ischemic stroke: a systematic review and meta-summary of the literature. J Thromb Thrombolysis 2020; 50 (03) 587-595
    CrossrefPubMedGoogle Scholar
  • 50 Cheruiyot I, Sehmi P, Ominde B. et al. Intracranial hemorrhage in coronavirus disease 2019 (COVID-19) patients. Neurol Sci 2021; 42 (01) 25-33
    CrossrefPubMedGoogle Scholar
  • 51 Cagnazzo F, Arquizan C, Derraz I. et al. Neurological manifestations of patients infected with the SARS-CoV-2: a systematic review of the literature. J Neurol 2021; 268 (08) 2656-2665
    CrossrefPubMedGoogle Scholar
  • 52 Nawabi J, Morotti A, Wildgruber M. et al. Clinical and imaging characteristics in patients with SARS-CoV-2 infection and acute intracranial hemorrhage. J Clin Med 2020; 9 (08) 1-15
    CrossrefPubMedGoogle Scholar
  • 53 Büttner L, Bauknecht HC, Fleckenstein FN. et al. Neuroimaging Findings in Conjunction with Severe COVID-19. Röfo Fortschr Geb Röntgenstr Neuen Bildgeb Verfahr 2021; 193 (07) 822-829
    PubMedGoogle Scholar
  • 54 Shahjouei S, Naderi S, Li J. et al. Risk of stroke in hospitalized SARS-CoV-2 infected patients: A multinational study. EBioMedicine 2020; 59: 102939
    CrossrefPubMedGoogle Scholar
  • 55 Cezar-Junior AB, Faquini IV, Silva JLJ. et al. Subarachnoid hemorrhage and COVID-19: Association or coincidence?. Medicine (Baltimore) 2020; 99 (51) e23862
    CrossrefPubMedGoogle Scholar
  • 56 Mishra S, Choueka M, Wang Q. et al. Intracranial Hemorrhage in COVID-19 Patients. J Stroke Cerebrovasc Dis 2021; 30 (04) 105603
    CrossrefPubMedGoogle Scholar
  • 57 Sawlani V, Scotton S, Nader K. et al. COVID-19-related intracranial imaging findings: a large single-centre experience. Clin Radiol 2021; 76 (02) 108-116
    CrossrefPubMedGoogle Scholar
  • 58 Choi Y, Lee MK. Neuroimaging findings of brain MRI and CT in patients with COVID-19: A systematic review and meta-analysis. Eur J Radiol 2020; 133: 109393
    CrossrefPubMedGoogle Scholar
  • 59 de Oliveira Manoel AL, Goffi A, Zampieri FG. et al. The critical care management of spontaneous intracranial hemorrhage: a contemporary review. Crit Care 2016; 20 (01) 272
    CrossrefPubMedGoogle Scholar
  • 60 Martini SR, Flaherty ML, Brown WM. et al. Risk factors for intracerebral hemorrhage differ according to hemorrhage location. Neurology 2012; 79 (23) 2275-2282
    CrossrefPubMedGoogle Scholar
  • 61 Kuo CL, Pilling LC, Atkins JL. et al. APOE e4 genotype predicts severe COVID-19 in the UK biobank community cohort. Vol. 75, Journals of Gerontology - Series A Biological Sciences and Medical Sciences. Oxford University Press; 2020: 2231-2232
    Google Scholar
  • 62 Kurki SN, Kantonen J, Kaivola K. et al; FinnGen. APOE ε4 associates with increased risk of severe COVID-19, cerebral microhaemorrhages and post-COVID mental fatigue: a Finnish biobank, autopsy and clinical study. Acta Neuropathol Commun 2021; 9 (01) 199
    CrossrefPubMedGoogle Scholar
  • 63 Zhang H, Shao L, Lin Z. et al. APOE interacts with ACE2 inhibiting SARS-CoV-2 cellular entry and inflammation in COVID-19 patients. Signal Transduct Target Ther 2022; 7 (01) 261 https://www.nature.com/articles/s41392-022-01118-4 [Internet]
    CrossrefPubMedGoogle Scholar
  • 64 Dhamoon MS, Thaler A, Gururangan K. et al; Mount Sinai Stroke Investigators*. Acute Cerebrovascular Events With COVID-19 Infection. Stroke 2021; 52 (01) 48-56
    CrossrefPubMedGoogle Scholar
  • 65 Dogra S, Jain R, Cao M. et al. Hemorrhagic stroke and anticoagulation in COVID-19. J Stroke Cerebrovasc Dis 2020; 29 (08) 104984
    CrossrefPubMedGoogle Scholar
  • 66 Paniz-Mondolfi A, Bryce C, Grimes Z. et al. Central nervous system involvement by severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2). J Med Virol 2020; 92 (07) 699-702
    CrossrefPubMedGoogle Scholar
  • 67 Wang H, Tang X, Fan H. et al. Potential mechanisms of hemorrhagic stroke in elderly COVID-19 patients. Aging (Albany NY) 2020; 12 (11) 10022-10034
    CrossrefPubMedGoogle Scholar
  • 68 Perrin P, Collongues N, Baloglu S. et al. Cytokine release syndrome-associated encephalopathy in patients with COVID-19. Eur J Neurol 2021; 28 (01) 248-258
    CrossrefPubMedGoogle Scholar
  • 69 Zhang F, Ren Y, Shi Y. et al. Predictive ability of admission neutrophil to lymphocyte ratio on short-term outcome in patients with spontaneous cerebellar hemorrhage. Medicine (Baltimore) 2019; 98 (25) e16120
    CrossrefPubMedGoogle Scholar
  • 70 Lattanzi S, di Napoli M, Ricci S, Divani AA. Matrix Metalloproteinases in Acute Intracerebral Hemorrhage. Vol. 17, Neurotherapeutics. Springer; 2020: 484-496
    Google Scholar
  • 71 Dakay K, Kaur G, Mayer SA, Santarelli J, Gandhi C, Al-Mufti F. Cerebral Herniation Secondary to Stroke-Associated Hemorrhagic Transformation, Fulminant Cerebral Edema in Setting of COVID-19 Associated ARDS and Active Malignancy. J Stroke Cerebrovasc Dis 2020; 29 (12) 105397
    CrossrefPubMedGoogle Scholar
  • 72 Dias DA, de Brito LA, Neves LO, Paiva RGS, Barbosa Júnior OA, Tavares-Júnior JWL. Hemorrhagic PRES: an unusual neurologic manifestation in two COVID-19 patients. Arq Neuropsiquiatr 2020; 78 (11) 739-740
    Article in Thieme ConnectPubMedGoogle Scholar
  • 73 Princiotta Cariddi L, Tabaee Damavandi P, Carimati F. et al. Reversible Encephalopathy Syndrome (PRES) in a COVID-19 patient. J Neurol 2020; 267 (11) 3157-3160
    CrossrefPubMedGoogle Scholar
  • 74 Sweid A, Hammoud B, Bekelis K. et al. Cerebral ischemic and hemorrhagic complications of coronavirus disease 2019. Int J Stroke 2020; 15 (07) 733-742
    CrossrefPubMedGoogle Scholar
  • 75 Wang HY, Li XL, Yan ZR, Sun XP, Han J, Zhang BW. Potential neurological symptoms of COVID-19. Ther Adv Neurol Disord 2020; 13: 1756286420917830
    CrossrefPubMedGoogle Scholar
  • 76 Divani AA, Liu X, Di Napoli M. et al. Blood Pressure Variability Predicts Poor In-Hospital Outcome in Spontaneous Intracerebral Hemorrhage. Stroke 2019; 50 (08) 2023-2029
    CrossrefPubMedGoogle Scholar
  • 77 Pal R, Bhansali A. COVID-19, diabetes mellitus and ACE2: The conundrum. Diabetes Res Clin Pract 2020; 162: 108132
    CrossrefPubMedGoogle Scholar
  • 78 Camacho E, LoPresti MA, Bruce S. et al. The role of age in intracerebral hemorrhages. J Clin Neurosci 2015; 22 (12) 1867-1870
    CrossrefPubMedGoogle Scholar