STROKE IN COVID-19 PATIENTS: A SCOPING REVIEW

a scoping review, according to the framework proposed by the Joanna Briggs Institute, using the LILACS, MEDLINE, WoS, EMBASE, CINAHL and SCOPUS databases, from April to September 2020. The following keywords were used: coronavirus infections, stroke, nervous system diseases and inpatients, based on the Medical Subject Headings.

Results:

24 studies that evidenced specific clinical symptoms of stroke such as dysarthria, facial paralysis, sensory deficit, headache, hemiparesis and ataxia in patients with COVID-19 were included. The association between stroke and COVID-19 was found by the following exams: C-reactive protein, D-dimer, computed tomography and, magnetic resonance, among others, as well as by care procedures focused on the findings in the exams, associated with three clinical outcomes, based on the brain ischemia zone affected and the time of viral manifestation of each patient.

Conclusion:

the specific clinical manifestations of patients who suffered a stroke after COVID-19 were mapped, as well as diagnostic procedures and therapies used, in addition to identifying neurological damage based on the clinical outcome of these patients.

DESCRIPTORS:
Coronavirus infections; Stroke; Academic review; Hospital care; Adult's health

Databases	Search strategy
MEDLINE	(inpatients) AND ("coronavirus infections" AND "nervous system diseases e inpatients") AND (stroke) OR (inpatients) AND ("coronavirus infections") AND (stroke)
Embase	(inpatients) AND ("coronavirus infections" AND "nervous system diseases e inpatients") AND (stroke) OR (inpatients) AND ((("coronavirus infections"))) AND ((("stroke")))
SCOPUS and WoS	(TITLE-ABS-KEY (inpatients) AND ("coronavirus infections" AND "nervous system diseases e inpatients") AND (stroke) OR TITLE-ABS-KEY (inpatients) AND ("coronavirus infections") AND (stroke)
CINAHL	(inpatients) AND ("coronavirus infections" AND "nervous system diseases e inpatients") AND (stroke) OR (inpatients) AND ("coronavirus infections") AND (stroke)

Authors/ Countries	Titles	Journals	Designs Samples Stroke cases
Oxley et al.1515. Oxley TJ, Mocco J, Majidi S, Kellner CP, Shoirah H, Singh IP, et al. Large-vessel stroke as a presenting feature of Covid-19 in the young. N Engl J Med [Internet]. 2020 [cited 2020 June 29];382(20):e60. Available from: https://doi.org/10.1056/NEJMc2009787 https://doi.org/10.1056/NEJMc2009787... United States	Large-vessel stroke as a presenting feature of COVID-19 in the young	N Engl J Med	Case report
			Five patients
			Age mean: 40 years old
			Clinical data: 60% COVID-19 and stroke; 40% only stroke
			Gender: 80% men
			Evolution: Severe stroke
Co et al.1616. Co COC, Yu JRT, Laxamana LC, David-Ona DIA. Intravenous thrombolysis for stroke in a COVID-19 positive filipino patient, a case report. J Clin Neurosci [Internet]. 2020 [cited 2020 June 29];77:234-6. Available from: https://doi.org/10.1016/j.jocn.2020.05.006 https://doi.org/10.1016/j.jocn.2020.05.0... Philippines	Intravenous thrombolysis for stroke in a COVID-19 positive Filipino patient, a case report	J Clin Neurosci	Case report
			One female patient
			Age: 62 years old
			Female gender
			Clinical data: COVID-19 and stroke
			Evolution: acute neurological complications
Lodigiani et al.1717. Lodigiani C, Lapichino G, Carenzo L, Cecconi M, Ferrazzi P, Sebastian T, et al. Venous and arterial thromboembolic complications in COVID-19 patients admitted to an academic hospital in Milan, Italy. Thromb Res [Internet]. 2020 [cited 2020 June 29];191:9-14. Available from: https://doi.org/10.1016/j.thromres.2020.04.024 https://doi.org/10.1016/j.thromres.2020.... Italy	Venous and arterial thromboembolic complications in COVID-19 patients admitted to an academic hospital in Milan, Italy	Thromb Res	Retrospective Cohort
			388 patients
			Age mean: 66 years old
			Clinical data: 5.2% stroke
			Gender: 68% men and 32% women
			Evolution: thromboembolic complications and DIC*
Moshayedi et al.1818. Moshayedi P, Ryan TE, Mejia LLP, Nour M, Liebeskind DS. Triage of Acute ischemic stroke in confirmed COVID-19: large vessel occlusion associated with coronavirus infection. Front Neurol [Internet]. 2020 [cited 2020 Jul 19];11:353. Available from: https://doi.org/10.3389/fneur.2020.00353 https://doi.org/10.3389/fneur.2020.00353... United States	Triage of Acute ischemic stroke in confirmed COVID-19: large vessel occlusion associated with coronavirus infection	Front Neurol	Case report
			One male patient
			Age: 80 years old
			Male gender
			Clinical data: COVID-19 and stroke
			Evolution: intracranial hemorrhage, heart failure, cardiogenic shock and bilateral limb ischemia
Qureshi et al.1919. Qureshi AI, Abd-Allah F, Al-Senani F, Aytac E, Borhani-Haghighi A, Ciccone A, et al. Management of acute ischemic stroke in patients with COVID-19 infection: report of an international panel. Int J Stroke [Internet]. 2020 [cited 2020 Jul 19];15(5):540-54. Available from: https://doi.org/10.1177/1747493020923234 https://doi.org/10.1177/1747493020923234... United States	Management of acute ischemic stroke in patients with COVID-19 infection: report of an international panel	Int J Stroke	Theoretical study
Tunç et al.2020. Tunç A, Ünlübaş Y, Alemdar M, Akyüz E. Coexistence of COVID-19 and acute ischemic stroke report of four cases. J Clin Neurosci [Internet]. 2020 [cited 2020 Jul 19];77:227-9. Available from: https://doi.org/10.1016/j.jocn.2020.05.018 https://doi.org/10.1016/j.jocn.2020.05.0... Peru	Coexistence of COVID-19 and acute ischemic stroke report of four cases	J Clin Neurosci	Case report
			Four (04) patients
			Age mean: 65 years old
			Gender: 50% men and 50% women
			Clinical data: COVID-19 and stroke 100%
			Evolution: anterior artery infarction and arrhythmia
Valderrama et al.2121. Valderrama EV, Humbert K, Lord A, Frontera J, Yaghi S. Severe acute respiratory syndrome coronavirus 2 infection and ischemic stroke. Stroke [Internet]. 2020 [cited 2020 Jul 26];51(7):e124-7. Available from: https://doi.org/10.1161/strokeaha.120.030153 https://doi.org/10.1161/strokeaha.120.03... United States	Severe acute respiratory syndrome coronavirus 2 infection and ischemic stroke	Stroke	Case report
			One male patient
			Age: 52 years old
			Gender: male
			Clinical data: COVID-19 and stroke
			Evolution: hemorrhage
Rothstein et al.2222. Rothstein A, Oldridge O, Schwennesen H, Do D, Cucchiara BL. Acute Cerebrovascular Events in Hospitalized COVID-19 Patients. Stroke [Internet]. 2020 [cited 2020 Jul 26];51(9):e219-22. https://doi.org/10.1161/strokeaha.120.030995 https://doi.org/10.1161/strokeaha.120.03... United States	Acute Cerebrovascular Events in Hospitalized COVID-19 Patients	Stroke	Retrospective and observational
			844 patients
			Age mean: 59 years old
			Clinical data: 2.4% ischemic stroke, 0.9% hemorrhagic stroke
			Gender: 52% female
			Outcome: hemorrhages and DIC*
Lin et al.2323. Lin C, Arevalo YA, Nanavati HD, Lin DM. Racial differences and an increased systemic inflammatory response are seen in patients with COVID-19 and ischemic stroke. Brain Behav Immun Health [Internet]. 2020 [cited 2020 Jul 26];8:100137. Available from: https://doi.org/10.1016/j.bbih.2020.100137 https://doi.org/10.1016/j.bbih.2020.1001... United States	Racial differences and an increased systemic inflammatory response are seen in patients with COVID-19 and ischemic stroke	Brain, Behav Immun Health	Cross-sectional, observational
			60 patients
			Age mean: 58 years old
			Gender: 55% female
			Clinical data: 15% COVID-19
			Evolution: increase in mortality and in hospital stay
Avula et al.2424. Avula A, Nalleballe K, Narula N, Sapozhnikov S, Dandu V, Toom S, et al. COVID-19 presenting as stroke. Brain Behav Immun [Internet]. 2020 [cited 2020 Sept 11];87:115-9. Available from: https://doi.org/10.1016/j.bbi.2020.04.077 https://doi.org/10.1016/j.bbi.2020.04.07... United States	COVID-19 presenting as stroke	Brain, Behav Immun Health	Retrospective
			Four patients
			Age mean: 81 years old
			Gender: 75% female
			Clinical data: Stroke
			Evolution: neuropsychomotor impairment
Benussi et al.2525. Benussi A, Pilotto A, Premi E, Libri I, Giunta M, Agosti C, et al. Clinical characteristics and outcomes of inpatients with neurologic disease and COVID-19 in Brescia, Lombardy, Italy. Neurology [Internet]. 2020 [cited 2020 Sept 11];95(7):e910-20. Available from: https://doi.org/10.1212/WNL.0000000000009848 https://doi.org/10.1212/WNL.000000000000... Italy	Clinical characteristics and outcomes of inpatients with neurologic disease and COVID-19 in Brescia, Lombardy, Italy	Neurology	Retrospective Cohort
			173 patients
			Age mean: 72 years old
			Gender: 53.8% male
			Clinical data: 34.2% stroke
			Evolution: high intra-hospital mortality
Hernández-Fernández et al.2626. Hernández-Fernández F, Sandoval VH, Barbella-Aponte RA, Collado-Jiménez R, Ayo-Martín Ó, Barrena C, et al. Cerebrovascular disease in patients with COVID-19: neuroimaging, histological and clinical description. Brain [Internet]. 2020 [cited 2020 Sept 11];143(10):3089-103. Available from: https://doi.org/10.1093/brain/awaa239 https://doi.org/10.1093/brain/awaa239... Spain	Cerebrovascular disease in patients with COVID-19: neuroimaging, histological and clinical description	Brain	Retrospective
			1,683 patients
			Age mean: 67 years old
			Gender: 78% male
			Clinical data: 74.2% stroke
			Evolution: hypercoagulability and systemic complications
Grewal et al.2727. Grewal P, Pinna P, Hall JP, Dafer RM, Tavarez T, Pellack DR, et al. Acute ischemic stroke and COVID-19: experience from a comprehensive stroke center in Midwest US. Front Neurol [Internet]. 2020 [cited 2020 Sept 11];11:910. Available from: https://doi.org/10.3389/fneur.2020.00910 https://doi.org/10.3389/fneur.2020.00910... United States	Acute Ischemic Stroke and COVID-19: Experience from a Comprehensive Stroke Center in Midwest US	Frontiers in Neurology	Retrospective and observational
			650 patients
			Age mean: 61 years old
			Gender: 46% male
			Clinical data: 2% stroke
			Evolution: high inflammatory activity and coagulability markers
Hanif et al.2828. Hanif A, Khan S, Mantri N, Hanif S, Saleh M, Alla Y, et al. Thrombotic complications and anticoagulation in COVID-19 pneumonia: a New York City hospital experience. Ann Hematol [Internet]. 2020 [cited 2020 Sept 11];99(10):2323-8. Available from: https://doi.org/10.1007/s00277-020-04216-x https://doi.org/10.1007/s00277-020-04216... United States	Thrombotic complications and anticoagulation in COVID-19 pneumonia: a New York City hospital experience	Ann Hematol Oncol	Retrospective
			1,308 patients
			Age mean: 62 years old
			Gender: 62.3% male
			Clinical data: 1.19% stroke
			Evolution: need for transfusional support and death
Jain et al.2929. Jain R, Young M, Dogra S, Kennedy H, Nguyen V, Jones 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 [Internet]. 2020 [cited 2020 Sept 11];414:116923. Available from: https://doi.org/10.1016/j.jns.2020.116923 https://doi.org/10.1016/j.jns.2020.11692... United States	COVID-19 related neuroimaging findings: A signal of thromboembolic complications and a strong prognostic marker of poor patient outcome	J Neurol Sci	Retrospective
			3,218 patients
			Age mean: 66 years old
			Gender: 60.7% male
			Clinical data: 1.1% stroke
			Evolution: intracranial hemorrhage and death
Yaghi et al.3030. Yaghi S, Ishida K, Torres J, Grory BM, Raz E, Humbert K, et al. SARS-CoV-2 and stroke in a New York healthcare system. Stroke [Internet]. 2020 [cited 2020 Sept 18];51:2002-11. Available from: https://doi.org/10.1161/strokeaha.120.030335 https://doi.org/10.1161/strokeaha.120.03... United States	SARS-CoV-2 and Stroke in a New York Healthcare System	Stroke	Retrospective and observational
			3,556 patients
			Age mean: 63 years old
			Gender: 71.9% male
			Clinical data: 0.9% stroke
			Evolution: elevated D-dimer and high mortality
Shahjouei et al.3131. Shahjouei S, Naderi S, Li J, Khan A, Chaudhary D, Farahmand G, et al. Risk of stroke in hospitalized SARS-CoV-2 infected patients: a multinational study. EBioMedicine [Internet]. 2020 [cited 2020 Sept 18];59:102939. Available from: https://doi.org/10.1016/j.ebiom.2020.102939 https://doi.org/10.1016/j.ebiom.2020.102... Spain	Risk of stroke in hospitalized SARS-CoV-2 infected patients: A multinational study	EBioMedicine	Observational, multicentric and multinational
			26,175 patients
			Age mean: 67 years old
			Gender: 47% female
			Clinical data: 0.9% stroke
			Evolution: need for mechanical ventilation and ischemic heart problems
Liu et al.3232. Liu J, Zhang S, Wu Z, Shang Y, Dong X, Li G, et al. Clinical outcomes of COVID-19 in Wuhan, China: a large cohort study. Ann Intensive Care [Internet]. 2020 [cited 2020 Sept 21];10(1):99. Available from: https://doi.org/10.1186/s13613-020-00706-3 https://doi.org/10.1186/s13613-020-00706... Germany	Clinical outcomes of COVID-19 in Wuhan, China: a large cohort study	Ann Intensive Care	Retrospective Cohort
			1,190 patients
			Age mean: 57 years old
			Gender: 46.6% female
			Clinical data: 3.3% stroke
			Evolution: need for mechanical ventilation and intra-hospital death
Yamakawa et al.3333. Yamakawa M, Kuno T, Mikami T, Takagi H, Gronseth G. Clinical characteristics of stroke with COVID-19: a systematic review and meta-analysis. J Stroke Cerebrovasc Dis [Internet]. 2020 [cited 2020 Sept 18];29(12):105288. Available from: https://doi.org/10.1016/j.jstrokecerebrovasdis.2020.105288 https://doi.org/10.1016/j.jstrokecerebro... United Kingdom	Clinical Characteristics of Stroke with COVID-19: A Systematic Review and Meta-Analysis	Int J Stroke Cerebrovasc. Dis	Theoretical
			215 articles
			4.6% stroke
Zhang et al.3434. Zhang L, Sun W, Wang Y, Wang X, Liu Y, Zhao S, et al. Clinical course and mortality of stroke patients with coronavirus disease 2019 in Wuhan, China. Stroke [Internet]. 2020 [cited 2020 Sept 18];51(9):2674-82. Available from: https://doi.org/10.1161/strokeaha.120.030642 https://doi.org/10.1161/strokeaha.120.03... United States	Clinical Course and Mortality of Stroke Patients with Coronavirus Disease 2019 in Wuhan, China	Stroke	A series of unicentric cases
			709 patients
			Age mean: 55 years old
			Gender: 45% male
			Clinical data: 8% stroke
			Evolution: high mortality
Siegler et al.3535. Siegler JE, Cardona CP, Arenillas JF, Talavera B, Guillen AN, Chavarría-Miranda A, et al. Cerebrovascular events and outcomes in hospitalized patients with COVID-19: The SVIN COVID-19 Multinational Registry. Int J Stroke [Internet]. 2020 [cited 2020 Sept 18];16(4):437-47. Available from: https://doi.org/10.1177/1747493020959216 https://doi.org/10.1177/1747493020959216... United States	Cerebrovascular events and outcomes in hospitalized patients with COVID-19: The SVIN COVID-19 Multinational Registry	Int l J Stroke	Observational and retrospective cohort study
			14,483 patients
			Age mean: 60 years old
			Gender: 55.8% female
			Clinical data: 1.13% stroke
			Evolution: long-term thrombotic complications
Studart-neto et al.3636. Studart-Neto A, Guedes BF, Tuma RL, Camelo FAE, Kubota GT, Lepsen BD, et al. Neurological consultations and diagnoses in a large, dedicated COVID-19 university hospital. Arq Neuropsiquiatr [Internet]. 2020 [cited 2020 Sept 18];78(8):494-500. Available from: https://doi.org/10.1590/0004-282x20200089 https://doi.org/10.1590/0004-282x2020008... Brazil	Neurological consultations and diagnoses in a large, dedicated COVID-19 university hospital	Arq Neuropsiquiatria	Retrospective study
			1,208 patients
			Age mean: 57 years old
			Gender: 61.8% male
			Clinical data: 16.7% stroke
			Evolution: severe neurological complications, respiratory failure and death
Teo et al.3737. Teo KC, Leung WCY, Wong YK, Liu RKC, Chan AHY, Choi OMY, et al. Delays in stroke onset to hospital arrival time during COVID-19. Stroke [Internet]. 2020 [cited 2020 Sept 18];51(7):2228-31. Available from: https://doi.org/10.1161/strokeaha.120.030105 https://doi.org/10.1161/strokeaha.120.03... United States	Delays in Stroke Onset to Hospital Arrival Time During COVID-19	Stroke	Retrospective study
			386 patients
			Age mean: 70 years old
			Gender: 43.8% male
			Clinical data: 9.1% stroke
			Evolution: increase in mortality
Nguyen-Huynh et al.3838. Nguyen-Huynh MN, Tang XN, Vinson DR, Flint AC, Alexander JG, Meighan M, et al. Acute stroke presentation, care, and outcomes in community hospitals in Northern California during the COVID-19 pandemic. Stroke [Internet]. 2020 [cited 2020 Sept 18];51(10):2918-24. Available from: https://doi.org/10.1161/strokeaha.120.031099 https://doi.org/10.1161/strokeaha.120.03... United States	Acute Stroke Presentation, Care, and Outcomes in Community Hospitals in Northern California During the COVID-19 Pandemic	Stroke	Cohort study
			9,120 patients
			Age mean: 65 years old
			Gender: 52.9% female
			Clinical data: 11.6% stroke
			Evolution: increase in mortality

Personal Morbidity History
Asthma; Transient ischemic attack; Cancer; Type I diabetes mellitus; Type II diabetes mellitus; Dyslipidemia; Ischemic heart disease; Coronary artery disease; Chronic liver disease; Chronic kidney disease; Chronic obstructive pulmonary disease.	Carotid stenosis; Atrial fibrillation; Hypercholesterolemia, Hypertension; Hyperlipidemia; Stroke history; Immunodeficiency; Acute myocardial infarction; Urinary tract infection; Heart failure.	Obesity; Smoking pneumonia; Acute coronary syndrome; Smoking; Pulmonary/venous thromboembolism; Tuberculosis; Substance abuse.
Clinical manifestations
Specific: Aphasia; Change in the level of consciousness; Ataxia; Coma; Confusion; Sensory deficit; Facial breakdown; Breakdown in speech; Dysarthria; Dysphagia; Altered mental state; Hemianopsia; Hemihypoesthesia; Hemiplegia in upper or lower limbs mainly on the right side; Hemiparesis; Disordered movements; Facial paralysis; Dizziness.
Nonspecific: Headache; Nasal congestion; Nasal discharges; Seizure; Delirium; Dyspnea; Sore throat; Chest pain; Sneezing; Fatigue; Fever; Hemoptysis; Hypogeusia; Respiratory failure; Myalgia; Nausea; Sialorrhea; Syncope; Gastrointestinal symptoms; Eye symptoms; Tachycardia; Cough; Dizziness; Vomiting.
Recommendations for biochemical examinations
Reduced albumin; Recent and increased antiphospholipid (anticardiolipin) antibodies; Increased aspartate; Altered and increased white cell count; Increased creatinine.	Increased glucose; Reduced hematocrit; Decreased hemoglobin; Increased IL-6; Reduced low density lipoprotein; Increased neutrophil; High C-reactive protein; High ferritin; High erythrocyte sedimentation rate.	Increased partial prothrombin action time; Increased partial thromboplastin action time; Increased cardiac troponins; Increased troponin T; Equivalent unit of fibrinogen (D-dimer) elevated at the beginning.
Recommendation for imaging examinations
Skull Computed Tomography with loss of gray-white differentiation in the left occipital and parietal lobes. Internal carotid occlusion and penumbra area. Moderate hypodensity on the right frontal side. On the chest: bilateral ground-glass opacity.
Magnetic Resonance Imaging (infarction in the middle temporal artery) and vascular infarction in one, two or three areas.

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E-mail: textoecontexto@contato.ufsc.br

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[1] CORRESPONDING AUTHOR
João Cruz Neto enfjcncruz@gmail.com