COVID-19-associated stroke

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Editor-In-Chief: C. Michael Gibson, M.S., M.D. [1]; Associate Editor(s)-in-Chief: Parul Pahal, M.B.B.S[2], Moises Romo M.D.

Synonyms and keywords: COVID-19, SARS-CoV-2, stroke, CT scan, cerebrovascular disease, TPA, alteplase

Overview

Cerebral hemorrhage or cerebral ischemia disrupts cerebral perfusion and can lead to an acute neurologic condition, called stroke. Cerebrovascular complications have been reported in severe Coronavirus Disease 2019 (COVID-19). However, neurological complications are not very common in rapidly spreading COVID-19 which is caused by a novel coronavirus, severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2). The presenting complaints in majority of stroke patients reported in different studies were respiratory complaints (shortness of breath, cough) and non-specific constitutional symptoms such as fever, malaise, etc., and stroke developed later in the course of the disease. This is thought to be due to COVID-19-associated coagulopathy. However, there are few case reports and studies that have mentioned specific neurological presenting complaints such as altered mental status, limb weakness, and aphasia. Various non-pulmonary features are being reported as the COVID-19 understanding is unfolding with the spike of cases and continuously rising number of cases globally.

Historical Perspective

  • Mao et. al. in his study first reported neurological symptoms in COVID-19 patients hospitalized in Wuhan, China from January 16, 2020, to February 19, 2020. Neurological symptoms were reported in 78 patients out of 214 Covid-19 positive hospitalized patients. with COVID-19 in Wuhan, China. The stroke patients reported specifically were 14[1]. In this study, patients with cardiovascular risk factors who presented with severe systemic symptoms were at higher risk of stroke.
  • Yaghi et. al. retrospectively examined stroke patients admitted across different locations of NYU Langone hospital in New York. In this study, incidence of 0.9% was observed in laboratory confirmed COVID-19 positive patients included in this study. Stroke diagnosis was proved by imaging, and cryptogenic stroke was seen in most of these patients. The mortality was much higher in stroke patients who were COVID-19 positive.

Classification

  • There is no specific classification established for 'Stroke in COVID-19 patients'. It is same as the general classification of stroke.

Pathophysiology

The most common type of stroke in patients with COVID-19 is ischemic.[2]

The exact pathophysiology of 'stroke in COVID-19' is not fully understood. However, it is thought that stroke in COVID-19 could be due to one of the following pathophysiologies-

  • Sepsis induced coagulopathy in COVID-19 patients is thought to be contributing to microthromobosis. This is supported by elevation of D-dimer and C-reactive protein, which are hypercoagulability and inflammatory markers, in COVID-19 positive patients.
  • The angiotensin-converting enzyme II (ACEII) receptors are also present on the vascular endothelial cells and neural cells in the brain . These receptors expressed in the brain are responsible for sympathoadrenal system regulation, and vascular autoregulation[3]. When the virus binds to these receptors, this vascular autoregulation is hampered and can lead to elevated blood pressure, eventually leading to rupture of the cerebral vessels and intracranial hemorrhage[4]. It does so by altering the balance of renin-angiotensin system which likely triggers endothelium dysfunction, organ damage, which eventually results in stroke[5].
  • Viral Neurotropism and Neuroinvasion is another possible pathogenic mechanism for cerebrovascular accidents in COVID-19 patients. The coronaviruses usually cause mild respiratory illness, but the beta coronavirues are known to have a role in nervous system involvement[6]. The Novel coronavirus “severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2)” is a beta coronavirus, similar to severe acute respiratory syndrome coronavirus (SARS-CoV) and Middle East respiratory syndrome coronavirus (MERS-CoV)[7]. It,therefore, has infection mechanism and potential to invade the nervous system, similar to SARS-Cov and MERS-Cov[8]. The detection of virus in the cells of the brain on autopsy[9] (neural and capillary endothelial cells), and viral presence in the cerebrospinal fluid of the encephalitis patient infected with SARS-Cov-2[10] supports the neuro-invasiveness of the virus. The two possible routes are retrograde axonal transport (via nasal cavity) or hematogenous spread (via blood brain barrier endothelial cells)[9]. Once the virus reaches the brain, it attaches with the ACE II receptors.
  • Direct entry into brain tissues from cribriform plate to brain[11]. This is one of the proposed mechanism as COVID-19 positive patients also presented with anosmia and hyposmia which possibly occurs due to viral effect on olfactory bulb, which is in close proximity to cribriform plate[1]

Further investigations should be done to better understand the mechanism of Stroke in patients with COVID-19.

Causes

Coronavirus disease 2019 (COVID-19) associated stroke is caused by SARS-CoV-2.


Differentiating COVID-19-associated stroke from other Diseases

Stroke associated with COVID-19 should be differentiated from other diseases that can have similar presentation as stroke. These include-


Stroke in COVID-19 positive patients vs. Stroke in non-COVID-19 patients:

A retrospective cohort study (15th March,2020 to 19th April,2020) conducted by Yaghi et. al. in hospitalized patients in New York Healthcare systems compared stroke characteristics in patients with and without COVID-19[12]. This study included 3,556 COVID-19 positive patients, out of which 32 patients were diagnosed with ischemic stroke based on imaging. These COVID-19 positive stroke patients were then compared with 46 hospitalized stroke patients without COVID-19. Based on findings of this study-

    • Younger patient population (average age-63 years) as compared to relatively older patient population (average age-70 years) in non-COVID-19 patients.
    • Severe stroke (National Institutes of Health Stroke Scale- average score 19) as compared to non-COVID patients with lesser average score (8) seen on National Institutes of Health Stroke Scale
    • Higher D-dimer levels which point towards severe blood clotting (10,000 in this study). Relatively lower D-dimer levels (525 in this study) were seen in non-COVID patients.
    • Mostly Cryptogenic stroke seen in COVID-19 patients.
    • Increased mortality seen in COVID-19 patients.
    • Most of COVID-19 patients did not have any history of prior stroke (only 3.1% reported stroke history) as opposed to non-COVID patient group in which prior history of stroke was reported in 13%.
    • Non-COVID patients were more likely to have higher blood pressure levels.

Further studies are going on to understand the clinical characteristics specific to stroke in COVID-19 patients. It has been observed that the findings vary in different countries possibly due to racial/ethnicity variations. Since strokes have been reported in critically ill COVID-19 patients, hence, it is difficult to diagnose stroke in intubated and sedated COVID-19 patients.


Stroke in COVID-19 positive patients vs. Stroke in Influenza patients:

Out of 1916 COVID-19 patients (Emergency Department visits or were hospitalized with COVID-19) in retrospective cohort study which included patients from two academic hospitals in New York, 31 patients (1.6%) with median age 69 years, experienced acute ischemic stroke. The majority of these patients were men (58%). 8 patients (26%] had initial presentation as stroke while 23 had stroke over the course of the disease after testing positive for COVID-19.

Based on this study, the COVID-19 patients have much higher incidence of stroke when compared to influenza patients.[13]

Epidemiology and Demographics

The incidence of stroke in COVID-19 varies significantly depending on the study population.

Prevalence of stroke in patients with COVID-19
Date of publication Country Author Number of patients Severe infection Neurological symptoms Acute Cerebrovascular disease Ischemic/Hemorrhagic Stroke
April 10, 2020 Wuhan, China Mao et al.[1] 214 88 patients (41.1%), Mean age-58.2 years 78 patients (36.4%) 5 among severe [5.7%] infection group vs 1 [0.8%]) in non-severe group Ischemic-4, Hemorrhagic-1
May 29, 2020 Wuhan, China Qin et al.[14] (Retrospective cohort study) 1875 461 severe on admission 50 patients ie. 15 among severe and 35 among mild on admission (Median age-70 years), 30 males and 20 females Ischemic-90%, Hemorrhagic-10%
May 20, 2020 New York Yaghi et al.[12] (Retrospective cohort study) 3556 Stroke at the time of admission-14/32 (43.8%), eventually developed stroke during hospitalization-18 (56.2%) 32 patients (0.9%) Ischemic stroke- 32
April 28, 2020 New York city Oxley et al.[15] 5 Large vessel stroke-5, Mean age-<50 years
July 12, 2020 New York Valderrama et al. 1 (52-year old male) Ischemic stroke
Table 1. Prevalence of COVID-19-associated stroke varies in different studies


  • The incidence of stroke in hospitalized COVID-19 patients is reported to be 0.9–2%[16].majority of them being ischemic subtype. The mortality in COVID-19 positive stroke patients is reported to be 39%[1].
  • The ischemic stroke prevalence in COVID-19 patients is 1.6%.[16]
  • A New York study published in May reported that the proportion of these strokes seem to be higher in younger men.[12] Most of these strokes are large vessel ischemic strokes and are catastrophic.
  • In a retrospective observational case series of six stroke patients in a hospital in Italy, with lab confirmed COVID-19, the median age reported was 69 years. Ischemic stroke subtype was seen in 4 patients(67%) as compared to hemorrhagic which was only seen in 2 patients (33%). Vascular risk factors were seen in 5/6 patients, which included diabetes mellitus, arterial hypertension
  • In a single center retrospective study conducted in Wuhan by Qin C. et al. which included 1875 laboratory-confirmed COVID-19 patients from january 27th, 2020, to March 5th, 2020, 50 patients had history of stroke. The median age of this study group was 63 years, with stroke patients relatively older(70 years) when compared to non-stroke patients (62 years).[14]


Stroke is one of the neurological manifestations in patients with severe infection. There is limited information on COVID-19 patients with stroke who survived.

Risk Factors

Stroke in COVID-19 infected patients is seen in relatively young patients as compared to with non COVID-19 patients.

COVID-19 associated stroke in severe patients. This includes older population with comorbidities like diabetes, hypertension, etc. However, due to disparities in the stroke prevalence in different studies, no clear association has been established.

Screening

There is insufficient evidence to recommend routine screening for stroke in COVID-19 patients. However, if the patient presents with stroke, COVID-19 screening should be done.

Natural History, Complications, and Prognosis

Prognosis is generally poor for COVID-19 patients with stroke. A study reported a high proportion of these patients were admitted to the Intensive Care Unit(ICU) and required mechanical ventilation. The mortality of COVID-19 patients with stroke was much higher when compared to COVID-19 patients with no history of stroke[14].

Cerebral hemorrhage or ischemia disrupts cerebral perfusion and can lead to an acute neurologic condition, stroke. It is one of the neurological complications of SARS-Cov-2 infection, and is seen in critically ill COVID-19 patients. 5% of hospitalized COVID-19 patients with severe illness had acute stroke, with majority of patients with Ischemic stroke. The severe and critically ill patients when compared to moderate cases, had increased hypercoagulability and inflammatory markers. These patients are at higher risk for stroke. The better outcomes in critically ill patients who received prophylactic thrombolytic therapy points towards a possibility of hypercoagulability associated with COVID-19.[1]

Diagnosis

Diagnostic Study of Choice

History and Symptoms

Patient no. Onset of neurologic symptoms
Age and Gender
Neurologic Signs & Symptoms
1 On Admission 73-year old, Male Respiratory distress, fever, and altered mental status [23]
2 On Admission 83-year old, Female Fever, slurring of speech, facial droop, and reduced oral intake [23]
3 On Admission 80-year old female Left sided weakness, altered mental status, one week history of frequent falls [23]
4 On Admission 88-year old, Female An 15 minute episode of weakness and numbness of right arm and word finding difficulty [23]
5 On Admission 58-year old, Male Dense Right-sided weakness and acute onset aphasia [24]
Table 2. Reported cases of patients with COVID-19 infection and symptoms suggestive of stroke.

Physical Examination

National Institutes of Health Stroke Scale (NIHSS)
Tested item Title Response and score
1A Level of consciousness 0—Alert
1—Drowsy
2—Obtunded
3—Coma/unresponsive
1B Orientation questions (2) 0—Answers both correctly
1—Answers 1 correctly
2—Answers neither correctly
2 Gaze 0—Normal horizontal movements
1—Partial gaze palsy
2—Complete gaze palsy
3 Visual fields 0—No visual field defect
1—Partial hemianopia
2—Complete hemianopia
3—Bilateral hemianopia
4 Facial movement 0—Normal
1—Minor facial weakness
2—Partial facial weakness
3—Complete unilateral palsy
5 Motor function (arm)

a. Left

b. Right

0—No drift
1—Drift before 10 s
2—Falls before 10 s
3—No effort against gravity
4—No movement
6 Motor function (leg)

a. Left

b. Right

0—No drift
1—Drift before 5 s
2—Falls before 5 s
3—No effort against gravity
4—No movement
7 Limb ataxia 0—No ataxia
1—Ataxia in 1 limb
2—Ataxia in 2 limbs
8 Sensory 0—No sensory loss
1—Mild sensory loss
2—Severe sensory loss
9 Language 0—Norma
1—Mild aphasia
2—Severe aphasia
3—Mute or global aphasia
10 Articulation of words 0—Norma
1—Mild dysarthria
2—Severe dysarthria
11 Extinction or inattention 0—Absent
1—Mild loss (1 sensory modality lost)
2—Severe loss (2 modalities lost)
Table 3. Adapted from Lyden et al., 1994[28] American Heart Association, Inc.
  • The pre-stroke Modified Rankin Score (mRS) (Table 4) is an estimated score used to assess the patient’s pre-stroke level of function. An estimated mRS should be abstracted from current medical record documentation about the patient’s ability to perform activities of daily living prior to the hospitalization for the acute ischemic stroke event.[29]
Alberta stroke program early CT score (ASPECTS)
Area affected Score
Subganglionic Nuclei: M1 - Frontal operculum   1
M2 - Anterior temporal lobe 1
M3 - Posterior temporal lobe 1
Supraganglionic Nuclei: M4  - Anterior MCA    1
M5  - Lateral MCA   1
M6  - Posterior MCA    1
Basal Ganglia: C - Caudate 1
L - Lentiform Nucleus     1
I - Insula 1
IC - Internal Capsule 1
Table 4. Adapted from The University of Calgary ASPECT score in Accute stroke, 2020[30]
Pre-Stroke Modified Rankin Score (mRS)
Score Item tested
0 The patient had no residual symptoms.
1 The patient had no significant disability; able to carry out all activities.
2 The patient had slight disability; unable to carry out all activities but able to look after self without daily help.
3 The patient had moderate disability; requiring some external help but able to walk without the assistance of another individual.
4  The patient had moderately severe disability; unable to walk or attend to bodily functions without assistance of another individual.
5 The patient had severe disability; bedridden, incontinent, requires continuous care.
6 Unable to determine (UTD) from the medical record documentation.
Table 5. Adapted from Specifications Manual for Joint Commission National Quality Measures, 2018[29]


Laboratory Findings

  • Patients with stroke associated to COVID-19 will have a positive test for COVID-19 confirmed either through molecular tests, nucleic acid amplification test, or serological testing.

Ultrasound

X-ray

CT scan

MRI

  • MRI of the head before IV alteplase administration to exclude microbleeds is not recommended.[17]
  • Multimodal MRI of the head should be done in patients who present within 24 hours of the initiation of symptoms.[2]
  • In patients who wake up with clinical symptoms of stroke of unknown onset (more than 3 hours?), an MRI with diffusion-positive FLAIR may be useful for selecting those who can benefit from IV alteplase administration.[17]

Electrocardiogram

Treatment

Medical therapy

  • The reported cases of treatment for COVID-19-associated stroke have followed the same guidelines as patients with no COVID-19 infection. The following recommendations are mainly based on the current guidelines of management for stroke of the AHA 2019.
  • IV alteplase is always preferred over mechanical thrombectomy when there are no contraindications.[36]
  • The usefulness of anticoagulants such as thrombin inhibitors (dabigatran) and factor Xa inhibitors (rivaroxaban, apixaban, edoxaban) is not well established in the acute setting of stroke.[37]
  • The use of thrombolysis via ultrasound waves concomitant to IV fibrinolysis is not recommended.[38]
  • In patients who are 75 years of age or younger with clinical ASCVD, high-intensity statin therapy should be initiated or continued with the aim of achieving a 50% or greater reduction in LDL-C levels.*
  • A clinician-patient risk discussion is recommended before initiation of statin therapy to review net clinical benefit, weighing the potential for ASCVD risk reduction against the potential for statin-associated side effects, statin-drug interactions, and safety, while emphasizing that side effects can be addressed successfully.*
  • For patients with ischemic stroke who qualify for statin treatment, in-hospital initiation of statin therapy is reasonable.[39]*
  • Among patients already taking statins at the time of onset of ischemic stroke, continuation of statin therapy during the acute period is reasonable.*

Alteplase

Tenecteplase

Antiplatelet therapy

  • Administration of aspirin is recommended in patients with AIS within 24 to 48 hours after onset. For those treated with IV alteplase, aspirin administration is generally delayed until 24 hours later.[48]
  • The dose of aspirin is usually between 160-300mg daily.[49]
  • IV aspirin administration within 90 minutes after the start of IV alteplase is associated with symptomatic intracranial hemorrhage, for which co administration is discouraged but benefits should be assessed in each individual case.[17][50]
  • Dual antiplatelet therapy with aspirin and clopidogrel (75 mg/d, with a loading dose of 600mg) may be started within 24 hours after symptom onset and continued for 21 days in patients with no cardioembolic ischemic stroke.[51]
  • Aspirin should not substitute IV alteplase or mechanical thrombectomy in patients eligible for these therapies.

Surgery

  • The usefulness of emergency carotid endarterectomy, carotid angioplasty and stenting in the absence of an intracranial clot is not well established.[17]

Mechanical thrombectomy with a stent retriever

  • Patients should receive mechanical thrombectomy with a stent retriever if they meet all the following criteria:[53]
    1. Prestroke mRS score of 0 to 1
    2. Causative occlusion of the internal carotid artery or MCA segment 1 (M1)
    3. Age ≥18 years
    4. NIHSS score of ≥6
    5. ASPECTS of ≥6; and
    6. Treatment can be initiated within 6 hours of symptom onset

Aspiration thrombectomy

  • Direct aspiration thrombectomy as first-pass mechanical thrombectomy is recommended as noninferior to stent retriever for patients who meet all the following criteria:[54]
    1. Prestroke mRS score of 0 to 1;
    2. Causative occlusion of the internal carotid artery or M1;
    3. Age ≥18 years;
    4. NIHSS score of ≥6;
    5. ASPECTS ≥6; and
    6. Treatment initiation within 6 hours of symptom onset.

Intra arterial fibrinolysis

Other aspects of management

Primary Prevention

Secondary Prevention

References

  1. ↑ 1.0 1.1 1.2 1.3 1.4 Mao, Ling; Jin, Huijuan; Wang, Mengdie; Hu, Yu; Chen, Shengcai; He, Quanwei; Chang, Jiang; Hong, Candong; Zhou, Yifan; Wang, David; Miao, Xiaoping; Li, Yanan; Hu, Bo (2020). "Neurologic Manifestations of Hospitalized Patients With Coronavirus Disease 2019 in Wuhan, China". JAMA Neurology. 77 (6): 683. doi:10.1001/jamaneurol.2020.1127. ISSN 2168-6149.
  2. ↑ 2.0 2.1 2.2 2.3 2.4 2.5 2.6 Qureshi, Adnan I; Abd-Allah, Foad; Al-Senani, Fahmi; Aytac, Emrah; Borhani-Haghighi, Afshin; Ciccone, Alfonso; Gomez, Camilo R; Gurkas, Erdem; Hsu, Chung Y; Jani, Vishal; Jiao, Liqun; Kobayashi, Adam; Lee, Jun; Liaqat, Jahanzeb; Mazighi, Mikael; Parthasarathy, Rajsrinivas; Steiner, Thorsten; Suri, M Fareed K; Toyoda, Kazunori; Ribo, Marc; Gongora-Rivera, Fernando; Oliveira-Filho, Jamary; Uzun, Guven; Wang, Yongjun (2020). "Management of acute ischemic stroke in patients with COVID-19 infection: Report of an international panel". International Journal of Stroke. 15 (5): 540–554. doi:10.1177/1747493020923234. ISSN 1747-4930.
  3. ↑ Saavedra, Juan M. (2005). "Brain Angiotensin II: New Developments, Unanswered Questions and Therapeutic Opportunities". Cellular and Molecular Neurobiology. 25 (3–4): 485–512. doi:10.1007/s10571-005-4011-5. ISSN 0272-4340.
  4. ↑ Sharifi-Razavi, A.; Karimi, N.; Rouhani, N. (2020). "COVID-19 and intracerebral haemorrhage: causative or coincidental?". New Microbes and New Infections. 35: 100669. doi:10.1016/j.nmni.2020.100669. ISSN 2052-2975.
  5. ↑ Hess, David C.; Eldahshan, Wael; Rutkowski, Elizabeth (2020). "COVID-19-Related Stroke". Translational Stroke Research. 11 (3): 322–325. doi:10.1007/s12975-020-00818-9. ISSN 1868-4483.
  6. ↑ Arbour, Nathalie; Day, Robert; Newcombe, Jia; Talbot, Pierre J. (2000). "Neuroinvasion by Human Respiratory Coronaviruses". Journal of Virology. 74 (19): 8913–8921. doi:10.1128/JVI.74.19.8913-8921.2000. ISSN 1098-5514.
  7. ↑ Yu, Fei; Du, Lanying; Ojcius, David M.; Pan, Chungen; Jiang, Shibo (2020). "Measures for diagnosing and treating infections by a novel coronavirus responsible for a pneumonia outbreak originating in Wuhan, China". Microbes and Infection. 22 (2): 74–79. doi:10.1016/j.micinf.2020.01.003. ISSN 1286-4579.
  8. ↑ Li, Yan‐Chao; Bai, Wan‐Zhu; Hashikawa, Tsutomu (2020). "The neuroinvasive potential of SARS‐CoV2 may play a role in the respiratory failure of COVID‐19 patients". Journal of Medical Virology. 92 (6): 552–555. doi:10.1002/jmv.25728. ISSN 0146-6615.
  9. ↑ 9.0 9.1 Paniz‐Mondolfi, Alberto; Bryce, Clare; Grimes, Zachary; Gordon, Ronald E.; Reidy, Jason; Lednicky, John; Sordillo, Emilia Mia; Fowkes, Mary (2020). "Central nervous system involvement by severe acute respiratory syndrome coronavirus‐2 (SARS‐CoV‐2)". Journal of Medical Virology. 92 (7): 699–702. doi:10.1002/jmv.25915. ISSN 0146-6615.
  10. ↑ Moriguchi, Takeshi; Harii, Norikazu; Goto, Junko; Harada, Daiki; Sugawara, Hisanori; Takamino, Junichi; Ueno, Masateru; Sakata, Hiroki; Kondo, Kengo; Myose, Natsuhiko; Nakao, Atsuhito; Takeda, Masayuki; Haro, Hirotaka; Inoue, Osamu; Suzuki-Inoue, Katsue; Kubokawa, Kayo; Ogihara, Shinji; Sasaki, Tomoyuki; Kinouchi, Hiroyuki; Kojin, Hiroyuki; Ito, Masami; Onishi, Hiroshi; Shimizu, Tatsuya; Sasaki, Yu; Enomoto, Nobuyuki; Ishihara, Hiroshi; Furuya, Shiomi; Yamamoto, Tomoko; Shimada, Shinji (2020). "A first case of meningitis/encephalitis associated with SARS-Coronavirus-2". International Journal of Infectious Diseases. 94: 55–58. doi:10.1016/j.ijid.2020.03.062. ISSN 1201-9712.
  11. ↑ Baig, Abdul Mannan; Khaleeq, Areeba; Ali, Usman; Syeda, Hira (2020). "Evidence of the COVID-19 Virus Targeting the CNS: Tissue Distribution, Host–Virus Interaction, and Proposed Neurotropic Mechanisms". ACS Chemical Neuroscience. 11 (7): 995–998. doi:10.1021/acschemneuro.0c00122. ISSN 1948-7193.
  12. ↑ 12.0 12.1 12.2 Yaghi, Shadi; Ishida, Koto; Torres, Jose; Mac Grory, Brian; Raz, Eytan; Humbert, Kelley; Henninger, Nils; Trivedi, Tushar; Lillemoe, Kaitlyn; Alam, Shazia; Sanger, Matthew; Kim, Sun; Scher, Erica; Dehkharghani, Seena; Wachs, Michael; Tanweer, Omar; Volpicelli, Frank; Bosworth, Brian; Lord, Aaron; Frontera, Jennifer (2020). "SARS-CoV-2 and Stroke in a New York Healthcare System". Stroke. 51 (7): 2002–2011. doi:10.1161/STROKEAHA.120.030335. ISSN 0039-2499.
  13. ↑ Merkler, Alexander E.; Parikh, Neal S.; Mir, Saad; Gupta, Ajay; Kamel, Hooman; Lin, Eaton; Lantos, Joshua; Schenck, Edward J.; Goyal, Parag; Bruce, Samuel S.; Kahan, Joshua; Lansdale, Kelsey N.; LeMoss, Natalie M.; Murthy, Santosh B.; Stieg, Philip E.; Fink, Matthew E.; Iadecola, Costantino; Segal, Alan Z.; Cusick, Marika; Campion, Thomas R.; Diaz, Ivan; Zhang, Cenai; Navi, Babak B. (2020). "Risk of Ischemic Stroke in Patients With Coronavirus Disease 2019 (COVID-19) vs Patients With Influenza". JAMA Neurology. doi:10.1001/jamaneurol.2020.2730. ISSN 2168-6149.
  14. ↑ 14.0 14.1 14.2 Qin, Chuan; Zhou, Luoqi; Hu, Ziwei; Yang, Sheng; Zhang, Shuoqi; Chen, Man; Yu, Haihan; Tian, Dai-Shi; Wang, Wei (2020). "Clinical Characteristics and Outcomes of COVID-19 Patients With a History of Stroke in Wuhan, China". Stroke. 51 (7): 2219–2223. doi:10.1161/STROKEAHA.120.030365. ISSN 0039-2499.
  15. ↑ Oxley, Thomas J.; Mocco, J.; Majidi, Shahram; Kellner, Christopher P.; Shoirah, Hazem; Singh, I. Paul; De Leacy, Reade A.; Shigematsu, Tomoyoshi; Ladner, Travis R.; Yaeger, Kurt A.; Skliut, Maryna; Weinberger, Jesse; Dangayach, Neha S.; Bederson, Joshua B.; Tuhrim, Stanley; Fifi, Johanna T. (2020). "Large-Vessel Stroke as a Presenting Feature of Covid-19 in the Young". New England Journal of Medicine. 382 (20): e60. doi:10.1056/NEJMc2009787. ISSN 0028-4793.
  16. ↑ 16.0 16.1 Tsivgoulis, Georgios; Katsanos, Aristeidis H.; Ornello, Raffaele; Sacco, Simona (2020). "Ischemic Stroke Epidemiology During the COVID-19 Pandemic". Stroke. 51 (7): 1924–1926. doi:10.1161/STROKEAHA.120.030791. ISSN 0039-2499.
  17. ↑ 17.00 17.01 17.02 17.03 17.04 17.05 17.06 17.07 17.08 17.09 17.10 17.11 17.12 17.13 17.14 17.15 17.16 17.17 17.18 17.19 17.20 17.21 17.22 17.23 17.24 17.25 17.26 17.27 17.28 17.29 17.30 17.31 17.32 Powers, William J.; Rabinstein, Alejandro A.; Ackerson, Teri; Adeoye, Opeolu M.; Bambakidis, Nicholas C.; Becker, Kyra; Biller, José; Brown, Michael; Demaerschalk, Bart M.; Hoh, Brian; Jauch, Edward C.; Kidwell, Chelsea S.; Leslie-Mazwi, Thabele M.; Ovbiagele, Bruce; Scott, Phillip A.; Sheth, Kevin N.; Southerland, Andrew M.; Summers, Deborah V.; Tirschwell, David L. (2019). "Guidelines for the Early Management of Patients With Acute Ischemic Stroke: 2019 Update to the 2018 Guidelines for the Early Management of Acute Ischemic Stroke: A Guideline for Healthcare Professionals From the American Heart Association/American Stroke Association". Stroke. 50 (12). doi:10.1161/STR.0000000000000211. ISSN 0039-2499.
  18. ↑ Yew KS, Cheng EM (April 2015). "Diagnosis of acute stroke". Am Fam Physician. 91 (8): 528–36. PMID 25884860.
  19. ↑ Bouchez, Laurie; Sztajzel, Roman; Vargas, Maria Isabel; Machi, Paolo; Kulcsar, Zsolt; Poletti, Pierre-Alexandre; Pereira, Vitor Mendes; Lövblad, Karl-Olof (2017). "CT imaging selection in acute stroke". European Journal of Radiology. 96: 153–161. doi:10.1016/j.ejrad.2016.10.026. ISSN 0720-048X.
  20. ↑ 20.0 20.1 Hernández-Pérez M, Pérez de la Ossa N, Aleu A, Millán M, Gomis M, Dorado L; et al. (2014). "Natural history of acute stroke due to occlusion of the middle cerebral artery and intracranial internal carotid artery". J Neuroimaging. 24 (4): 354–8. doi:10.1111/jon.12062. PMID 24251821.
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  30. ↑ 30.0 30.1 "Home".
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  38. ↑ Nacu, Aliona; Kvistad, Christopher E.; Naess, Halvor; Øygarden, Halvor; Logallo, Nicola; Assmus, Jörg; Waje-Andreassen, Ulrike; Kurz, Kathinka D.; Neckelmann, Gesche; Thomassen, Lars (2017). "NOR-SASS (Norwegian Sonothrombolysis in Acute Stroke Study)". Stroke. 48 (2): 335–341. doi:10.1161/STROKEAHA.116.014644. ISSN 0039-2499.
  39. ↑ Sanossian, Nerses; Saver, Jeffrey L.; Liebeskind, David S.; Kim, Doojin; Razinia, Tannaz; Ovbiagele, Bruce (2006). "Achieving Target Cholesterol Goals After Stroke". Archives of Neurology. 63 (8): 1081. doi:10.1001/archneur.63.8.1081. ISSN 0003-9942.
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  43. ↑ Powers, William J.; Derdeyn, Colin P.; Biller, José; Coffey, Christopher S.; Hoh, Brian L.; Jauch, Edward C.; Johnston, Karen C.; Johnston, S. Claiborne; Khalessi, Alexander A.; Kidwell, Chelsea S.; Meschia, James F.; Ovbiagele, Bruce; Yavagal, Dileep R. (2015). "2015 American Heart Association/American Stroke Association Focused Update of the 2013 Guidelines for the Early Management of Patients With Acute Ischemic Stroke Regarding Endovascular Treatment". Stroke. 46 (10): 3020–3035. doi:10.1161/STR.0000000000000074. ISSN 0039-2499.
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  52. ↑ Albers, Gregory W.; Marks, Michael P.; Kemp, Stephanie; Christensen, Soren; Tsai, Jenny P.; Ortega-Gutierrez, Santiago; McTaggart, Ryan A.; Torbey, Michel T.; Kim-Tenser, May; Leslie-Mazwi, Thabele; Sarraj, Amrou; Kasner, Scott E.; Ansari, Sameer A.; Yeatts, Sharon D.; Hamilton, Scott; Mlynash, Michael; Heit, Jeremy J.; Zaharchuk, Greg; Kim, Sun; Carrozzella, Janice; Palesch, Yuko Y.; Demchuk, Andrew M.; Bammer, Roland; Lavori, Philip W.; Broderick, Joseph P.; Lansberg, Maarten G. (2018). "Thrombectomy for Stroke at 6 to 16 Hours with Selection by Perfusion Imaging". New England Journal of Medicine. 378 (8): 708–718. doi:10.1056/NEJMoa1713973. ISSN 0028-4793.
  53. ↑ Goyal, Mayank; Menon, Bijoy K; van Zwam, Wim H; Dippel, Diederik W J; Mitchell, Peter J; Demchuk, Andrew M; Dávalos, Antoni; Majoie, Charles B L M; van der Lugt, Aad; de Miquel, Maria A; Donnan, Geoffrey A; Roos, Yvo B W E M; Bonafe, Alain; Jahan, Reza; Diener, Hans-Christoph; van den Berg, Lucie A; Levy, Elad I; Berkhemer, Olvert A; Pereira, Vitor M; Rempel, Jeremy; Millán, Mònica; Davis, Stephen M; Roy, Daniel; Thornton, John; Román, Luis San; Ribó, Marc; Beumer, Debbie; Stouch, Bruce; Brown, Scott; Campbell, Bruce C V; van Oostenbrugge, Robert J; Saver, Jeffrey L; Hill, Michael D; Jovin, Tudor G (2016). "Endovascular thrombectomy after large-vessel ischaemic stroke: a meta-analysis of individual patient data from five randomised trials". The Lancet. 387 (10029): 1723–1731. doi:10.1016/S0140-6736(16)00163-X. ISSN 0140-6736.
  54. ↑ 54.0 54.1 Turk, Aquilla S; Siddiqui, Adnan; Fifi, Johanna T; De Leacy, Reade A; Fiorella, David J; Gu, Eugene; Levy, Elad I; Snyder, Kenneth V; Hanel, Ricardo A; Aghaebrahim, Amin; Woodward, B Keith; Hixson, Harry R; Chaudry, Mohammad I; Spiotta, Alejandro M; Rai, Ansaar T; Frei, Donald; Almandoz, Josser E Delgado; Kelly, Mike; Arthur, Adam; Baxter, Blaise; English, Joey; Linfante, Italo; Fargen, Kyle M; Mocco, J (2019). "Aspiration thrombectomy versus stent retriever thrombectomy as first-line approach for large vessel occlusion (COMPASS): a multicentre, randomised, open label, blinded outcome, non-inferiority trial". The Lancet. 393 (10175): 998–1008. doi:10.1016/S0140-6736(19)30297-1. ISSN 0140-6736.
  55. ↑ Guluma, Kama Z.; Liebeskind, David S.; Raman, Rema; Rapp, Karen S.; Ernstrom, Karin B.; Alexandrov, Andrei V.; Shahripour, Reza B.; Barlinn, Kristian; Starkman, Sidney; Grunberg, Ileana D.; Hemmen, Thomas M.; Meyer, Brett C.; Alexandrov, Anne W. (2015). "Feasibility and Safety of Using External Counterpulsation to Augment Cerebral Blood Flow in Acute Ischemic Stroke—The Counterpulsation to Upgrade Forward Flow in Stroke (CUFFS) Trial". Journal of Stroke and Cerebrovascular Diseases. 24 (11): 2596–2604. doi:10.1016/j.jstrokecerebrovasdis.2015.07.013. ISSN 1052-3057.
  56. ↑ Anderson, Craig S.; Arima, Hisatomi; Lavados, Pablo; Billot, Laurent; Hackett, Maree L.; Olavarría, Verónica V.; Muñoz Venturelli, Paula; Brunser, Alejandro; Peng, Bin; Cui, Liying; Song, Lily; Rogers, Kris; Middleton, Sandy; Lim, Joyce Y.; Forshaw, Denise; Lightbody, C. Elizabeth; Woodward, Mark; Pontes-Neto, Octavio; De Silva, H. Asita; Lin, Ruey-Tay; Lee, Tsong-Hai; Pandian, Jeyaraj D.; Mead, Gillian E.; Robinson, Thompson; Watkins, Caroline (2017). "Cluster-Randomized, Crossover Trial of Head Positioning in Acute Stroke". New England Journal of Medicine. 376 (25): 2437–2447. doi:10.1056/NEJMoa1615715. ISSN 0028-4793.
  57. ↑ Roffe, Christine; Nevatte, Tracy; Sim, Julius; Bishop, Jon; Ives, Natalie; Ferdinand, Phillip; Gray, Richard (2017). "Effect of Routine Low-Dose Oxygen Supplementation on Death and Disability in Adults With Acute Stroke". JAMA. 318 (12): 1125. doi:10.1001/jama.2017.11463. ISSN 0098-7484.
  58. ↑ Saxena, Manoj; Young, Paul; Pilcher, David; Bailey, Michael; Harrison, David; Bellomo, Rinaldo; Finfer, Simon; Beasley, Richard; Hyam, Jonathan; Menon, David; Rowan, Kathryn; Myburgh, John (2015). "Early temperature and mortality in critically ill patients with acute neurological diseases: trauma and stroke differ from infection". Intensive Care Medicine. 41 (5): 823–832. doi:10.1007/s00134-015-3676-6. ISSN 0342-4642.
  59. ↑ Schrader, Joachim; Lüders, Stephan; Kulschewski, Anke; Berger, Jürgen; Zidek, Walter; Treib, Johannes; Einhäupl, Karl; Diener, Hans Christoph; Dominiak, Peter (2003). "The ACCESS Study". Stroke. 34 (7): 1699–1703. doi:10.1161/01.STR.0000075777.18006.89. ISSN 0039-2499.
  60. ↑ Dennis M, Lewis S, Cranswick G, Forbes J (January 2006). "FOOD: a multicentre randomised trial evaluating feeding policies in patients admitted to hospital with a recent stroke". Health Technol Assess. 10 (2): iii–iv, ix–x, 1–120. doi:10.3310/hta10020. PMID 16409880.
  61. ↑ Meader, N.; Moe-Byrne, T.; Llewellyn, A.; Mitchell, A. J. (2013). "Screening for poststroke major depression: a meta-analysis of diagnostic validity studies". Journal of Neurology, Neurosurgery & Psychiatry. 85 (2): 198–206. doi:10.1136/jnnp-2012-304194. ISSN 0022-3050.


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