ABSTRACT

Introduction:

Although the 2019 severe acute respiratory syndrome coronavirus 2 infection (SARS-CoV-2, COVID-19) pandemic poses new challenges to the healthcare system to provide support for thousands of patients, there is special concern about common medical emergencies, such as stroke, that will continue to occur and will require adequate treatment. The allocation of both material and human resources to fight the pandemic cannot overshadow the care for acute stroke, a time-sensitive emergency that with an inefficient treatment will further increase mortality and long-term disability.

Objective:

This paper summarizes the recommendations from the Scientific Department on Cerebrovascular Diseases of the Brazilian Academy of Neurology, the Brazilian Society of Cerebrovascular Diseases and the Brazilian Society of Neuroradiology for management of acute stroke and urgent neuro-interventional procedures during the COVID-19 pandemic, including proper use of screening tools, personal protective equipment (for patients and health professionals), and patient allocation.

Keywords:
neurointerventional treatment; coronavirus infections; stroke

RESUMO

Introdução:

A pandemia causada pelo novo coronavírus da síndrome respiratória aguda grave 2 (SARS-CoV-2, COVID-19) apresenta novos e importantes desafios à gestão de saúde no Brasil. Além da difícil missão de prestar atendimento aos milhares de pacientes infectados pelo COVID-19, os sistemas de saúde têm que manter a assistência às emergências médicas comuns em períodos sem pandemia, tais como o acidente vascular cerebral (AVC), que continuam ocorrendo e requerem tratamento com presteza e eficiência. A alocação de recursos materiais e humanos para o enfrentamento à pandemia não pode comprometer o atendimento ao AVC agudo, uma emergência cujo tratamento é tempo-dependente e se não realizado implica em importante impacto na mortalidade e incapacitação a longo prazo.

Objetivo:

Este trabalho resume as recomendações do Departamento Científico de Doenças Cerebrovasculares da Academia Brasileira de Neurologia, da Sociedade Brasileira de Doenças Cerebrovasculares e da Sociedade Brasileira de Neurorradiologia para o tratamento do AVC agudo e para a realização de procedimentos de neurointervenção urgentes durante a pandemia de COVID-19, incluindo o uso adequado de ferramentas de triagem e equipamentos de proteção pessoal (para pacientes e profissionais de saúde), além da alocação apropriada de pacientes.

Palavras-chave:
neurointervenção; infecções por coronavirus; acidente vascular cerebral

INTRODUCTION

The recent outbreak caused by the severe acute respiratory syndrome coronavirus 2 infection (SARS-CoV-2) and its high transmission rates resulted in a situation that was officially declared as pandemic by the World Health Organization (WHO) on March 11, 2020¹1. Mahase E. Covid-19: WHO declares pandemic because of "alarming levels" of spread, severity, and inaction. BMJ. 2020 Mar;368:m1036. https://doi.org/10.1136/bmj.m1036
https://doi.org/https://doi.org/10.1136/... . Presently, there have been over 3 million confirmed cases and over 200,000 deaths from SARS-CoV-2 Coronavirus Disease 2019 (COVID-19) worldwide¹1. Mahase E. Covid-19: WHO declares pandemic because of "alarming levels" of spread, severity, and inaction. BMJ. 2020 Mar;368:m1036. https://doi.org/10.1136/bmj.m1036
https://doi.org/https://doi.org/10.1136/... . According to the Brazilian Department of Health, the first case of COVID-19 in Brazil was confirmed on February 26, 2020, and reached the community transmission stage on March 20, 2020. The epidemic peak in Brazil has been estimated for late April and early May 2020²2. Brasil. Ministério da Saúde. Painel de casos de doença pelo coronavírus 2019 (COVID-19) no Brasil pelo Ministério da Saúde. 2020. [cited 2020 Apr 17]. Available from: Available from: https://covid.saude.gov.br/
https://covid.saude.gov.br/... .

All regions of Brazil have been affected, leading to new challenges to ensure adequate care for suspected or confirmed cases of COVID-19 and the safety of health professionals and other patients, reducing their exposure to the risk of infection and safeguarding the care of other potentially life-threatening conditions²2. Brasil. Ministério da Saúde. Painel de casos de doença pelo coronavírus 2019 (COVID-19) no Brasil pelo Ministério da Saúde. 2020. [cited 2020 Apr 17]. Available from: Available from: https://covid.saude.gov.br/
https://covid.saude.gov.br/... .

While the pandemic poses new challenges to the healthcare system to provide support for thousands of COVID-19 cases (often requiring hospitalization and intensive care admission), common medical emergencies, such as stroke, should also be considered, because they will continue to occur and require adequate treatment. The allocation of both material and human resources to fight the pandemic cannot overshadow the care for those time-sensitive emergencies, because in the event of inefficient treatment, they will further increase mortality, long-term disability, and costs.

Although we have few data to develop a robust and consistent guideline and acknowledging that recommendations may need to be adapted according to the pandemic evolution and each healthcare facility specificities, the purpose of this expert joint consensus of the Scientific Department on Cerebrovascular Diseases of the Brazilian Academy of Neurology, the Brazilian Society of Cerebrovascular Diseases and The Brazilian Society of Neuroradiology is to provide an organization framework for acute stroke patients’ healthcare and those who require urgent neuro-interventional procedures in the COVID-19 pandemic setting.

COVID-19 AND THE NERVOUS SYSTEM

Typical symptoms of COVID-19 (fever, cough, sore throat, dyspnea, anorexia, nausea, vomiting, diarrhea, abdominal pain) have been well described in the literature, and neurological symptoms may be seen in about one-third of the cases³3. Baig AM. Neurological manifestations in COVID-19 caused by SARS-CoV-2. CNS Neurosci Ther. 2020 May;26(5):499-501. https://doi.org/10.1111/cns.13372
https://doi.org/https://doi.org/10.1111/... ^,44. Jin H, Hong C, Chen S, Zhou Y, Wang Y, Mao L, et al. Consensus for prevention and management of coronavirus disease 2019 (COVID-19) for neurologists. Stroke Vasc Neurol. 2020 Apr;svn-2020-000382. https://doi.org/10.1136/svn-2020-000382
https://doi.org/https://doi.org/10.1136/... ^,55. Mao L, Jin H, Wang M, Hu Y, Chen S, He Q, et al. Neurologic manifestations of hospitalized patients with Coronavirus disease 2019 in Wuhan, China. JAMA Neurol. 2020 Apr;e201127. https://doi.org/10.1001/jamaneurol.2020.1127
https://doi.org/https://doi.org/10.1001/... ^,66. Toscano G, Palmerini F, Ravaglia S, Ruiz L, Invernizzi P, Cuzzoni MG, et al. Guillain-Barré syndrome associated with SARS-CoV-2. N Engl J Med. 2020 Apr;NEJMc2009191. https://doi.org/10.1056/NEJMc2009191
https://doi.org/https://doi.org/10.1056/... ^,77. Munhoz RP, Pedroso JL, Nascimento FA, Almeida SM, Barsottini OGP, Cardoso FEC, Teive HAG. Neurological complications in patients with SARS-CoV-2 infection: a systematic review. Arq. Neuro-Psiquiatr. 2020;78(5):290-300. https://doi.org/10.1590/0004-282X20200051
https://doi.org/https://doi.org/10.1590/... . Neurologic involvement may be presented as central nervous system manifestations (dizziness, headache, impaired consciousness, acute cerebrovascular disease, ataxia, and seizure), peripheral nervous system manifestations (anosmia, ageusia, vision impairment, nerve pain, and Guillain Barré Syndrome), and myopathies³3. Baig AM. Neurological manifestations in COVID-19 caused by SARS-CoV-2. CNS Neurosci Ther. 2020 May;26(5):499-501. https://doi.org/10.1111/cns.13372
https://doi.org/https://doi.org/10.1111/... ^,44. Jin H, Hong C, Chen S, Zhou Y, Wang Y, Mao L, et al. Consensus for prevention and management of coronavirus disease 2019 (COVID-19) for neurologists. Stroke Vasc Neurol. 2020 Apr;svn-2020-000382. https://doi.org/10.1136/svn-2020-000382
https://doi.org/https://doi.org/10.1136/... ^,55. Mao L, Jin H, Wang M, Hu Y, Chen S, He Q, et al. Neurologic manifestations of hospitalized patients with Coronavirus disease 2019 in Wuhan, China. JAMA Neurol. 2020 Apr;e201127. https://doi.org/10.1001/jamaneurol.2020.1127
https://doi.org/https://doi.org/10.1001/... ^,66. Toscano G, Palmerini F, Ravaglia S, Ruiz L, Invernizzi P, Cuzzoni MG, et al. Guillain-Barré syndrome associated with SARS-CoV-2. N Engl J Med. 2020 Apr;NEJMc2009191. https://doi.org/10.1056/NEJMc2009191
https://doi.org/https://doi.org/10.1056/... ^,88. Zhao H, Shen D, Zhou H, Liu J, Chen S. Guillain-Barré syndrome associated with SARS-CoV-2 infection: causality or coincidence? Lancet Neurol. 2020 May;19(5):383-4. https://doi.org/10.1016/S1474-4422(20)30109-5
https://doi.org/https://doi.org/10.1016/... .

Focal neurological deficits due to cerebrovascular disease are less frequent (2.8%) in the course of COVID-19, but they might occur more often amongst those who develop a more severe form of the disease (5.7%)⁵5. Mao L, Jin H, Wang M, Hu Y, Chen S, He Q, et al. Neurologic manifestations of hospitalized patients with Coronavirus disease 2019 in Wuhan, China. JAMA Neurol. 2020 Apr;e201127. https://doi.org/10.1001/jamaneurol.2020.1127
https://doi.org/https://doi.org/10.1001/... . However, they can be an initial manifestation of the disease, and early recognition of infection will significantly impact the line of care of these patients conciliating healthcare professional's protection and proper treatment strategies, especially in time-sensitive therapies like reperfusion for acute ischemic stroke³3. Baig AM. Neurological manifestations in COVID-19 caused by SARS-CoV-2. CNS Neurosci Ther. 2020 May;26(5):499-501. https://doi.org/10.1111/cns.13372
https://doi.org/https://doi.org/10.1111/... ^,44. Jin H, Hong C, Chen S, Zhou Y, Wang Y, Mao L, et al. Consensus for prevention and management of coronavirus disease 2019 (COVID-19) for neurologists. Stroke Vasc Neurol. 2020 Apr;svn-2020-000382. https://doi.org/10.1136/svn-2020-000382
https://doi.org/https://doi.org/10.1136/... ^,55. Mao L, Jin H, Wang M, Hu Y, Chen S, He Q, et al. Neurologic manifestations of hospitalized patients with Coronavirus disease 2019 in Wuhan, China. JAMA Neurol. 2020 Apr;e201127. https://doi.org/10.1001/jamaneurol.2020.1127
https://doi.org/https://doi.org/10.1001/... ^,66. Toscano G, Palmerini F, Ravaglia S, Ruiz L, Invernizzi P, Cuzzoni MG, et al. Guillain-Barré syndrome associated with SARS-CoV-2. N Engl J Med. 2020 Apr;NEJMc2009191. https://doi.org/10.1056/NEJMc2009191
https://doi.org/https://doi.org/10.1056/... .

COVID-19 might increase the risk of cerebrovascular disease by several mechanisms. It may predispose to both venous and arterial thromboembolic disease due to excessive inflammation, hypoxia, immobilization, and disseminated intravascular coagulation. The serum D-dimer level is generally increased, which could be a marker of embolic vascular events⁹9. Zhang Y, Xiao M, Zhang S, Xia P, Cao W, Jiang W, et al. Coagulopathy and antiphospholipid antibodies in patients with Covid-19. N Engl J Med. 2020 Apr;382(17):e38. https://doi.org/10.1056/NEJMc2007575
https://doi.org/https://doi.org/10.1056/... . Despite systematic thrombosis prophylaxis, the incidence of thrombotic complications in intensive care unit (ICU) patients with COVID-19 was remarkably high (31%) in one report¹⁰10. Klok FA, Kruip M, van der Meer NJM, Arbous MS, Gommers D, Kant KM, et al. Incidence of thrombotic complications in critically ill ICU patients with COVID-19. Thromb Res. 2020 Apr;S0049-3848(20)30120-1. https://doi.org/10.1016/j.thromres.2020.04.013
https://doi.org/https://doi.org/10.1016/... . Middle East Respiratory Syndrome (MERS- CoV) can cause acute myocarditis and heart failure, and since COVID-19 has a similar pathogenicity may also predispose to brain embolism from cardiac sources¹¹11. Zheng YY, Ma YT, Zhang JY, Xie X. COVID-19 and the cardiovascular system. Nat Rev Cardiol. 2020 May;17(5):259-60. https://doi.org/10.1038/s41569-020-0360-5
https://doi.org/https://doi.org/10.1038/... .

PATIENT CARE IN THE ISCHEMIC STROKE ACUTE PHASE

Triage

Patient-specific considerations should be balanced in conjunction with the safety of healthcare professionals who are engaged in the triage, assessment, and treatment of patients during the acute stroke phase. Besides the current screening and triage for stroke, healthcare professionals should further examine the COVID-19 pandemic and include an infection control screen, which should check for recent signs and symptoms listed in Table 1 ³3. Baig AM. Neurological manifestations in COVID-19 caused by SARS-CoV-2. CNS Neurosci Ther. 2020 May;26(5):499-501. https://doi.org/10.1111/cns.13372
https://doi.org/https://doi.org/10.1111/... ^,55. Mao L, Jin H, Wang M, Hu Y, Chen S, He Q, et al. Neurologic manifestations of hospitalized patients with Coronavirus disease 2019 in Wuhan, China. JAMA Neurol. 2020 Apr;e201127. https://doi.org/10.1001/jamaneurol.2020.1127
https://doi.org/https://doi.org/10.1001/... . As community transmission started to be established, screening for recent trips became irrelevant. However, history of contact with a confirmed case during the previous 14 days might be beneficial for screening COVID-19 infected individuals, especially in areas with a limited number of infected subjects. This recommended screening may not always be feasible as patients may not be able to communicate reliably due to stroke symptoms (such as aphasia, severe dysarthria, and decreased level of consciousness), and family members may not be on the scene. In such cases, we recommend proceeding with usual COVID-19 safety precautions until the screening can be reliably completed or infection is excluded by formal testing. Screening should be completed during the emergency department (ED) stay using all available sources of information (including telephone contact) to provide the adequate patient transfer.

Patients might be admitted as a spontaneous demand or as a referral from other centers, requiring a reliable triage performed upfront by pre-hospital healthcare professionals and the hospital triage staff. Communication across sites before patient transfer and consistent implementation of local screening protocols are paramount.

Ideally, every stroke patient admitted should be tested for COVID-19 through the reverse transcription polymerase chain reaction (RT-PCR) or rapid serological tests. However, considering the limitation of tests in under-resourced countries, only symptomatic cases have been tested. It is noteworthy that massive testing has not been feasible in our reality, so there is a high proportion of asymptomatic patients or patients with seasonal flu-like symptoms who have been infected by SARS-CoV-2. Recent data estimate that the percentage of pre-symptomatic transmission ranged from 46 to 55%, and infectiousness peaks at zero to two days before symptom onset¹²12. He X, Lau EHY, Wu P, Deng X, Wang J, Hao X, et al. Temporal dynamics in viral shedding and transmissibility of COVID-19. Nat Med. 2020 Apr;26:672-5. https://doi.org/10.1038/s41591-020-0869-5
https://doi.org/https://doi.org/10.1038/... ^,1313. Li R, Pei S, Chen B, Song Y, Zhang T, Yang W, et al. Substantial undocumented infection facilitates the rapid dissemination of novel coronavirus (SARS-CoV-2). Science. 2020 May;368(6490):489-93. https://doi.org/10.1126/science.abb3221
https://doi.org/https://doi.org/10.1126/... . Consequently, the proposed screening is not able to effectively exclude COVID-19, and protective measures are advisable for every stroke patient. Furthermore, the triage, as mentioned (Table 1, Figure 1), may be useful to guide patient transfer to the most appropriate clinical unit (COVID unit or stroke/ICU).

Protected code stroke

Code stroke is a well-known term used to prioritize hyperacute assessment and care of patients with a suspected stroke. The word ‘code’ promotes efficient multi-player, tiered communication among healthcare professionals setting up a process of measured urgent actions during the hyperacute management of a patient with stroke signs and symptoms¹⁴14. Gomez CR, Malkoff MD, Sauer CM, Tulyapronchote R, Burch CM, Banet GA. Code stroke. An attempt to shorten in-hospital therapeutic delays. Stroke. 1994 Oct;25(10):1920-3. https://doi.org/10.1161/01.str.25.10.1920
https://doi.org/https://doi.org/10.1161/... . In the COVID-19 pandemic, code stroke (along with similar medical emergencies) is being modified to the protected designation (Protected Code Stroke - PCS) to provide an extra layer of protection for healthcare professionals and patients.

The appropriate use of personal protective equipment (PPE) by all team members is essential in the PCS. After community transmission, routine PCS should include contact and droplet precautions for all patients. Proper protection requires a full-sleeved gown, eye protection (face shield), gloves, and head covering (Table 2). Since aerosol-generating events might occur in acute stroke, we recommend the use of N95 or KN95 face masks for all stroke team members directly involved in patient’s care at the ED.

Aerosol-generating medical procedures during a code stroke include oropharyngeal/nasal (open) suctioning, bag-valve-mask ventilation, nebulization, high flow oxygen masks, and noninvasive positive pressure ventilation. As such, these events should be avoided or minimized as much as possible. Highly aerosol-generating procedures, such as intubation and chest compressions, should be performed in the appropriate setting according to local/regional protocols¹⁵15. Tran K, Cimon K, Severn M, Pessoa-Silva CL, Conly J. Aerosol generating procedures and risk of transmission of acute respiratory infections to healthcare workers: a systematic review. PLoS One. 2012;7(4):e35797. https://doi.org/10.1371/journal.pone.0035797
https://doi.org/https://doi.org/10.1371/... . Placement of a surgical mask in non-intubated patients is also recommended¹⁶16. Khosravani H, Rajendram P, Notario L, Chapman MG, Menon BK. Protected code stroke: hyperacute stroke management during the Coronavirus disease 2019 (COVID-19) pandemic. Stroke. 2020 Apr:STROKEAHA120029838. https://doi.org/10.1161/STROKEAHA.120.029838
https://doi.org/https://doi.org/10.1161/... .

After initial triage, patients should be referred to the most appropriate location in the ED (ED of COVID unit or regular ED) for urgent neurological assessment, laboratory collection (including rapid serological tests or RT-PCR), and early stabilization.

When patients present signs of respiratory distress, are obtunded or require high fractions of oxygen (FiO₂>0.5), we recommend early consultation with an emergency care or intensive care physician for proper airway management. High flow oxygen masks and noninvasive positive pressure ventilation should be avoided; therefore, early orotracheal intubation should be considered for those patients.

The COVID-19 should not change the indications for acute ischemic stroke reperfusion therapies. In patients eligible for IV thrombolysis and/or mechanical thrombectomy, usual care should be taken following local/regional protocols¹⁷17. Pontes-Neto OM, Cougo P, Martins SC, Abud DG, Nogueira RG, Miranda M, et al. Brazilian guidelines for endovascular treatment of patients with acute ischemic stroke. Arq Neuro-Psiquiatr. 2017 Jan;75(1):50-6. https://doi.org/10.1590/0004-282x20160174
https://doi.org/https://doi.org/10.1590/... ^,1818. Powers WJ, Rabinstein AA, Ackerson T, Adeoye OM, Bambakidis NC, Becker K, et al. 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. 2019 Dec;50(12):e344-e418. https://doi.org/10.1161/STR.0000000000000211
https://doi.org/https://doi.org/10.1161/... . An individual with COVID-19 can be asymptomatic, but be a significant source of infection¹³13. Li R, Pei S, Chen B, Song Y, Zhang T, Yang W, et al. Substantial undocumented infection facilitates the rapid dissemination of novel coronavirus (SARS-CoV-2). Science. 2020 May;368(6490):489-93. https://doi.org/10.1126/science.abb3221
https://doi.org/https://doi.org/10.1126/... ^,1414. Gomez CR, Malkoff MD, Sauer CM, Tulyapronchote R, Burch CM, Banet GA. Code stroke. An attempt to shorten in-hospital therapeutic delays. Stroke. 1994 Oct;25(10):1920-3. https://doi.org/10.1161/01.str.25.10.1920
https://doi.org/https://doi.org/10.1161/... ^,1515. Tran K, Cimon K, Severn M, Pessoa-Silva CL, Conly J. Aerosol generating procedures and risk of transmission of acute respiratory infections to healthcare workers: a systematic review. PLoS One. 2012;7(4):e35797. https://doi.org/10.1371/journal.pone.0035797
https://doi.org/https://doi.org/10.1371/... .

Changes in high-resolution chest computed tomography (HRCCT) before viral symptoms can be detected in about 20% of the patients¹⁶16. Khosravani H, Rajendram P, Notario L, Chapman MG, Menon BK. Protected code stroke: hyperacute stroke management during the Coronavirus disease 2019 (COVID-19) pandemic. Stroke. 2020 Apr:STROKEAHA120029838. https://doi.org/10.1161/STROKEAHA.120.029838
https://doi.org/https://doi.org/10.1161/... . Thus, a HRCCT may be recommended after an initial non-contrast head computed tomography (NCCT) assessment for patients with a suspected stroke. Nonetheless, the feasibility of this recommendation should be assessed by each institution, weighing the availability of resources and the potential risk of silent COVID-19 spreaders. In the event of a positive HRCCT, the patient should be considered a suspected case of COVID-19 infection, and the appropriate protocol should be followed¹⁹19. Bernheim A, Mei X, Huang M, Yang Y, Fayad ZA, Zhang N, et al. Chest CT Findings in Coronavirus Disease-19 (COVID-19): Relationship to Duration of Infection. Radiology. 2020 Jun;295(3):200463. https://doi.org/10.1148/radiol.2020200463
https://doi.org/https://doi.org/10.1148/... . The HRCCT findings will be more frequent in the intermediate (three to six days) and late (from seven days) phases from symptoms onset¹⁷17. Pontes-Neto OM, Cougo P, Martins SC, Abud DG, Nogueira RG, Miranda M, et al. Brazilian guidelines for endovascular treatment of patients with acute ischemic stroke. Arq Neuro-Psiquiatr. 2017 Jan;75(1):50-6. https://doi.org/10.1590/0004-282x20160174
https://doi.org/https://doi.org/10.1590/... . If the HRCCT is negative, COVID-19 cannot be excluded, particularly in pre-symptomatic and early phases, but it may help to guide the transfer of the patient to an appropriate unit (COVID or non-COVID units).

Definition criteria for COVID-19 disease

According to the WHO, a COVID-19 case may be defined as suspected, probable, or confirmed (Table 3)²⁰20. World Health Organization. Coronavirus disease 2019 (COVID-19) pandemic. [cited 2020 Mar 24]; Available from: Available from: https://www.who.int/emergencies/diseases/novel-coronavirus-2019
https://www.who.int/emergencies/diseases... . For acute stroke management, the decision-making process should be very expeditious, but sometimes a full triage is not feasible. Therefore, we adapted the WHO classification, and patients should be considered at low risk for COVID-19 infection if the screening for COVID-19 is negative (Table 1).

Patients should be considered a suspected case of COVID-19 in case of:

Patients should be considered a possible case of COVID-19 if:

Patients should be considered a confirmed case of COVID-19 infection if:

Medical management of acute ischemic stroke in COVID-19 patients

Patients with transient ischemic attack that do not necessarily require hospital admission may be appropriately managed at an outpatient level if the appropriate etiological investigation and secondary prevention can be performed in a timely fashion. Careful assessment needs to balance the risk/benefit ratio²¹21. Markus HS, Brainin M. EXPRESS: COVID-19 and Stroke - A Global World Stroke Organisation perspective. Int J Stroke. 2020 Apr;1747493020923472. https://doi.org/10.1177/1747493020923472
https://doi.org/https://doi.org/10.1177/... .

Patient evaluation with extended acute CT angiography protocols (angio-CT), including great vessels and cardiac CT, might help to expedite the assessment of stroke etiology and decrease the risk of infections associated with additional in-hospitals transfers for exams, such as carotid ultrasonography and echocardiography²²22. Hur J, Choi BW. Cardiac CT imaging for ischemic stroke: current and evolving clinical applications. Radiology. 2017 Apr;283(1):14-28. https://doi.org/10.1148/radiol.2016152043
https://doi.org/https://doi.org/10.1148/... . However, based on current evidence, cardiac CT is not routinely recommended for the evaluation of intracardiac structures in stroke patients.

It is noteworthy that the appropriate use of PPE by all team members (including stroke unit/ICU physicians, nursing staff, physical therapists, and speech therapists) involved in patient care is critical (Table 2).

Stroke telemedicine

Telemedicine has a great potential for triage and management of stroke patients during the COVID-10 pandemic, and its implementation at a pre-hospital and outpatient level should be encouraged. Stroke teleconsultations might spare the use of PPE, avoid unnecessary inter-facility transfers, and reduce exposure risk for the stroke team²¹21. Markus HS, Brainin M. EXPRESS: COVID-19 and Stroke - A Global World Stroke Organisation perspective. Int J Stroke. 2020 Apr;1747493020923472. https://doi.org/10.1177/1747493020923472
https://doi.org/https://doi.org/10.1177/... . The current available evidence supports the use of a modified neurological examination and reliable National Institutes of Health Stroke Scale (NIHSS) assessment using telemedicine²³23. Awadallah M, Janssen F, Korber B, Breuer L, Scibor M, Handschu R. Telemedicine in general neurology: interrater reliability of clinical neurological examination via audio-visual telemedicine. Eur Neurol. 2018;80(5-6):289-94. https://doi.org/10.1159/000497157
https://doi.org/https://doi.org/10.1159/... ^,2424. Barrett KM, Pizzi MA, Kesari V, TerKonda SP, Mauricio EA, Silvers SM, et al. Ambulance-based assessment of NIH Stroke Scale with telemedicine: A feasibility pilot study. J Telemed Telecare. 2017 May;23(4):476-83. https://doi.org/10.1177/1357633X16648490
https://doi.org/https://doi.org/10.1177/... . A low-cost smartphone-based teleconsultation system for acute stroke has been validated in Brazil²⁵25. Martins SCO, Weiss G, Almeida AG, Brondani R, Carbonera LA, de Souza AC, et al. Validation of a smartphone application in the evaluation and treatment of acute stroke in a Comprehensive Stroke Center. Stroke. 2020 Jan;51(1):240-6. https://doi.org/10.1161/STROKEAHA.119.026727
https://doi.org/https://doi.org/10.1161/... .

NEUROINTERVENTION PROCEDURES DURING THE PANDEMIC

Mechanical thrombectomy (MT) for acute ischemic stroke due to large vessel occlusion is a well-established procedure for the early and late time window²⁶26. Albers GW, Marks MP, Kemp S, Christensen S, Tsai JP, Ortega-Gutierrez S, et al. Thrombectomy for stroke at 6 to 16 hours with selection by perfusion imaging. N Engl J Med. 2018 Feb;378:708-18. https://doi.org/10.1056/NEJMoa1713973
https://doi.org/https://doi.org/10.1056/... ^,2727. Goyal M, Menon BK, van Zwam WH, Dippel DW, Mitchell PJ, Demchuk AM, et al. Endovascular thrombectomy after large-vessel ischaemic stroke: a meta-analysis of individual patient data from five randomized trials. Lancet. 2016 Apr;387(10029):1723-31. https://doi.org/10.1016/S0140-6736(16)00163-X
https://doi.org/https://doi.org/10.1016/... ^,2828. Nogueira RG, Jadhav AP, Haussen DC, Bonafe A, Budzik RF, Bhuva P, et al. Thrombectomy 6 to 24 hours after stroke with a mismatch between deficit and infarct. N Engl J Med. 2018 Jan 4;378(1):11-21. https://doi.org/10.1056/NEJMoa1706442
https://doi.org/https://doi.org/10.1056/... . COVID-19 should not modify inclusion and exclusion criteria for endovascular reperfusion. As a time-sensitive procedure, MT protocols should be reorganized to minimize the exposure risk of patients and healthcare professionals, but without compromising the speed of evaluation and treatment.

The neurointervention team should define if the procedure is elective (e.g. unruptured cerebral aneurysm) or urgent, considering the risks/benefits of the procedure in relation to the likelihood of contamination and/or activation of the viral infection in asymptomatic individuals. It is a consensus among several Societies and Organizations, such as WHO, American College of Surgeons, Society of Vascular and Interventional Neurology, Society of Neurointerventional Surgery, French Society of Neuroradiology, Brazilian College of Surgeons, National Agency for Supplementary Health Service and the Brazilian Department of Health, that elective surgeries should be temporarily postponed during the COVID-19 pandemic, concentrating material resources, specialized teams, and ICU beds for the most severe cases⁸8. Zhao H, Shen D, Zhou H, Liu J, Chen S. Guillain-Barré syndrome associated with SARS-CoV-2 infection: causality or coincidence? Lancet Neurol. 2020 May;19(5):383-4. https://doi.org/10.1016/S1474-4422(20)30109-5
https://doi.org/https://doi.org/10.1016/... ^,99. Zhang Y, Xiao M, Zhang S, Xia P, Cao W, Jiang W, et al. Coagulopathy and antiphospholipid antibodies in patients with Covid-19. N Engl J Med. 2020 Apr;382(17):e38. https://doi.org/10.1056/NEJMc2007575
https://doi.org/https://doi.org/10.1056/... ^,1010. Klok FA, Kruip M, van der Meer NJM, Arbous MS, Gommers D, Kant KM, et al. Incidence of thrombotic complications in critically ill ICU patients with COVID-19. Thromb Res. 2020 Apr;S0049-3848(20)30120-1. https://doi.org/10.1016/j.thromres.2020.04.013
https://doi.org/https://doi.org/10.1016/... ^,1111. Zheng YY, Ma YT, Zhang JY, Xie X. COVID-19 and the cardiovascular system. Nat Rev Cardiol. 2020 May;17(5):259-60. https://doi.org/10.1038/s41569-020-0360-5
https://doi.org/https://doi.org/10.1038/... ^,1212. He X, Lau EHY, Wu P, Deng X, Wang J, Hao X, et al. Temporal dynamics in viral shedding and transmissibility of COVID-19. Nat Med. 2020 Apr;26:672-5. https://doi.org/10.1038/s41591-020-0869-5
https://doi.org/https://doi.org/10.1038/... .

There are only a few articles regarding elective surgery with COVID-19 related complications in asymptomatic patients²⁹29. Seddiq N, Al-Qahtani M, Al-Tawfiq JA, Bukamal N. First confirmed case of Middle East respiratory syndrome Coronavirus infection in the Kingdom of Bahrain: In a Saudi gentleman after cardiac bypass surgery. Case Rep Infect Dis. 2017;2017:1262838. https://doi.org/10.1155/2017/1262838
https://doi.org/https://doi.org/10.1155/... . Lei et al. reported 34 patients that underwent different surgeries, of whom 15 (44.1%) developed respiratory insufficiency requiring intensive care assistance and 7 (20.5%) died³⁰30. Lei S, Jiang F, Su W, Chen C, Chen J, Mei W, et al. Clinical characteristics and outcomes of patients undergoing surgeries during the incubation period of COVID-19 infection. EClinicalMedicine. 2020 Apr;100331. https://doi.org/10.1016/j.eclinm.2020.100331
https://doi.org/https://doi.org/10.1016/... . In such retrospective report, the authors attribute the decreased cell-mediated immunological response to surgical stress, leading to accelerated viral replication, as demonstrated by the shorter incubation time of the disease (average of 2.5 days). Older age, prolonged surgical time, procedure complexity, high blood pressure, diabetes, and cardiac disease were associated with a worse prognosis.

On the other hand, an elective procedure can evolve into an emergency, depending on the type of vascular brain lesion and waiting time. Physicians are responsible for deciding the most appropriate moment for intervention. According to the National Agency of Supplementary Health, doctor and patient must keep a communication channel, using new technologies that allow non-presential evaluation and follow-up during the new coronavirus pandemic.

Thus, even though there is a growing number of confirmed cases and deaths, the following urgent/emergency procedures are recommended in case of cerebrovascular diseases:

RECOMMENDATIONS FOR NEUROINTERVENTIONAL PROCEDURES IN PATIENTS AT LOW RISK FOR COVID-19

A patient is considered at low risk for COVID-19 infection if the screening for COVID-19 is negative (Table 1). In such situation, individuals should undergo the procedure in the angiography room for patients without COVID-19 (if applicable) and wear a surgical mask during the entire hospitalization. Usual care, including protective measures for COVID-19, should be adapted according to the procedure, local standards, and aerosolization risk (Table 2). After the procedure, the patient should be admitted to the most appropriate unit of care (Stroke Unit or ICU), based on local protocols.

RECOMMENDATIONS FOR PROCEDURES IN PATIENTS WITH SUSPECTED, POSSIBLE, AND CONFIRMED COVID-19

Patients should be placed on contact and droplet precautions. During procedures, chiefly those generating aerosols, healthcare personnel should wear full protection (Table 2).

It is crucial to follow the items below when dealing with patients with suspected/documented COVID-19.

Pre-procedure

In the angiography suite

Notably, some authors have suggested that patients with dominant cerebral hemisphere occlusions and/or aphasia, as well as those with high NIHSS (>15), be considered for early intubation¹⁸18. Powers WJ, Rabinstein AA, Ackerson T, Adeoye OM, Bambakidis NC, Becker K, et al. 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. 2019 Dec;50(12):e344-e418. https://doi.org/10.1161/STR.0000000000000211
https://doi.org/https://doi.org/10.1161/... . However, no reliable evidence supports this suggestion, as none of these factors have been demonstrated to be predictors of conversion from sedation to general anesthesia. Therefore, we discourage the preemptive intubation of these patients in the absence of agitation or any of the other aforementioned conditions, as this would lead to a high number of unnecessary intubations during a time of crisis when we should strive to optimize the use of our resources. The main idea behind the recommendations for early intubation is to minimize the risk of intra-procedural intubation, considering it is a less controlled intervention and, as such, carries a higher risk of contamination. However, this needs to be balanced against the higher exposure of medical teams that intubate and extubate these patients, as well as to the additional use of time and resources. Thus, teams are encouraged to consider their local experiences in these decisions.

Post-procedure

INFORMED CONSENT

The risk of COVID-19 contamination is higher in hospitalization, and this additional risk factor should be made explicit in the consent form, especially in cases where urgency/emergency is not undoubtedly characterized, as for example in unruptured aneurysms.

TRAINING

During care of COVID-19 patients, many protocol violations are possible in doffing and donning of PPE. Additionally, health professionals may not be familiar with the required procedures and use of the equipment (such as fogging of the “face shield” impairing visibility).

In this setting, training with on-site simulation is highly recommended to ensure proper execution of protocols and to avoid unnecessary stress, especially among professionals involved in aerosol-generating procedures, such as orotracheal intubation, nasogastric tube insertion, among others. All healthcare professionals should be fit-tested for N95 masks, especially those who deal directly with aerosol-generating procedures.

The N95 masks used in aerosol-generating procedures or contaminated with blood, respiratory or nasal secretions should be preferably discarded, although this recommendation might be impractical in most centers due to limited availability of resources. N95 respirators contaminated with blood, respiratory or nasal secretions, or other bodily fluids from patients, should also be discarded. Extended use of N95 masks is permitted, but it still carries a risk of contamination during donning and doffing, because virus particles may be viable up to six days in porous surfaces³¹31. Coulliette AD, Perry KA, Edwards JR, Noble-Wang JA. Persistence of the 2009 pandemic influenza A (H1N1) virus on N95 respirators. Appl Environ Microbiol. 2013 Apr;79(7):2148-55. https://doi.org/10.1128/AEM.03850-12
https://doi.org/https://doi.org/10.1128/... . Accordingly, training on donning, doffing, and proper storing of N95 facial masks is essential to avoid contamination of healthcare professionals while handling these PPE. The use of a cleanable face shield over an N95 respirator reduces the risk of surface contamination. Hospitals should ensure adequate storage area or keep the masks in a clean and breathable container, such as a paper bag³²32. Centers for Disease Control and Prevention. Recommended Guidance for Extended Use and Limited Reuse of N95 Filtering Facepiece Respirators in Healthcare Settings. [cited 2020 Apr 31]. Available from: Available from: https://www.cdc.gov/niosh/topics/hcwcontrols/recommendedguidanceextuse.html
https://www.cdc.gov/niosh/topics/hcwcont... .

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