Practice recommendations for neurovascular ultrasound investigations of acute stroke patients in the setting of the COVID19 pandemic: an expert consensus from the European Society of Neurosonology and Cerebral Hemodynamics



# Introduction
Since the COVID-19 pandemic stormed into healthcare systems worldwide, protected stroke pathways have been suggested, in order not to spread the viral infection and ensure hyper-acute treatment [bib_ref] Protected Code Stroke: Hyperacute stroke management during the coronavirus disease 2019 (COVID-19)..., Khosravani [/bib_ref] [bib_ref] Acute stroke management pathway during Coronavirus-19 pandemic, Baracchini [/bib_ref]. Noteworthy, patients with acute ischaemic stroke are at high risk for contracting SARS-CoV-2 virus, particularly the severe form, because COVID-19 and cerebrovascular * Correspondence: C. [Correction added on 18 August 2020, after first online publication: The corresponding author listed has been amended from A. Pieroni to C. Baracchini at the request of the authors, the co-author name G. Tsvigoulis has been amended to G. Tsivgoulis in this version.] diseases share common risk factors [bib_ref] Prevalence and impact of cardiovascular metabolic diseases on COVID-19 in China, Li [/bib_ref]. Conversely, amongst patients hospitalized with SARS-CoV-2 respiratory distress, about 5% might suffer a stroke [bib_ref] Neurologic Manifestations of Hospitalized Patients With Coronavirus Disease, Mao [/bib_ref]. During the acute stages of the pandemic, thousands of healthcare professionals have already contracted COVID-19 infection [bib_ref] Characteristics of and important lessons from the coronavirus disease 2019 (COVID-19) outbreak..., Wu [/bib_ref] , although the actual number is likely to be higher because healthcare workers are not always tested and protection measures at hospitals are not always readily available. This is the setting in which neurovascular ultrasound providers (physicians, sonographers) should expect to be involved in the care of stroke patients. In light of this situation, effective safety and prevention strategies need to be implemented not only during the lockdown period but especially afterwards when healthcare workers and patients will tend to let their guard down. Therefore, the European Society of Neurosonology and Cerebral Hemodynamics (ESNCH) is providing the following recommendations for the performance of neurovascular ultrasound investigations with the aim of protecting both patients and ultrasound providers. To develop this document, members of the Ultrasound in Acute Stroke Working Group of the ESNCH examined literature articles and reviews using the following keywords: 'corona virus' or 'COVID-19' or 'SARS-CoV-2 virus', and 'acute stroke' or 'cerebrovascular disease', and 'ultrasound'. The World Health Organization and the Center for Disease Control and Prevention (CDC) recommendations on the COVID-19 pandemic were also consulted. After a thorough discussion with the Education and Guidelines Working Group of the ESNCH, a final consensus was reached [fig_ref] Table 1: ESNCH recommendations for neurovascular ultrasound in acute stroke during the COVID-19 pandemicPre-hospital... [/fig_ref] and [fig_ref] Figure 1: Recommendations for neurovascular ultrasound investigation of acute stroke patients during COVID-19 Pandemic [/fig_ref]. The successful care of COVID-19-positive or presumed positive stroke patients will depend also on these prevention strategies [bib_ref] Fair allocation of scarce medical resources in the time of Covid-19, Emanuel [/bib_ref].

## Pre-hospital assessment
Field personnel should screen all patients for COVID-19 infection using standardized checklists of clinical signs and symptoms (i.e. fever, cough, chest pain, dyspnoea, anosmia, ageusia, headache, myalgias and gastrointestinal symptoms including vomiting and diarrhoea) or history of close contact exposure with a COVID-positive patient, and immediately dispatch these data to the emergency operations centre for preparedness. Stroke patients might not be able to provide a full history due to neurological impairment; in this case, close relatives should be asked for clinical signs and symptoms, possible contacts with COVID-19-infected persons or risky social behaviour over the past 2 weeks. If the screening is positive or medical history is not available, patients should be considered as possibly COVID-19 infected. For safety reasons, a COVID-19 known positive or presumed positive patient should wear a surgical mask, whilst healthcare providers should use appropriate protection according to COVID status (see below). Furthermore, clinically oriented extracranial and intracranial ultrasound evaluation, if available, should be performed during transport to reveal large vessel occlusion strokes and indicate the most suitable destination for the patient [bib_ref] Transcranial ultrasound from diagnosis to early stroke treatment: part 2: Prehospital neurosonography..., Schlachetzki [/bib_ref] [bib_ref] Prehospital stroke diagnostics based on neurological examination and transcranial ultrasound, Herzberg [/bib_ref]. Eligibility for hyper-acute therapies is not modified by the COVID-19 pandemic; consequently current guidelines should be implemented [bib_ref] Current endovascular strategies for posterior circulation large vessel occlusion stroke: report of..., Kayan [/bib_ref] [bib_ref] Indications for thrombectomy in acute ischemic stroke from emergent large vessel occlusion..., Mokin [/bib_ref] as a denial of these therapies might increase the social burden of stroke, creating also a greater drain on healthcare resources [bib_ref] Relationship between functional disability and costs one and two years post stroke, Lekander [/bib_ref].

## Intra-hospital assessment
If resources are available, all stroke patients should undergo a fast track COVID-19 nasopharyngeal test It is recommended to have one laboratory designated as a 'COVID room', stocked with enhanced PPE and with at least one dedicated ultrasound machine for COVID-19-positive or presumed positive patients A room adjacent to the angiography suite should be designated as post-thrombectomy ultrasound monitoring in order to prevent in-hospital transmission and indicate the most appropriate safety measures for ultrasound providers.

## Covid-19-negative patients
As the sensitivity of nasopharyngeal swabs is about 70%, the ESNCH recommends wearing standard personal protective equipment (PPE): surgical mask, latex-free disposable gloves and a disposable gown. Before and after direct patient contact, appropriate hand hygiene, even with a sanitizer, is imperative.

## Covid-19-positive or presumed positive patients
Therapeutic decisions on systemic or endovascular reperfusion therapies for COVID-19-positive and presumed positive patients presenting with acute stroke symptoms may rely on ultrasound to avoid potential time delays related to computed tomography or magnetic resonance angiography [bib_ref] Yield and accuracy of urgent combined carotid/transcranial ultrasound testing in acute cerebral..., Chernyshev [/bib_ref]. FFP2 masks), surgical cap, goggles, face shield, fullsleeved gown, two pairs (internal and external) of extended cuff gloves and outer short cuff gloves, boottype shoe covers, and proper donning/doffing hygiene. In the case of resource limitations, a standard surgical mask can be worn over the N95 or FFP2 mask for preservation of the latter. If resources are not available, stroke patients presumed to be COVID-19 negative on a clinical and anamnestic basis should wear a surgical mask, whilst healthcare providers should wear at least standard PPE.

## Ultrasound equipment
Since many patients who undergo neurovascular ultrasound will be COVID-19 positive or presumed positive in the current environment, effective cleaning of ultrasound equipment is compulsory. Transducers and ultrasound equipment must be cleaned with a compatible disinfectant after each patient, also in accordance with local guidelines. For external procedures, such as extracranial and intracranial ultrasound, low-level disinfection (LLD) is effective in agreement with CDC guidelines. Common LLD agents include quaternary ammonium compounds, alcohols and phenols available as sprays and disinfectant wipes. Ultrasound providers should ensure that the chosen LLD method is compatible with the transducer; for example, alcohols are often contraindicated due to material incompatibility. If LLD agents are depleted, soap and water are a valid alternative. Noteworthy, external transducers that come into contact with contaminated skin, such as skin infections, should be covered with a single-use transducer cover. If transducer covers are not available, medical gloves or other physical barriers as compatible medical dressings should be used. If the transducer comes in contact with mucous membranes or any body fluids, or a transducer cover is required and becomes compromised, the transducer must undergo high-level disinfection (HLD). HLD agents include hydrogen peroxide, hypochlorite/hypochlorous acid, glutaraldehyde, peracetic acid, phenol/phenolate, chlorhexidine gluconate. At the end of the day, the ultrasound room should also undergo appropriate cleaning and disinfection.

## Organization of neurosonology laboratory
For hospitals with multiple neurovascular ultrasound laboratories, it is recommended to have one laboratory designated as a 'COVID room', stocked with enhanced PPE to minimize risk and with at least one dedicated ultrasound machine for COVID-19-positive or presumed positive patients, since COVID-19 can survive on plastic surfaces for up to 72 h [bib_ref] Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1, Van Doremalen [/bib_ref]. Concerning post-thrombectomy ultrasound monitoring [bib_ref] Diagnostic criteria and yield of real-time transcranial Doppler monitoring of intra-arterial reperfusion..., Rubiera [/bib_ref] [bib_ref] Increased middle cerebral artery mean blood flow velocity index after stroke thrombectomy..., Kneihsl [/bib_ref] [bib_ref] Early hemodynamic predictors of good outcome and reperfusion injury after endovascular treatment, Baracchini [/bib_ref] [bib_ref] Microemboli after successful thrombectomy do not affect outcome but predict new embolic..., Sheriff [/bib_ref] , if possible a room adjacent to the angiography suite should be designated for this purpose, to minimize exposure of any at-risk group of patients to potential COVID-19 contact in the hospital environment.

## Disclosure of conflict of interest
The authors declare no financial or other conflicts of interest.

# Data availability statement
Data sharing is not applicable to this article as no new data were created or analysed in this study.
[fig] Figure 1: Recommendations for neurovascular ultrasound investigation of acute stroke patients during COVID-19 Pandemic. PPE, personal protective equipment; US, ultrasound. [Colour figure can be viewed at wileyonlinelibra ry.com] [/fig]
[table] Table 1: ESNCH recommendations for neurovascular ultrasound in acute stroke during the COVID-19 pandemicPre-hospital assessmentField personnel should screen all acute stroke patients for COVID-19 infection If the screening is positive or medical history is not available, patients should be considered as possibly COVID-19 infected A COVID-19 known positive or presumed positive patient [/table]