ARTICLE
Global Impact of COVID-19 on Stroke Care and
IV Thrombolysis
Raul G. Nogueira, MD, Muhammad M. Qureshi, MBBS, MPH, Mohamad Abdalkader, MD, Sheila Ouriques
Martins, MD, PhD, Hiroshi Yamagami, MD, PhD, Zhongming Qiu, MD, PhD, Ossama Yassin Mansour, MD, PhD,
Anvitha Sathya, Anna Czlonkowska, MD, PhD, Georgios Tsivgoulis, MD, PhD, Diana Aguiar de Sousa, MD, Jelle
Demeestere, MD, Robert Mikulik, MD, PhD, Peter Vanacker, MD, PhD, James E. Siegler, MD, Janika Kõrv, MD,
PhD, Jose Biller, MD, Conrad W. Liang, MD, PhD, Navdeep S. Sangha, MD, Alicia M. Zha, MD, Alexandra L.
Czap, MD, Christine Anne Holmstedt, MD, Tanya N. Turan, MD, George Ntaios, MD, Konark Malhotra, MD,
Ashis Tayal, MD, Aaron Loochtan, DO, Annamarei Ranta, MD, PhD, Eva A. Mistry, MBBS, Anne W.
Alexandrov, PhD, David Y. Huang, MD, PhD, Shadi Yaghi, MD, Eytan Raz, MD, PhD, Sunil A. Sheth, MD,
Mahmoud H. Mohammaden, MD, Michael Frankel, MD, Eric Guemekane Bila Lamou, MD, MSc, Hany M.
Aref, MD, Ahmed Elbassiouny, MD, Farouk Hassan, MD, Tarek Menecie, MD, Wessam Mustafa, MD, Hossam
M. Shokri, MD, Tamer Roushdy, MD, Fred S. Sarfo, MD, Tolulope Oyetunde Alabi, MBBS, MWACP, Babawale
Arabambi, MBBS, FWACP, Ernest O. Nwazor, MBBS, FMCP, Taofiki Ajao Sunmonu, MD, Kolawole
Wahab, MBBS, MPH, MSc, FMCP, Joseph Yaria, MBBS, MSc, Haytham Hussein Mohammed, MD, Philip B.
Adebayo, MBBS, MSc, FWACP, FCP, Anis D. Riahi, MD, Samia Ben Sassi, MD, et al. on behalf of the SVIN COVID19 Global Stroke Registry
Correspondence
Dr. Nguyen
[email protected]
®
Neurology 2021;96:e2824-e2838. doi:10.1212/WNL.0000000000011885
Abstract
RELATED ARTICLE
Objective
To measure the global impact of COVID-19 pandemic on volumes of IV thrombolysis (IVT),
IVT transfers, and stroke hospitalizations over 4 months at the height of the pandemic (March 1
to June 30, 2020) compared with 2 control 4-month periods.
Where in the World Have
All the Strokes Gone?
Page 1069
Methods
We conducted a cross-sectional, observational, retrospective study across 6 continents, 70
countries, and 457 stroke centers. Diagnoses were identified by their ICD-10 codes or classifications in stroke databases.
Results
There were 91,373 stroke admissions in the 4 months immediately before compared to 80,894
admissions during the pandemic months, representing an 11.5% (95% confidence interval [CI]
−11.7 to −11.3, p < 0.0001) decline. There were 13,334 IVT therapies in the 4 months
preceding compared to 11,570 procedures during the pandemic, representing a 13.2% (95% CI
−13.8 to −12.7, p < 0.0001) drop. Interfacility IVT transfers decreased from 1,337 to 1,178, or
an 11.9% decrease (95% CI −13.7 to −10.3, p = 0.001). Recovery of stroke hospitalization
volume (9.5%, 95% CI 9.2–9.8, p < 0.0001) was noted over the 2 later (May, June) vs the 2
earlier (March, April) pandemic months. There was a 1.48% stroke rate across 119,967
COVID-19 hospitalizations. Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2)
infection was noted in 3.3% (1,722/52,026) of all stroke admissions.
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Conclusions
The COVID-19 pandemic was associated with a global decline in the volume of stroke hospitalizations, IVT, and interfacility IVT transfers. Primary stroke centers and centers with higher
COVID-19 inpatient volumes experienced steeper declines. Recovery of stroke hospitalization
was noted in the later pandemic months.
The Author Byline is continued at the end of the article.
Author affiliations appear at the end of the article.
Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.
Authors Raul G. Nogueira, MD, and Thanh N. Nguyen, MD, contributed equally to this work.
Authors, their locations, and their contributions are listed at links.lww.com/WNL/B357.
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Glossary
CI = confidence interval; , COVID-19 = coronavirus disease 2019; , CSC = comprehensive stroke center; , ICD-10 =
International Classification of Diseases–10; , IQR = interquartile range; , IVT = IV thrombolysis; , PSC = primary stroke center;
, SARS-CoV-2 = severe acute respiratory syndrome coronavirus 2.
The coronavirus disease 2019 (COVID-19) pandemic has
restructured health care systems worldwide to care for critically
ill patients with COVID-19.1 The high virulence of severe acute
respiratory syndrome coronavirus 2 (SARS-CoV-2) and
COVID-19–related morbidity and mortality have strained
paradigms of health care worldwide. Several neurologic manifestations have been reported in association with SARS-CoV-2,
including ischemic, hemorrhagic, and cerebral venous stroke.
Whereas infection can trigger an inflammatory prothrombotic
cascade and ischemic stroke, stroke can induce immune dysregulation and expose a patient’s vulnerability to infection.2
The heterogeneity of stroke subtypes that have emerged in
association with SARS-CoV-23,4 suggests heterogeneous
mechanisms of stroke including endothelial dysfunction,
thrombotic diathesis, and nonspecific effects of inflammation.5
Patients with COVID-19–associated stroke have been reported
to have a higher risk for severe disability and mortality.4,6,7
Whereas there has been an increase in thromboembolic
events reported with COVID-19,8 a decline in acute stroke
code activations, stroke hospitalizations, and mechanical
thrombectomy volumes have been reported at local, regional,
and national levels,9-13 with most reports from comprehensive
stroke centers (CSCs) in highly resourced countries. There is
a relative paucity of information on the effect of the pandemic
on acute stroke hospitalization volume and IV thrombolysis
(IVT) acute treatment in low- or middle-income countries
and in primary stroke centers (PSCs) without endovascular
capability. There is also little information on the recovery of
volumes in the later phases of the pandemic.
Objectives and Prespecified Hypothesis
In this context, the present study aims to broaden the scope of
evaluating the effect of the COVID-19 pandemic on global
stroke care to include developed and developing nations in the
early and later phases of the COVID-19 pandemic. Our primary
aim was to evaluate the effect of COVID-19 on stroke care as
measured by the changes in volumes for (1) overall stroke
hospitalizations and (2) IVT treatment (both direct presenting
and patients transferred with IVT) for acute stroke across the
prepandemic and pandemic periods in a multinational pool of
PSCs and CSCs. In a secondary aim, the pandemic months were
divided into an early (March 1, 2020, to April 30, 2020) and later
phase (May 1, 2020, to June 30, 2020) to evaluate for stroke or
IVT volume recovery in the later months.
We hypothesized that, in the face of the pandemic’s strain on
health care infrastructure, (1) a global reduction in all 3 aforementioned measurements of stroke care would occur over the
Neurology.org/N
pandemic in relation to both prepandemic periods, (2) hospitals
with higher COVID-19 inpatient volumes would report greater
decreases in stroke admissions and IVT volumes (direct and
transfers) compared to hospitals with lower COVID-19 inpatient volumes, (3) the degree of decline in stroke hospitalizations and IVT volumes would be less profound in CSC
compared to PSC, (4) a geographic variation would exist in the
intensity of decline in stroke care, and (5) a recovery in stroke
hospitalizations and IVT volumes would be observed in the 2
later pandemic months vs the early pandemic period.
Methods
Study Design
This was a cross-sectional, observational, retrospective study
evaluating monthly volumes of consecutive patients hospitalized with a diagnosis of COVID-19, stroke, IVT treatment,
and IVT transfers. The diagnoses were identified by their
related ICD-10 codes (primary, secondary, or tertiary discharge codes) or classifications in clinical stroke databases
maintained at participating centers. Case ascertainment was
verified by a physician or stroke coordinator.
Setting and Participants
Data were collected from collaborators of the Society of
Vascular and Interventional Neurology (SVIN) including
the Latin America Stroke Group, Middle East North Africa
Stroke and Interventional Neurotherapies Organization
(MENA-SINO), the Japanese Society of Vascular & Interventional Neurology Society (JSVIN), and academic partners from 6 continents, 70 countries, and 457 centers.
Centers were screened for potential external confounders
that could explain any unexpected changes in volumes. Of
the 457 centers, 54 centers were excluded due to incomplete
data or confounders. One center in Africa (Zimbabwe) was
excluded due to a health care worker strike from September
to January. One center in Egypt was excluded due to the
emergency department being closed most days in June 2020.
One center in Arkansas was excluded from the stroke hospitalization volume analysis because this center became the
designated center for all patients with stroke in its region
during the pandemic, resulting in an abrupt increase in
stroke volumes. One center in Malaysia was excluded as this
was a new center in May 2020. Of the remaining 403 hospitals, 285 centers contributed to both stroke and thrombolysis volume data. For IVT transfers, centers with a mean
of 4 or more transfers per month during the baseline control
period were included.
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We compared the stroke, IVT, and IVT transfer diagnosis in
the 4 initial months of the pandemic (March 1, 2020, to June
30, 2020) with (1) the immediately preceding 4 months
(November 2019 to February 2020) as the primary analysis
and (2) the equivalent 4 months in the previous year (March
1, 2019, to June 30, 2019) as the secondary analysis. The
primary analysis provided a picture of stroke care utilization
prior to COVID-19, whereas the secondary analysis allowed
for the adjustment for seasonal variations in the risks for
stroke.14
Study Variables and Outcomes Measures
Stroke hospitalization was defined as admission to a hospital
with a TIA, ischemic stroke, or intracerebral hemorrhage.
IVT was defined as acute ischemic stroke treatment with
IVT. IVT transfer was defined as a patient who was treated
with IVT and transferred to another stroke center. Centers
were asked not to duplicate patients receiving IVT if both
referral and recipient centers were included in this analysis;
the patient was computed with the referring center, and as an
IVT transfer for the recipient hospital. COVID-19 hospitalization was defined as any patient admitted with COVID19 diagnosis to the hospital, which could encompass nonneurologic diagnosis.
Median monthly volumes for overall stroke hospitalizations
and IVT treatments for direct presenting and transfer patients
were computed and compared across the pandemic and
prepandemic periods for the overall population and across the
low, intermediate, and high volume strata based on mean
monthly volume tertiles for COVID-19 hospitalizations (≤6.2
vs >6.2 to 61.9 vs >61.9 COVID-19 admissions/month),
stroke admissions (≤39.0 vs >39.0 to 72.9 vs >72.9 stroke
admissions/month), and IVT volume (≤4.0 vs >4.0 to 10.0
vs >10.0 IVT/month).
Standard Protocol Approvals, Registrations,
and Patient Consents
This was an investigator-initiated project. The first and last
authors wrote the first draft of the manuscript with subsequent input of all coauthors. There were no external
funding sources. The institutional review boards from the
coordinating sites (Emory University School of Medicine and
Boston University School of Medicine) considered that the
investigators did not have access to identifiable protected
health information and thus no informed consent or institutional review board oversight was required since the study
did not meet the federal description of human subject
research.
Data Availability
The authors declare that all supporting data are available
within the article. Supplemental data are available from Dryad
(tables e-1 to e-6, figure e-1, e-2, doi.org/10.5061/dryad.
g1jwstqpw). Anonymized data are available upon reasonable
request.
Statistics
The monthly volumes for IVT and stroke hospitalizations
were compared for the period before (1 year and immediately
before) and during the COVID-19 pandemic. The normality
of the data was tested with the Shapiro-Wilk test. The nonparametric Wilcoxon signed-rank test was applied to compare
differences in monthly volume between 2 time periods. The
analyses were repeated in the setting of low, intermediate, and
high COVID-19 and stroke volume hospitals.
Figure 1 Monthly Stroke vs Coronavirus Disease 2019 (COVID-19) Admissions
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We looked at the percentage change in the number of IV
thrombolysis and stroke admissions before and during the
COVID-19 pandemic. The 95% confidence intervals (CIs)
for percentage change were calculated using the Wilson
procedure without correction for continuity. The relative
percentage decrease in volume between low, intermediate,
and high-volume hospitals was tested using the z test of
proportion. All data were analyzed using SAS version 9.4 (SAS
Institute) and the significance level was set at a p value of
< 0.05.
Results
There were 82,465, 91,373, and 80,894 stroke hospitalizations
(overall n = 254,732) and 12,527, 13,334 and 11,570 IVT
therapies (overall n = 37,431) included across the 4-month
prior-year pandemic, 4-month immediately prepandemic, and
4-month pandemic periods, respectively. Country-specific
data contributions and relative changes across the pandemic
are summarized in table e-3 (doi.org/10.5061/dryad.
g1jwstqpw).
Stroke Hospitalization
Monthly stroke hospitalization as compared with COVID-19
hospitalization volumes are represented in figure 1. In the
primary analysis, there were 91,373 hospitalizations in the 4
months of the prepandemic period compared to 80,894
during the pandemic months, representing an 11.5% drop
(95% CI −11.7 to −11.3, p < 0.0001; monthly median
[interquartile range (IQR)] stroke hospitalization volume/
center 54.0 [30.8–86.5] to 43.0 [24.3–71.3], p < 0.0001, n =
325 sites) (table 1). There was geographic variation of the
decline in stroke hospitalization: Asia, −6.5% (95% CI −6.8 to
−6.3, p<0.0001); North America, −18.8% (95% CI −19.3 to
−18.3, p < 0.0001); Europe, −10.9% (95% CI −11.3 to −10.5,
Table 1 Stroke Volumes Immediately Before and During the Coronavirus Disease 2019 (COVID-19) Pandemic
Overall volume
Monthly volume, median (IQR)
Relative (%)
change, % (95%
CI)
Immediately
before
During
COVID-19
Differencea
(95% CI)
325
54.0
(30.8–86.5)
43.0
(24.3–71.3)
−6.7 (−8.3 to
−5.8)
<0.0001
<0.0001
85
51.5
(24.5–89.8)
46.3
(21.5–86.3)
−3.0 (−5.0 to
1.5)
0.002
−12.0 (−12.4 to
−11.6)
<0.0001
102
50.2
(27.8–83.0)
38.8
(24.5–68.0)
−7.5 (−9.0 to
−4.0)
<0.0001
21,913
−17.5 (−18.0 to
−17.1)
<0.0001
91
61.3
(48.5–96.3)
49.0
(35.8–71.3)
−11.3 (−13.8
to −8.0)
<0.0001
10,518
8,951
−14.9 (−15.6 to
−14.2)
<0.0001
113
23.5
(16.5–31.0)
20.3
(12.0–25.8)
−3.2 (−4.3 to
−2.0)
<0.0001
108
23,698
19,449
−17.9 (−18.4 to
−17.5)
<0.0001
108
55.1
(48.0–61.3)
43.3
(37.6–52.4)
−9.6 (−11.0
to −7.7)
<0.0001
104
57,157
52,494
−8.2 (−8.4 to −7.9)
<0.0001
104
105.2
(87.9–146.3)
94.7
(72.4–145.3)
−11.8 (−16.0
to −8.5)
<0.0001
Primary
89
14,782
12,222
−17.3 (−17.9 to
−16.7)
<0.0001
89
31.5
(19.8–52.0)
26.0
(13.3–42.0)
−5.3 (−8.0 to
4.0)
<0.0001
Comprehensive
236
76,591
68,672
−10.3 (−10.6 to
−10.1)
<0.0001
236
61.3 (39.1 to
95.9)
51.4
(30.4–85.7)
−7.5 (−9.2 to
−6.0)
<0.0001
p Value
N
−11.5 (−11.7 to
−11.3)
<0.0001
28,890
−3.2 (−3.4 to −3.0)
24,849
21,879
91
26,575
Low
113
Intermediate
High
N
n1
n2
325
91,373
80,894
Low
85
29,835
Intermediate
102
High
Overall
p Value
Hospital COVID-19
volumeb
Hospital stroke
volumec
Primary vs
comprehensive
stroke centerd
Abbreviations: CI = confidence interval; IQR = interquartile range; N = number of hospitals; n = number of admissions.
n1 and immediately before are based on 4 months before the pandemic (November 2019 to February 2020). n2 and during COVID-19 are based on March
2020 to June 2020. p Values are from Poisson means test (overall volume analysis) and Wilcoxon signed-rank test (monthly volume analysis).
a
Difference denotes the median difference between the 2 time periods.
b
p: Low vs intermediate <0.0001; low vs high <0.0001; intermediate vs high <0.0001.
c
p: Low vs intermediate <0.0001; low vs high <0.0001; intermediate vs high <0.0001.
d
p: Primary vs comprehensive <0.0001.
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p<0.0001); South America, −17.4% (95% CI −18.5 to
−16.3, p < 0.0001); Africa, −30.2% (95% CI −32.2 to −28.3,
p < 0.0001); whereas Oceania (−1.9%; 95% CI −2.5 to −1.5, p
= 0.3) did not demonstrate significance (table e-1, doi.org/10.
5061/dryad.g1jwstqpw). PSCs −17.3% (95% CI −17.9 to
−16.7, n = 89) demonstrated greater declines compared to
CSCs−10.3% (95% CI −10.6 to −10.1, n = 236) (table 1).
IV Thrombolysis
IV thrombolytic volumes declined with 13,334 interventions
in the prepandemic period vs 11,570 during the pandemic,
representing a 13.2% drop (95% CI −13.8 to −12.7, p < 0.001;
median [IQR] monthly IVT volume/center 6.5 [2.8–12.0] to
5.3 [2.0–10.5], p < 0.001, n = 389 centers) (table 2, figure 2).
IVT decline was seen in most continents: Asia, −9.9% (95%
CI −11.0 to −8.9, p<0.0001); North America, −14.4% (95%
CI −15.6 to −13.3, p < 0.0001); Europe, −13.5% (95% CI
−14.4 to −12.6, p < 0.0001); South America, −24.2% (95% CI
−27.6 to −21.0, p < 0.0001); Africa −23.5% (95% CI −29.8 to
−18.2, p < 0.01). There was no appreciable difference in IVT
in Oceania −1.9% (95% CI −3.9 to −0.92, p = 0.7) (table e-2,
doi.org/10.5061/dryad.g1jwstqpw). IVT declines were
greater in PSCs −15.5% (95% CI −16.9 to −14.2, n = 138
centers) vs CSCs −12.6% (95% CI −13.3 to −12.0, n = 251
centers, p = 0.0001) (table 2).
Recovery of Stroke and IVT Volume Analysis
In the recovery analysis, there were 38,616 stroke hospitalizations in the early 2 months of the pandemic compared to
42,278 stroke hospitalizations in the later 2 pandemic months,
representing an increase of 9.5% (95% CI 9.2–9.8, p < 0.0001,
n = 325 centers). The recovery in stroke hospitalization volume was seen in all strata of COVID-19 hospitalization burden, with a gradient of recovery more significant in low
Table 2 Tissue Plasminogen Activator (tPA) Procedure Volumes Immediately Before and During the Coronavirus Disease
2019 (COVID-19) Pandemic
Overall volume
Monthly volume, median (IQR)
Relative (%)
change, % (95%
CI)
p Value
N
Immediately
Before
During
COVID-19
Differencea
(95% CI)
−13.2 (−13.8 to
−12.7)
<0.0001
389
6.5 (2.8–12.0)
5.3
(2.0–10.5)
−0.75 (−1.0
to −0.50)
<0.0001
2,871
−9.2 (−10.3 to
−8.2)
<0.0001
112
3.5 (1.5–8.5)
3.1
(1.3–8.1)
−0.25 (−0.50
to −0.19)
<0.0001
3,373
2,947
−12.6 (−13.8 to
−11.6)
<0.0001
102
6.3 (3.3–13.0)
5.3
(2.5–10.8)
−0.75 (−1.0
to −0.25)
<0.0001
96
4,252
3,439
−19.1 (−20.3 to
−18.0)
<0.0001
96
9.1 (5.6–15.3)
7.5
(4.0–12.5)
−1.9 (−2.5 to
−1.0)
<0.0001
Low
133
1,052
929
−11.7 (−13.8 to
−9.9)
0.003
133
1.8 (1.5–2.8)
1.3
(1.0–2.5)
−0.19 (−0.25
to −0.19)
0.007
Intermediate
133
3,553
3,049
−14.2 (−15.4 to
−13.1)
<0.0001
133
6.8 (5.0–8.0)
5.3
(3.8–7.3)
−1.0 (−1.5 to
−0.75)
<0.0001
High
123
8,729
7,592
−13.0 (−13.8 to
−12.3)
<0.0001
123
15.3
(12.3–19.5)
13.8
(10.3–17.8)
−2.3 (−3.0 to
−1.5)
<0.0001
Primary
138
2,763
2,334
−15.5 (−16.9 to
−14.2)
<0.0001
138
3.1 (1.5–6.5)
2.1
(1.3–5.5)
−0.25 (−0.75
to 0.19)
<0.0001
Comprehensive
251
10,571
9,236
−12.6 (−13.3 to
−12.0)
<0.0001
251
8.8 (4.5–14.0)
7.3
(3.5–12.8)
−1.0 (−1.3 to
−0.50)
<0.0001
N
n1
n2
389
13,334
11,570
Low
112
3,162
Intermediate
102
High
Overall
p Value
Hospital COVID-19
volumeb
Hospital IV tPA
volumec
Primary vs
comprehensive stroke
centerd
Abbreviations: CI = confidence interval; IQR = interquartile range; N = number of hospitals; n = number of procedures.
n1 and immediately before are based on 4 months before the pandemic (November 2019 to February 2020). n2 and during COVID-19 are based on March
2020 to June 2020. p Values are from Poisson means test (overall volume analysis) and Wilcoxon signed-rank test (monthly volume analysis).
a
Difference denotes the median difference between the 2 time periods.
b
p: Low vs intermediate <0.0001; low vs high <0.0001; intermediate vs high <0.0001.
c
p: Low vs intermediate 0.038; low vs high 0.234; intermediate vs high 0.076.
d
p: Primary vs comprehensive 0.0001.
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Figure 2 Monthly IV Thrombolysis (IVT) vs Coronavirus Disease 2019 (COVID-19) Admissions
(14.6%; 95% CI 14.0–15.2, p < 0.0001) vs intermediate
(9.0%; 95% CI 8.4–9.5, p < 0.0001) vs high-volume (4.6%;
95% CI 4.2–5.0, p < 0.0001) COVID-19 hospitalization.
There was a gradient in stroke hospitalization recovery by
baseline hospital stroke volume, significant in high-volume
(13.9%; 95% CI 13.5–14.3, p < 0.0001) stroke centers compared to intermediate or low volume centers, which in their
strata did not demonstrate significance in recovery. Stroke
hospitalization volume recovery was more significant in CSCs
(10.9%; 95% CI 10.6–11.3, p < 0.0001) compared to PSCs
(1.8%; 95% CI 1.5–2.1, p = 0.3) (table 3).
IV thrombolysis was administered to 5,714 patients in the
early pandemic compared to 5,856 patients in the later pandemic months, representing a nonsignificant increase of 2.5%
(95% CI 2.1–2.9, p = 0.19). Recovery in IVT volume was
more significant in intermediate (6.1%, 95% CI 5.0–7.4) vs
low (2.6%, 95% CI 1.9–3.6, p < 0.0001) COVID-19 hospitalization centers. A trend in IVT volume recovery was seen
with CSCs (4.1%, 95% CI 3.6–4.7, p = 0.053).
IVT Transfer Analysis
There were 1,337 IVT transfers in the prepandemic compared
to 1,178 in the pandemic months, representing an 11.9% drop
(95% CI −13.7 to −10.3, p = 0.001). The IVT transfer declines
were significant in the strata of hospitals with low (−18.3%,
95% CI −23.9 to −13.9, p = 0.03) and high (−14.9%, 95% CI
−18.1 to −12.1, p = 0.008) COVID-19 volume (table 4).
Secondary Analysis
Table 5 reveals the volumes for stroke hospitalizations, IVT,
and IVT transfers during the first 4 months of the pandemic vs
the corresponding period in the prior year. There were
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significant declines in the overall and monthly volumes for all
metrics.
Intersection of COVID-19, SARS-CoV-2 Infection,
and Stroke Hospitalizations
A total of 269 centers provided data on SARS-CoV-2 infection
and diagnosis of stroke in the same patient. A diagnosis of any
stroke was present in 1.48% (1778/119,967) of COVID-19
hospitalizations, with continental variation: Africa 1.6% (47/
2879), Asia 1.5% (317/20,858), Oceania 0.4% (1/257),
Europe 1.4% (507/36,871), North America 1.2% (615/
49,237), South America 3.0% (291/9,865) (table e-5, doi.
org/10.5061/dryad.g1jwstqpw).
SARS-CoV-2 infection was present in 3.3% (1722/52,026) of
stroke hospitalizations (table e-5, doi.org/10.5061/dryad.
g1jwstqpw) with continental variation: Africa 3.1% (56/
1828), Asia 2.7% (342/12,686), Oceania 0.1% (1/932),
Europe 3.3% (502/15,220), North America 3.0% (527/
17,855), South America 8.4% (294/3,505) (table e-6, doi.
org/10.5061/dryad.g1jwstqpw).
Discussion
In this temporal analysis of more than 254,000 stroke
hospitalizations worldwide, there was a global decrease in
stroke admissions (−11.5%), IV thrombolysis (−13.2%),
and IVT transfers (−11.9%) during the first 4 pandemic
months, compared to the immediately preceding period,
confirming our primary hypothesis. A decrease in volume
was also seen in relation to the equivalent period in the
prior year for all metrics. The declines in both stroke
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e2829
Table 3 Stroke and IV Tissue Plasminogen Activator (tPA) Overall Volumes During Early and Late Coronavirus Disease
2019 (COVID-19) Pandemic
Strokea
IV tPAb
N
Early
COVID19
Late
COVID19
Relative (%)
change, % (95% CI)
p
Value
<0.0001
389
5,714
5,856
2.5 (2.1 to −2.9)
0.187
14.6 (14.0 to 15.2)
<0.0001
112
1,417
1,454
2.6 (1.9 to 3.6)
0.490
11,408
9.0 (8.4 to 9.5)
<0.0001
102
1,430
1,517
6.1 (5.0 to 7.4)
0.109
10,712
11,201
4.6 (4.2 to 5.0)
0.001
96
1,717
1,722
0.29 (0.12 to 0.68)
0.932
113
4,468
4,483
0.34 (0.21 to 0.56)
0.874
133
464
465
0.22 (0.04 to 0.12)
0.974
Intermediate
108
9,604
9,845
2.5 (2.2 to 2.8)
0.084
133
1,525
1,524
0.07 (0.01 to 0.38)
0.986
High
104
24,544
27,950
13.9 (13.5 to 14.3)
<0.0001
123
3,725
3,867
3.8 (3.2 to 4.5)
0.103
Primary
89
6,057
6,165
1.8 (1.5 to 2.1)
0.329
138
1,189
1,145
−3.7 (−2.8 to −4.9)
0.363
Comprehensive
236
32,559
36,113
10.9 (10.6 to 11.3)
<0.0001
251
4,525
4,711
4.1 (3.6 to 4.7)
0.053
N
Early
COVID-19
Late
COVID-19
Relative (%)
change, % (95%
CI)
p Value
325
38,616
42,278
9.5 (9.2 to 9.8)
Low
85
13,461
15,429
Intermediate
102
10,471
High
91
Low
Overall
Hospital COVID-19
volume
Hospital stroke/IV
tPA volume
Primary vs
comprehensive
stroke center
Abbreviations: CI = confidence interval; N = number of hospitals.
The early and late COVID-19 periods are based on March 2020 to April 2020 and May 2020 to June 2020, respectively. p Value is from Poisson means test.
Stroke volume analysis. Hospital COVID-19 volume: low vs intermediate <0.0001; low vs high <0.0001; intermediate vs high <0.0001. Hospital stroke volume:
low vs intermediate <0.0001; low vs high <0.0001; intermediate vs high <0.0001. Primary vs comprehensive <0.0001.
b
IV tPA volume analysis. Hospital COVID-19 volume: low vs intermediate <0.0001; low vs high <0.0001; intermediate vs high <0.0001. IV tPA volume: low vs
intermediate 0.383; low vs high 0.0001; intermediate vs high <0.0001. Primary vs comprehensive = NA.
a
hospitalization and IVT were greater in PSCs compared to
CSCs. Recovery of stroke hospitalization volume (+9.5%)
was noted in the 2 subsequent months vs the 2 initial
months of the pandemic, with greater recovery in hospitals
with lower COVID-19 hospitalization volume, highvolume stroke centers, and CSCs.
Table 4 Tissue Plasminogen Activator (tPA) Transfer Volumes Immediately Before and During the Coronavirus Disease
2019 (COVID-19) Pandemic
Overall volume
Monthly volume, median (IQR)
N
n1
n2
Relative (%) change, %
(95% CI)
p
Value
N
Immediately
before
During
COVID-19
Differencea
(95% CI)
p
Value
39
1,337
1,178
−11.9 (−13.7 to −10.3)
0.001
39
7.5 (5.8 to 11.3)
7.3 (5.0 to
9.5)
−0.75 (−1.3 to
0.0)
0.027
Low
7
229
187
−18.3 (−23.9 to −13.9)
0.032
7
6.5 (5.8 to 8.5)
6.8 (6.5 to
7.5)
−1.0 (−9.8 to
1.8)
0.688
Intermediate
14
428
404
−5.6 (−8.2 to −3.8)
0.341
14
7.5 (4.5 to 11.5)
7.5 (4.3 to
9.8)
−0.38 (−1.8 to
1.3)
0.352
High
14
538
458
−14.9 (−18.1 to −12.1)
0.008
14
8.0 (6.0 to 11.3)
6.8 (5.3 to
9.5)
−1.3 (−2.5 to
1.3)
0.107
Overall
Hospital COVID-19
volumeb
Abbreviations: CI = confidence interval; IQR = interquartile range; N = number of hospitals; n = number of transfers.
n1 and immediately before are based on 4 months before the pandemic (November 2019 to February 2020). n2 and during COVID-19 are based on March
2020 to June 2020. p Values are from Poisson means test (overall volume analysis) and Wilcoxon signed-rank test (monthly volume analysis).
a
Difference denotes the median difference between the 2 time periods.
b
p: Low vs intermediate <0.0001; low vs high 0.239; intermediate vs high <0.0001.
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Table 5 Overall and Monthly Volumes 1 Year Before and During Coronavirus Disease 2019 (COVID-19) Pandemic
Overall volume
Monthly volume, median (IQR)
1 year
before
During
COVID-19
Differencea
(95% CI)
297
50.3 (28.3 to
80.8)
42.0 (24.3 to
70.3)
−5.8 (−7.8 to
−4.5)
<0.0001
<0.0001
377
6.0 (2.3 to
12.0)
5.3 (2.0 to
10.5)
−0.50 (−0.75 to
−0.25)
<0.0001
<0.0001
36
7.6 (5.3 to
12.0)
7.5 (5.5 to
9.5)
−1.1 (−2.0 to
0.25)
0.038
N
n1
n2
Relative (%) change, %
(95% CI)
p Value
N
Stroke
297
82,465
72,554
−12.0 (−12.2 to −11.8)
<0.0001
IV tPA
377
12,527
11,198
−10.6 (−11.2 to −10.1)
IV tPA
transfer
36
1,331
1,140
−14.4 (−16.3 to −12.6)
p Value
Abbreviations: CI = confidence interval; IQR = interquartile range; N = number of hospitals; n = number of admissions/procedures/transfers; tPA = tissue
plasminogen activator.
n1 and 1 year before are based on 4-month data 1 year before the pandemic (March 2019 to June 2019). n2 and during COVID-19 are based on data from
March 2020 to June 2020. p Values are from Poisson means test (overall volume analysis) and Wilcoxon signed-rank test (monthly volume analysis).
a
Difference denotes the median difference between the 2 time periods.
The decreases in the volume of stroke care provided were
noted across centers with high, intermediate, and low
COVID-19 hospitalization burden, and also across high, intermediate, and low volume stroke and IVT centers. As hypothesized, the magnitude of decrease of stroke
hospitalizations and IVT was greater in centers with higher
COVID-19 inpatient volumes.
Our results concur with other recent reports on the collateral
effects of the COVID-19 pandemic on stroke systems of care
including studies from China,11 Italy,15 Spain,10 France,12,16
Germany,17 Brazil,18 Canada,19 and the United States.9,20-22
Although prior analyses have described temporal and regional
changes in stroke hospitalizations and IVT, this is among the
first descriptions of the change at a global level, including
primary and CSCs. Hospital access related to high COVID-19
burden was unlikely a factor, as the decline was seen in centers
with few or no patients with COVID-19.23,24 Patient fear of
contracting COVID-19 may have played a role, along with a
decrease in presentation of TIA, mild, or moderate strokes, as
reported by Diegoli et al.18 Physical distancing measures may
have prevented patients from the timely witnessing of a
stroke. Similar to cardiovascular events, it is conceivable that
there was a true population-level reduction in cerebrovascular
events, possibly related to decreased consumption of highsodium, fast foods, reduced exposure to ambient air pollution,
or improvement in patient behaviors.24 A reduction in exposure to other common viruses that may play a role in
triggering vascular events may have also reduced stroke risk.
In the recovery analysis, there was a gradient of recovery in
stroke hospitalization in hospitals with lower compared to
higher COVID-19 burden. CSCs and high-volume stroke
centers demonstrated greater recovery, suggesting patients
with a higher acuity of care needs seeking care in these
comprehensive centers.
Our subgroup of 264 centers including 119,967 COVID-19
hospitalizations expands on prior mechanical thrombectomy
Neurology.org/N
analysis that was limited to CSCs (Nogueira) and represents
the largest sample reporting the concomitant diagnoses of
stroke and SARS-CoV-2 infection to date. Our 1.48% stroke
rate in COVID-19 hospitalizations is similar to the pooled
incidence of 1.1%–1.2% (range, 0.9%–2.7%) of hospitalized
patients with COVID-19.4 The higher rate may be explained
in part by the higher number of patients contracting SARSCoV-2 over time and higher availability of testing. Some
variation in the proportions are expected given the different
definitions (all strokes vs ischemic only) and populations
involved (all hospitalized vs severely infected only) across
studies. We also provide another perspective on this relationship by reporting an incidence of 3.3% (1722/52,026)
for SARS-CoV-2 infection across all stroke hospitalizations
among centers with documented COVID-19 hospitalization.
Finally, 25 years after the landmark National Institute of
Neurological Disorders and Stroke trials showing the benefit
of tPA, we learned from this global analysis that as of 2020, the
availability of IVT for acute stroke therapy continues to be
lacking in multiple countries in Africa (i.e., Nigeria, Kenya,
Zimbabwe, Ghana, Ethiopia, Sudan) owing to its high cost
and relative implementation complexity, limiting our analysis
of temporal IVT treatment trends for this continent. This void
highlights a disparity of access to basic stroke therapy in
multiple low-income countries across the world.
To our knowledge, this is the largest global study to date evaluating the intersection of the COVID-19 pandemic with stroke
care. Our study included the participation of diverse geography of
centers from 6 continents, 70 countries, and 457 CSCs and PSCs.
Our study has several limitations. The diagnosis of stroke/
TIA in some centers was obtained using administrative coding
of hospital ICD codes and hence there is a possibility of
misclassification of diagnosis, potentially compounded by
regional and national variations in stroke diagnosis and delivery of care. However, centers contributing to these data
have systems to track stroke metrics of care, thus the relative
Neurology | Volume 96, Number 23 | June 8, 2021
Copyright © 2021 American Academy of Neurology. Unauthorized reproduction of this article is prohibited.
e2831
changes in volume from this analysis are likely robust. Details
on patient-level data including demographics, stroke subtypes, and clinical outcomes were not collected as these were
outside the scope of the study. The definition of the pandemic
period was arbitrary because the outbreak started and peaked
at different times at different locations. This led to the computation of relative increases in volumes during the study
period in the earlier affected regions, such as China, resulting
in a potential underestimation of the global effect. Finally, the
sampling varied with the availability of complete data in each
subset of the analysis.
The COVID-19 pandemic was associated with an initial global
decline in the volume of stroke hospitalizations, IVT, and
interfacility IVT transfers. These reductions were observed
regardless of COVID-19 hospitalization burden and prepandemic stroke and IVT volumes. PSCs and centers with higher
COVID-19 inpatient volumes experienced steeper declines.
Recovery of stroke hospitalization but not IVT volume was
noted in the later phase of the pandemic months and associated
with lower COVID-19 hospital burden, high volume, and
CSCs. The findings of our study can inform future studies,
preparedness,25-27 and local policies in the event of a second
COVID-19 surge or future pandemic.
Author Byline (Continued)
Lenon Gwaunza, MBChB, MSc, Gift Wilson
Ngwende, MBChB, FCP, David Sahakyan, MD, Aminur
Rahman, MBBS, FCPS, MD, FINR, Zhibing Ai, MS, Fanghui
Bai, MD, Zhenhui Duan, MD, MS, Yonggang Hao, MD,
Wenguo Huang, MS, Guangwen Li, MD, Wei Li, MD,
Ganzhe Liu, MD, Jun Luo, MD, MS, Xianjin Shang, MD, Yi
Sui, MBBS, PhD, Ling Tian, MD, Hongbin Wen, MD, Bo
Wu, MD, Yuying Yan, MD, Zhengzhou Yuan, MD, Hao
Zhang, MD, PhD, Jun Zhang, MD, Wenlong Zhao, MD,
Wenjie Zi, MD, Thomas W. Leung, MD, Chandril
Chugh, MD, Vikram Huded, MD, Bindu Menon, MD, FRCP,
Jeyaraj Durai Pandian, MD, PN Sylaja, MD, Fritz Sumantri
Usman, Mehdi Farhoudi, MD, Elyar Sadeghi
Hokmabadi, MD, Anat Horev, MD, Anna Reznik, MA, Rotem
Sivan Hoffmann, MD, Nobuyuki Ohara, MD, Nobuyuki
Sakai, MD, DMSc, Daisuke Watanabe, MD, PhD, Ryoo
Yamamoto, MD, PhD, Ryosuke Doijiri, MD, Naoki
Tokuda, MD, PhD, Takehiro Yamada, MD, Tadashi
Terasaki, MD, Yukako Yazawa, MD, Takeshi Uwatoko, MD,
Tomohisa Dembo, MD, PhD, Hisao Shimizu, MD, Yuri
Sugiura, MD, Fumio Miyashita, MD, Hiroki Fukuda, MD,
PhD, Kosuke Miyake, MD, Junsuke Shimbo, MD, PhD,
Yusuke Sugimura, MD, Yoshiki Yagita, MD, PhD, Yohei
Takenobu, MD, PhD, Yuji Matsumaru, MD, PhD, Satoshi
Yamada, MD, PhD, Ryuhei Kono, MD, Takuya
Kanamaru, MD, PhD, Hidekazu Yamazaki, MD, Manabu
Sakaguchi, MD, PhD, Kenichi Todo, MD, PhD, Nobuaki
Yamamoto, MD, PhD, Kazutaka Sonoda, MD, Tomoko
Yoshida, MD, Hiroyuki Hashimoto, MD, PhD, Ichiro
Nakahara, MD, PhD, Aida Kondybayeva, MD, Kamila
Faizullina, MD, PhD, Saltanat Kamenova, MD, Murat
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Zhanuzakov, MD, Jang-Hyun Baek, MD, Yangha
Hwang, MD, PhD, Jin Soo Lee, MD, Si Baek Lee, MD, Jusun
Moon, MD, Hyungjong Park, MD, Jung Hwa Seo, MD,
Kwon-Duk Seo, MD, Sung Il Sohn, MD, PhD, Chang Jun
Young, MD, Rechdi Ahdab, MD, PhD, Wan Asyraf Wan
Zaidi, MMed, Zariah Abdul Aziz, MMed, Hamidon bin
Basri, MD, Law Wan Chung, MD, Aznita Binti
Ibrahim, MMed, Khairul Azmi Ibrahim, MMed, Irene
Looi, MBBS, Wee Yong Tan, MD, MRCP, Nafisah Wan
Yahya, MMed, Stanislav Groppa, MD, PhD, Pavel
Leahu, MD, Amal M. Al Hashmi, MD, Yahia Zakaria
Imam, MBBS, MD, MRCP, Naveed Akhtar, MD, Maria
Carissa Pineda-Franks, MD, Christian Oliver Co, MD, Dmitriy Kandyba, MD, Adel Alhazzani, MD, Hosam AlJehani, MBBS, MSc, Carol Huilian Tham, MBBS, MMed,
MRCP, Marlie Jane Mamauag, MD, Narayanaswamy
Venketasubramanian, FRCP, Chih-Hao Chen, MD, PhD,
Sung-Chun Tang, MD, PhD, Anchalee Churojana, MD, Esref
Akil, MD, özlem aykaç, MD, Atilla Ozcan Ozdemir, MD,
Semih Giray, MD, Syed Irteza Hussain, MD, Seby John, MD,
Huynh Le Vu, MD, Anh Duc Tran, MD, Huy Hoang
Nguyen, MD, Thong Nhu Pham, MD, Thang Huy
Nguyen, MD, Trung Quoc Nguyen, MD, Thomas
Gattringer, MD, PhD, Christian Enzinger, MD, Monika
Killer-Oberpfalzer, MD, PhD, Flavio Bellante, MD, Sofie De
Blauwe, MD, Geert Vanhooren, MD, Sylvie De Raedt, MD,
PhD, Anne Dusart, MD, Robin Lemmens, MD, PhD, Noemie
Ligot, MD, Matthieu Pierre Rutgers, MD, Laetitia
Yperzeele, MD, PhD, Filip Alexiev, MD, PhD, Teodora
Sakelarova, MD, Marina Roje Bedeković, MD, PhD, Hrvoje
Budincevic, MD, PhD, Igor Cindric, MD, Zlatko Hucika, MD,
David Ozretic, MD, Majda Seferovic Saric, PhD, František
Pfeifer, MD, Igor Karpowic, MD, David Cernik, MD, Martin
Sramek, MD, Miroslav Skoda, MD, Helena Hlavacova, MD,
Lukas Klecka, MD, Martin Koutny, MD, Daniel
Vaclavik, MD, Ondrej Skoda, MD, Jan Fiksa, MD, Katerina
Hanelova, MD, Miroslava Nevsimalova, MD, Robert
Rezek, MD, Petr Prochazka, MD, Gabriela Krejstova, MD, Jiri
Neumann, MD, Marta Vachova, MD, Henryk
Brzezanski, MD, David Hlinovsky, MD, Dusan Tenora, MD,
Rene Jura, MD, Lubomı́r Jurák, MD, Jan Novak, MD, Ales
Novak, MD, Zdenek Topinka, MD, Petr Fibrich, MD, Helena
Sobolova, MD, Ondrej Volny, MD, PhD, Hanne Krarup
Christensen, MD, PhD, Nicolas Drenck, Bsc, Helle Klingenberg Iversen, MD DMSci, Claus Z. Simonsen, MD, PhD,
Thomas Clement Truelsen, MD, PhD, Troels Wienecke, MD,
PhD, Riina Vibo, MD, PhD, Katrin Gross-Paju, MD, PhD,
Toomas Toomsoo, MD, PhD, Katrin Antsov, MD, Francois
Caparros, MD, MSc, Charlotte Cordonnier, MD, PhD, Maria
Dan, MD, Jean-Marc Faucheux, MD, Laura Mechtouff, MD,
Omer Eker, MD, PhD, Emilie Lesaine, MD, Basile
Ondze, MD, Roxane Peres, MD, Fernando Pico, MD, PhD,
Michel Piotin, MD, PhD, Raoul Pop, MD, PhD, Francois
Rouanet, MD, Tatuli Gubeladze, MD, PhD, Mirza
Khinikadze, MD, PhD, Nino Lobjanidze, MD, Alexander
Tsiskaridze, MD, PhD, Simon Nagel, MD, Peter Arthur
Ringleb, MD, Michael Rosenkranz, MD, Holger
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Schmidt, MBBS, Annahita Sedghi, MD, Timo
Siepmann, MD, Kristina Szabo, MD, Götz Thomalla, MD,
Lina Palaiodimou, MD, Dimitrios Sagris, MD, Odysseas
Kargiotis, MD, Peter Klivenyi, MD, PhD, Laszlo Szapary, MD,
PhD, Gabor Tarkanyi, MD, Alessandro Adami, MD, Fabio
Bandini, MD, Paolo Calabresi, MD, Giovanni Frisullo, MD,
PhD, Leonardo Renieri, MD, Davide Sangalli, MD, Anne
Pirson, MD, Maarten Uyttenboogaart, MD, PhD, Ido van den
Wijngaard, MD, PhD, Espen Saxhaug Kristoffersen, MD,
PhD, Waldemar Brola, MD, PhD, Małgorzata Fudala, MD,
PhD, Ewa Horoch-Lyszczarek, MD, Michal Karlinski, MD,
PhD, Radoslaw Kazmierski, MD, PhD, Pawel Kram, MD,
Marcin Rogoziewicz, MD, PhD, Rafal Kaczorowski, MD,
Piotr Luchowski, MD, Halina Sienkiewicz-Jarosz, MD, PhD,
Piotr Sobolewski, MD, PhD, Waldemar Fryze, MD, PhD,
Anna Wisniewska, MD, Malgorzata Wiszniewska, MD, PhD,
Patricia Ferreira, MD, Paulo Ferreira, MD, Luisa
Fonseca, MD, João Pedro Marto, MD, Teresa Pinho e
Melo, MD, Ana Paiva Nunes, MD, Miguel Rodrigues, MD,
MSc, Vı́tor Tedim Cruz, MD, PhD, Cristian FalupPecurariu, MD, PhD, Georgi Krastev, MD, PhD, Miroslav
Mako, MD, Marı́a Alonso de Leciñana, MD, PhD, Juan F.
Arenillas, MD, Oscar Ayo-Martin, MD, PhD, Antonio Cruz
Culebras, MD, Exuperio Diez Tejedor, MD, PhD, Joan
Montaner, MD, PhD, Soledad Pérez-Sánchez, MD, PhD,
Miguel Angel Tola Arribas, MA, MD, PhD, Alejandro
Rodriguez Vasquez, MD, Michael Mayza, MD, PhD, Gianmarco Bernava, MD, Alex Brehm, MD, Paolo Machi, MD,
PhD, Urs Fischer, MD, MSc, Jan Gralla, MD, Patrik L.
Michel, MD, Marios-Nikos Psychogios, MD, Davide
Strambo, MD, Soma Banerjee, MD, Kailash Krishnan, MRCP,
PhD, Joseph Kwan, MD, MPhil, FRCP, Asif Butt, MBBS,
Luciana Catanese, MD, Andrew M. Demchuk, MD, Thalia
Field, MD, MHSc, Jennifer Haynes, RN, Michael D. Hill, MD,
MSc, Houman Khosravani, MD, PhD, Ariane Mackey, MD,
Aleksandra Pikula, MD, Gustavo Saposnik, MD, MPH,
FRCPc,
Courtney
Anne
Scott,
MD,
Ashkan
Shoamanesh, MD, Ashfaq Shuaib, MD, Samuel Yip, MD,
PhD, Miguel A. Barboza, MD, MSc, Jose Domingo
Barrientos, MD, MSc, Ligia Ibeth Portillo Rivera, MD, Fernando Gongora-Rivera, MD, MSc, Nelson NovarroEscudero, MD, MSc, Anmylene Blanco, MD, Michael
Abraham, MD, Diana Alsbrook, MD, Dorothea Altschul, MD,
Anthony J. Alvarado-Ortiz, DO, Ivo Bach, MD, Aamir
Badruddin, MD, Nobl Barazangi, MD, PhD, Charmaine
Brereton, RN, MSN, Alicia Castonguay, PhD, Seemant
Chaturvedi, MD, Saqib A. Chaudry, MD, Hana Choe, MD,
Jae H. Choi, MD, Sushrut Dharmadhikari, MD, Kinjal
Desai, MD, MPH, Thomas G. Devlin, MD, PhD, Vinodh T.
Doss, MD, Randall Edgell, MD, Mark Etherton, MD, PhD,
Mudassir Farooqui, MBBS, Don Frei, MD, Dheeraj
Gandhi, MD, Mikayel Grigoryan, MD, Rishi Gupta, MD,
Ameer E. Hassan, DO, Johanna Helenius, MD, PhD, Artem
Kaliaev, MD, Ritesh Kaushal, MD, PhD, Priyank
Khandelwal, MD, Ayaz M. Khawaja, MD, Naim N.
Khoury, MD, MS, Benny S. Kim, MD, Dawn O.
Kleindorfer, MD, Feliks Koyfman, MD, Vivien H. Lee, MD,
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Lester Y. Leung, MD, MSc, Guillermo Linares, MD, Italo
Linfante, MD, Helmi L. Lutsep, MD, Lisa Macdougall, RN,
MS, Shailesh Male, MD, Amer M. Malik, MD, Hesham
Masoud, MD, Molly McDermott, MD, Brijesh P. Mehta, MD,
Jiangyong Min, MD, PhD, Manoj Mittal, MD, Jane G.
Morris, MD, Sumeet S. Multani, MD, Fadi Nahab, MD,
Krishna Nalleballe, MD, Claude B. Nguyen, MD, Roberta
Novakovic-White, MD, Santiago Ortega-Gutierrez, MD,
Rahul H. Rahangdale, MD, Pankajavalli Ramakrishnan, MD,
PhD, Jose Rafael Romero, MD, Natalia Rost, MD, Aaron
Rothstein, MD, Sean Ruland, DO, Ruchir Shah, MD, Malveeka Sharma, MD, Brian Silver, MD, Marc Simmons, MD,
Abhishek Singh, MD, Amy K. Starosciak, PhD, Sheryl L.
Strasser, MD, Viktor Szeder, MD, PhD, Mohamed
Teleb, MD, Jenny P. Tsai, MD, Barbara Voetsch, MD, PhD,
Oscar Balaguera, MD, Virginia A. Pujol Lereis, MD, Adriana
Luraschi, MD, Marcele Schettini Almeida, MD, Fabricio
Buchdid Cardoso, MD, Adriana Conforto, MD, Leonardo De
Deus Silva, MD, Luidia Varrone Giacomini, MD, Fabricio
Oliveira Lima, MD, MPH, PhD, Alexandre L. Longo, MD,
Pedro S.C. Magalhães, MD, Rodrigo Targa Martins, MD,
Francisco Mont’alverne, MD, PhD, Daissy Liliana Mora
Cuervo, MD, Leticia Costa Rebello, MD, Lenise Valler, MD,
Viviane Flumignan Zetola, MD, PhD, Pablo M. Lavados, MD,
MPH, Victor Navia, MD, Verónica V. Olavarrı́a, MD, Juan
Manuel Almeida Toro, MD, Pablo Felipe Ricardo Amaya,
Hernan Bayona, MD, Angel Corredor, MD, Carlos Eduardo
Rivera Ordonez, MD, Diana Katherine Mantilla Barbosa, MD,
Osvaldo Lara, MD, MSc, Mauricio R. Patiño, MD, Luis Fernando Diaz Escobar, MD, Donoband Edson Dejesus Melgarejo Fariña, MD, Analia Cardozo Villamayor, MD, Adolfo
Javier Zelaya Zarza, MD, Danny Moises Barrientos
Iman, MD, Liliana Rodriguez Kadota, MD, Bruce
Campbell, MBBS, PhD, Graeme J. Hankey, MD, Casey Hair,
Timothy Kleinig, MD, PhD, Alice Ma, MBBS, Rodrigo
Tomazini Martins, MD, PhD, Ramesh Sahathevan, Vincent
Thijs, MD, Daniel Salazar, MD, PhD, FRACP, Teddy YuanHao Wu, MD, PhD, Diogo C. Haussen, MD, David
Liebeskind, MD, Dileep R. Yavagal, MD, Tudor G. Jovin, MD,
Osama O. Zaidat, MD, Thanh N. Nguyen, MD
Affiliation
Department of Neurology (R.G.N., M.H.M., M.Frankel, D.C.H.), Marcus Stroke and Neuroscience Center,
Grady Memorial Hospital, Emory University School of Medicine, Atlanta; Department of Radiology
(M.M.Q., M.A., T.N.N., A.K.) and Radiation Oncology (M.M.Q.), Boston Medical Center, Boston University School of Medicine, Massachusetts; Department of Neurology (S.O.M.), Federal University of Rio
Grande do Sul, Porto Alegre; Hospital de Clı́nicas de Porto Alegre (S.O.M.), Brazil; Department of Stroke
Neurology (H. Yamagami), National Hospital Organization, Osaka National Hospital, Japan; Department of
Neurology (Z.Q.), Xinqiao Hospital of the Army Medical University, Chongqing, China; Department of
Neurology (O.Y.M.), Stroke and Neurointervention Division, Alexandria University Hospital, Alexandria
University, Egypt; Boston University School of Medicine (A.S.), Massachusetts; 2nd Department of Neurology (A.C.), Institute of Psychiatry and Neurology, Warsaw, Poland; Department of Neurology (G.T.,
L.P.), National & Kapodistrian University of Athens, School of Medicine, Attikon University Hospital,
Athens, Greece; Faculdade de Medicina (D.A.d.S.), Universidade de Lisboa, Lisbon, Portugal; Department
of Neurology (J.D., R.L.), Leuven University Hospital, Belgium; International Clinical Research Center and
Department of Neurology (R.M.), St. Anne´s University Hospital in Brno and Faculty of Medicine, Masaryk
University, Brno, Czech Republic; Department of Neurology (P.V.), Groeninge Hospital, Kortrijk; Department of Neurology (P.V.), University Hospitals Antwerp; Department of Translational Neuroscience
(P.V.), University of Antwerp, Belgium; Department of Neurology (J.E.S., T.G.J.), Cooper Neurological
Institute, Cooper University Hospital, Camden, New Jersey; Department of Neurology and Neurosurgery
(J. Kõrv), University of Tartu, Estonia; Department of Neurology (J.B., R.V.,S.R.), Loyola University
Chicago Stritch School of Medicine, Illinois; Department of Neurosurgery (C.W.L.), Kaiser Permanente
Fontana Medical Center; Department of Neurology (N.S.S.), Kaiser Permanente Los Angeles Medical
Neurology | Volume 96, Number 23 | June 8, 2021
Copyright © 2021 American Academy of Neurology. Unauthorized reproduction of this article is prohibited.
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Center; Department of Neurology (A.M.Z., S.A.S.), UT Health McGovern Medical School, Houston, Texas;
Department of Neurology (A.L.Z.), Medical University of South Carolina, Charleston; Department of
Internal Medicine (G.N.), School of Health Sciences, University of Thessaly, Larissa, Greece; Department of
Neurology (K.M., A.T.), Allegheny Health Network, Pittsburgh, Pennsylvania; Department of Neurology
(A.L.), Ohio Health Riverside Methodist Hospital Columbus; Department of Medicine and Neurology
(A.R.), University of Otago and Wellington Hospital, New Zealand; Department of Neurology (E.A.M.),
Vanderbilt University Medical Center, Nashville, Tennessee; Department of Neurology (A.W.A., D. Alsbrook), University of Tennessee Health Center, Memphis; Department of Neurology (D.Y.H.), University
of North Carolina at Chapel Hill; Departments of Neurology (S.Y.) and Radiology (E.R.), New York
University Grossman School of Medicine; Douala Gynaeco-Obstetric and Pediatric Hospital (E.G.B.L.),
University of Douala, Faculty of Medicine and Pharmaceutical Science, Cameroon; Ain Shams University
Specialized Hospital (H.M.A., H.M.S., A.E., T.R.); Cairo University Affiliated MOH Network (F.H.);
Department of Neurology (TM.), Nasser Institute for Research and Treatment, Cairo; Mansoura University
Affiliated Private Hospitals Network (W.M.), Egypt; Kwame Nkrumah University of Science and Technology (F.S.S.), Kumasi, Ghana; Stroke Unit (T.O.A., K.W.), University of Ilorin Teaching Hospital;
Neurology Unit (B.A.), Department of Medicine, Lagos State University Teaching Hospital; Department of
Medicine (E.O.N.), Federal Medical Centre Owerri, Imo State, Nigeria; Neurology Unit (T.A.S.), Department of Medicine, Federal Medical Centre, Owo, Ondo State, Nigeria; University College Hospital
(J.Y.), Ibadan, Nigeria; The National Ribat University Affiliated Hospitals (H.H.M.), Khartoum, Sudan;
Neurology Section (P.B.A.), Department of Internal Medicine, Aga-Khan University, Medical College East
Africa, Dar es Salaam, Tanzania; Tunis El Manar University (A.D.R.), Military Hospital of Tunis; Department of Neurology (S.B.S.), Mongi Ben Hmida National Institute of Neurology, Faculty of Medicine of
Tunis, University Tunis El Manar, Tunisia; Department of Physiology (L.G.), Parirenyatwa Hospital, and
Departments of Physiology and Medicine (G.W.N.), University of Zimbabwe, Harare; Department of
Cerebrovascular/Endovascular Neurosurgery Division (D.S.), Erebouni Medical Center, Yerevan, Armenia;
Department of Neurology (A.R.), Sir Salimulah College, Dhaka, Bangladesh; Department of Neurology
(Z.A.), Taihe Hospital of Shiyan City, Hubei; Department of Neurology (F.B.), Nanyang Central Hospital,
Henan; Department of Neurology (Z.D.), Wuhan No. 1 Hospital, Hubei, China; Department of Neurology
(Y. Hao.), Sir Run Run Shaw Hospital, Zhejiang University School of Medicine; Department of Neurology
(W.H.), Traditional Chinese Medicine Hospital of Maoming, Guangdong; Department of Neurology
(G.Li.), Affiliated Hospital of Qingdao University, Shandong; Department of Neurology (W.L), The First
Affiliated Hospital of Hainan Medical College; Department of Neurology (G.Liu.), Wuhan Central Hospital,
Hubei; Department of Neurology (J.L.), Mianyang 404th Hospital, Sichuan; Department of Neurology
(X.S.), Yijishan Hospital of Wannan Medical College, Anhui; Department of Neurology and Neuroscience
(Y.S.), Shenyang Brain Institute, Shenyang First People’s Hospital, Shenyang Medical College Affiliated
Brain Hospital; Department of Neurology (L.T.), Affiliated Yantai Yuhuangding Hospital of Qingdao
University, Shandong; Department of Neurology (H.W.), Xiangyang Central Hospital, Hubei; Department
of Neurology (B.W., Y.Yan), West China Hospital, Sichuan University, Chengdu; Department of Neurology
(Z.Y.), Affiliated Hospital of Southwest Medical University, Sichuan; Department of Neurology (H.Z.),
Affiliated Hangzhou First People’s Hospital, Zhejiang University School of Medicine; Department of
Neurology (J.Z.), The First Affiliated Hospital of Shandong First Medical University; Department of
Neurology (W.Z.), First Affiliated Hospital of Fujian Medical University, China; Acute Stroke Unit
(T.W.L.), The Prince of Wales Hospital, Kwok Tak Seng Centre for Stroke Research and Intervention, The
Chinese University of Hong Kong; Interventional Neurology (C.C.), MAX Superspecialty Hospital, Saket,
New Delhi; NH Institute of Neurosciences (V.H.), NH Mazumdar Shaw Medical Center, Bangalore;
Department of Neurology (B.M.), Apollo Speciality Hospitals Nellore; Department of Neurology (J.D.P.),
Christian Medical College, Ludhiana, Punjab; Sree Chitra Tirunal Institute for Medical Sciences and
Technology (P.N.S.), Kerala, India; Stroke Unit (F.S.U.), Pelni Hospital, Jakarta, Indonesia; Neurosciences
Research Center (M. Farhoudi, E.S.H.), Tabriz University of Medical Sciences, Tabriz, Iran; Beer Sheva
Hospital (A.H.); Department of Interventional Neuroradiology, Rambam Healthcare Campus, Haifa, Israel
(A.R., R.S.H.); Departments of Neurology (N.O.) and Neurosurgery (N.S.), Kobe City Medical Center
General Hospital, Kobe; Department of Stroke and Neurovascular Surgery (D.W.), IMS Tokyo-Katsushika
General Hospital; Yokohama Brain and Spine Center (R.Y.); Iwate Prefectural Central (R.D.); Department
of Neurology and Stroke Treatment (N.T.), Japanese Red Cross Kyoto Daiichi Hospital; Department of
Neurology (T.Y.), Kyoto Second Red Cross Hospital; Department of Neurology (T.T.), Japanese Red Cross
Kumamoto Hospital; Department of Stroke Neurology (Y. Yazawa), Kohnan Hospital, Sendai; Department
of Cerebrovascular Medicine (T.U.), Saga-Ken Medical Centre; Department of Neurology (T.D.), Saitama
Medical Center, Kawagoe; Department of Neurology (H.S.), Nara City Hospital; Department of Neurology
(Y.S.), Toyonaka Municipal Hospital, Osaka; Department of Neurology (F. Miyashita), Kagoshima City
Hospital; Department of Neurology (H.F.), Japanese Red Cross Matsue Hospital, Shimane; Department of
Neurology (K.M.), Shiroyama Hospital, Osaka; Department of Cerebrovascular Medicine (J.E.S.), Niigata
City General Hospital; Department of Neurology (Y.S.), Sugimura Hospital, Kumamoto; Stroke Medicine
(Y. Yagita), Kawasaki Medical School, Okayama; Department of Neurology (Y.T.), Osaka Red Cross
Hospital; Department of Stroke Prevention and Treatment (Y.M.), Department of Neurosurgery, University
of Tsukuba, Ibaraki; Department of Neurology (S.Y.), Stroke Center and Neuroendovascular Therapy,
Saiseikai Central Hospital, Tokyo; Department of Neurology (R.K.), Kin-ikyo Chuo Hospital, Hokkaido;
Department of Cerebrovascular Medicine (T.K.), NTT Medical Center Tokyo; Department of Neurology
and Neuroendovascular Treatment (H. Yamazaki), Yokohama Shintoshi Neurosurgical Hospital; Department of Neurology (M.S.), Osaka General Medical Center; Department of Neurology (K.T.), Osaka
University Hospital; Department of Advanced Brain Research (N.Y.), Tokushima University Hospital
Tokushima; Department of Neurology (K.S.), Saiseikai Fukuoka General Hospital, Fukuoka; Department of
Neurology (T.Y.), Tane General Hospital, Osaka; Division of Stroke (H.H.), Department of Internal
Medicine, Osaka Rosai Hospital; Department of Comprehensive Stroke (I.N.), Fujita Health University
School of Medicine, Toyoake, Japan; Department of Neurology (A.K.), Asfendiyarov Kazakh National
Medical University; Republican Center for eHealth (K.F.), Ministry of Health of the Republic of Kazakhstan;
Department of Medicine (S.K.), Al-Farabi Kazakh National University; Kazakh-Russian Medical University
(M.Z.), Kazakhstan; Department of Neurology (J.-H.B.), Kangbuk Samsung Hospital, Sungkyunkwan
University School of Medicine, Seoul; Department of Neurology (Y. Hwang), Kyungpook National University Hospital, School of Medicine, Kyungpook National University; Ajou University Hospital (J.S.L.);
Department of Neurology (S.B.L.), Uijeongbu St. Mary’s Hospital, College of Medicine, The Catholic
University of Korea; Department of Neurology (J.M.), National Medical Center, Seoul; Department of
Neurology (H.P., S.I.S.), Keimyung University School of Medicine, Dongsan Medical Center, Daegu;
Department of Neurology (J.H.S.), Busan Paik Hospital, School of Medicine, Inje University, Busan;
Department of Neurology (K.-D.S.), National Health Insurance Service Ilsan Hospital, Goyang; Asan
Medical Center (C.J.Y.), Seoul, South Korea; Department of Neurology (R.A.), LAU Medical Center-Rizk
Hospital, Beirut, Lebanon; Department of Medicine (W.A.W.Z., N.W.Y.), Pusat Perubatan Universiti
Kebangsaan Malaysia, Kuala Lumpur; Sultanah Nur Zahirah (Z.A.A., K.A.I.), Kuala Terengganu; University
Putra Malaysia (H.b.B.); Sarawak General Hospital, Kuching (L.W.C.); Hospital Sultan Abdul Halim
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Neurology | Volume 96, Number 23 | June 8, 2021
(A.B.I.), Sungai Petani Kedah; Hospital Seberang Jaya (I.L.), Pulau Pinang; Thomson Hospital Kota
Damansara (W.Y.T.), Malaysia; “Nicolae Testemitanu” State University of Medicine and Pharmacy (S.G.,
P.L.), and Department of Neurology, Emergency Medicine Institute, Chisinau, Republic of Moldova;
Department of Stroke Unit (A.M.A.H.), Royal Hospital Muscat, Oman; Neuroscience Institute (Y.Z.I.,
N.A.), Hamad Medical Corporation, Doha, Qatar; St. Luke’s Medical Center–Institute of Neurosciences
(M.C.P.-F., C.O.C.), Quezon City, Philippines; Endovascular Neurosurgery (D.K.), Saint-Petersburg
Dzhanelidze Research Institute of Emergency Medicine, St. Petersburg, Russia; Department of Neurology
(A.A.), Stroke Unit, King Saud University, College of Medicine, Riyadh; Department of Neurosurgery
(H.A.-J.), Interventional Radiology, and Critical Care Medicine, King Fahad Hospital of the University,
Imam Abdulrahman bin Faisal University, Saudi Arabia; Singapore National Neuroscience Institute
(C.H.T.); Changi General Hospital (M.J.M.), Singapore; Neuroscience Center, Raffles Hospital (N.V.),
Singapore; Department of Neurology (C.-H.C., S.-C.T.), National Taiwan University Hospital; Department
of Radiology (A.C.), Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, Thailand; Dicle
University Medical School and Hospital (E.A.), Diyarbakir; Stroke and Neurointervention Unit (O.A.,
A.O.O.), Eskisehir Osmangazi University; Gaziantep University Faculty of Medicine (S.G.), Turkey; Department of Neurology (S.I.H., S.J.), Neurological Institute at Cleveland Clinic Abu Dhabi, United Arab
Emirates; Stroke Center (H.L.V., A.D.C.), Hue Central Hospital, Hue, Vietnam; Stroke Department
(H.H.N., T.N.P.), Da Nang Hospital, Da Nang City; 115 People’s Hospital (T.H.N., T.Q.N.), Ho Chi Minh
City, Vietnam; Department of Neurology (T.G., C.E.), Medical University of Graz; Department of Neurology (M. K.-O.), Research Institute of Neurointervention, University Hospital Salzburg/Paracelsus
Medical University, Austria; Department of Neurology (F.B., A.D.), Centre Hospitalier Universitaire de
Charleroi, Belgium; Department of Neurology (S.D.B., G.V.), Sint Jan Hospital, Bruges; Department of
Neurology (S.D.R.), Brussels University Hospital (UZ Brussel); Department of Neurology (N.L.), ULB
Erasme Hospitals Brussels; Department of Neurology (M.P.R.), Europe Hospitals Brussels; Department of
Neurology (L.Y.), Antwerp University Hospital, Belgium; Neurology Clinic (F.A., T.S.), St. Anna University
Hospital, Sofia, Bulgaria; Department of Neurology (M.R.B.), Sestre Milosrdnice University Hospital,
Zagreb; Department of Neurology (H.B.), Sveti Duh University Hospital, Zagreb; Department of Neurology
(I.C.), General Hospital Virovitica; Department of Neurology (Z.H.), General Hospital Zabok; Department
of Radiology (F. Pfeifer), University Hospital Centre Zagreb, Croatia; Regional Hospital Karlovy Vary
(I.K.); Masaryk Hospital Usti nad Labem (D.C.); Military University Hospital Praha (M. Sramek); Oblastnı́
Nemocnice Náchod (M. Skoda); Regional Hospital Pribram (H.H.); Municipal Hospital Ostrava (L.K.);
Hospital Mlada Boleslav (M. Koutny); Hospital Vitkovice (D.V.); Hospital Jihlava (O.S.); General University Hospital Praha (J.F.); Hospital Litomysl (K.H.); Hospital České Budejovice (M.N.); Hospital Pisek
(R.R.); Hospital Uherske Hradiste (P.P.); Hospital Prostejov (G.K.); Regional Hospital Chomutov (J.N.);
Hospital Teplice (M.V.); Mining Hospital Karvina (H.B.); Thomayer Hospital Praha (D.H.); Hospital
Blansko (D.T.); University Hospital Brno (R.J.); Regional Hospital Liberec (L.J.); Hospital Ceska Lipa
(J.N.); Hospital Sokolov (A.N.); Regional Hospital Kolin (Z.T.); Hospital Trutnov (P. Fibrich); Hospital
Trinec (H.S.); Department of Neurology (O.V.), University Hospital Ostrava, Faculty of Medicine, Masaryk
University, Brno, Czech Republic; Bispebjerg Hospital (H.K.C.), University of Copenhagen; Stroke Center
(H.K.I., T.C.T.), Rigshospitalet, University of Copenhagen; Aarhus University Hospital (C.Z.S.), Aarhus;
Neurovascular Center, Zealand University Hospital, University of Copenhagen (T.W.), Roskilde, Denmark;
Department of Neurology and Neurosurgery (R.V.), University of Tartu, Estonia; Neurology Clinic (K.G.P.), West Tallinn Central Hospital; Center of Neurology (T.T.), East Tallinn Central Hospital, School of
Natural Sciences and Health, Tallinn University; Internal Medicine Clinic (K.A.), Pärnu Hospital, Estonia;
Université Lille, Inserm, CHU Lille, Lille Neuroscience & Cognition (C.C., F.C.); Centre Hospitalier
d’Arcachon (M.D.), Gujan-Mestras; Centre Hospitalier d’Agen (J.-M.F.); Neurologie Vasculaire (L.M.) and
Neuroradiologie (O.E.), Hospices Civils de Lyon, Hôpital Pierre Wertheimer, Bron; Centre Hospitalier et
Universitaire de Bordeaux (E.L., F.R.); Centre Hospitalier de Mont de Marsan (B.O.); Neurologie (R.P.),
Fondation Ophtalmologique Adolphe de Rothschild; Versailles Saint-Quentin-en-Yvelines University (F.
Pico); Neuroradiologie Interventionelle (M.P.), Fondation Ophtalmologique Adolphe de Rothschild;
Neuroradiologie Interventionelle (R.P.), Hôpitaux Universitaires de Strasbourg, France; K. Eristavi National
Center of Experimental and Clinical Surgery (T.G.), Tbilisi; Department of Neurosurgery (M. Khinikadze),
New Vision University Hospital, Tbilisi; Vivamedi Medical Center (M. Khinikadze), Tbilisi; Pineo Medical
Ecosystem (N.L.), Tbilisi; Ivane Javakhishvili Tbilisi State University (A.T.), Tbilisi, Georgia; Department of
Neurology (S.N., P.A.R.), University Hospital Heidelberg; Department of Neurology (M. Rosenkranz),
Albertinen Krankenhaus, Hamburg; Department of Neurology (H.S.), Elbe Klinken Stade, University
Medical Center Göttingen; Department of Neurology (T.S.), University Hospital Carl Gustav Carus,
Dresden; Kristina Szabo (K.S.), Department of Neurology, Medical Faculty Mannheim, University Heidelberg, Mannheim; Klinik und Poliklinik für Neurologie (G.T.), Kopf- und Neurozentrum, Universitätsklinikum Hamburg–Eppendorf, Germany; Department of Internal Medicine (D.S.), School of
Health Sciences, University of Thessaly, Larissa; Second Department of Neurology (O.K.), Stroke Unit,
Metropolitan Hospital, Piraeus, Greece; University of Szeged (P.K.), Szeged; University of Pecs (L.S., G.T.),
Hungary; Stroke Center (A.A.), IRCCS Istituto di Ricovero e Cura a Carattere Scientifico, Negrar, Verona;
Department of Neurology (F.B.), Ospedale San Paolo, Savona,; Institute of Neurology (P.C., G.F.), Fondazione Policlinico Universitario Agostino Gemelli, Rome; Interventional Neurovascular Unit (L.R.),
Careggi University Hospital, Florence; Stroke Unit (D.S.), Azienda Socio Sanitaria Territoriale (ASST) di
Lecco, Italy; Maastricht University Medical Center; Department of Neurology (M.U.), Radiology, University Medical Center Groningen; Department of Neurology (I.v.d.W.), Haaglanden Medical Center, the
Hague, the Netherlands; Department of Neurology (E.S.K.), Akershus University Hospital, Lørenskog,
General Practice, HELSAM, University of Oslo, Norway; Neurological Ward with Stroke Unit (W.B.),
Specialist Hospital in Konskie, Gimnazjalna, Poland and Collegium Medicum, Jan Kochanowski University,
Kielce, Poland; Neurological Ward with Stroke Unit (M.F.), District Hospital in Skarzysko-Kamienna;
Department of Neurology (E.H.L.), Szpitala im T. Marciniaka in Wroclaw; 2nd Department of Neurology
(M. Karlinski), Institute of Psychiatry and Neurology, Warsaw; Department of Neurology and Cerebrovascular Disorders (R.K., P.K.), Poznan University of Medical Sciences; 107th Military Hospital with
Polyclinic (M.R.), Walcz; Department of Neurology (R.K.), St. Queen Jadwiga, Clinical Regional Hospital
No. 2, Rzeszow; Department of Neurology (P.L.), Medical University of Lublin; 1st Department of Neurology (H.S.-J.), Institute of Psychiatry and Neurology, Warsaw; Department of Neurology and Stroke Unit
(P.S.), Holy Spirit Specialist Hospital in Sandomierz, Collegium Medicum Jan Kochanowski University in
Kielce; Copernicus PL (W.F.), Neurology and Stroke Department, Hospital M. Kopernik, Gdansk; Stroke
Unit (M.W.), Neurological Department, Stanislaw Staszic University of Applied Sciences, Pila, Poland;
Hospital São José (Patricia Ferreira), Centro Hospitalar Universitário de Lisboa Central, Lisbon; Stroke Unit
(Paulo Ferreira, V.T.C.), Hospital Pedro Hispano, Matosinhos; Stroke Unit, Internal Medicine Department
(L.F.), Neuroradiology Department, Centro Hospitalar Universitário de São João, Porto; Department of
Neurology (J.P.M.), Hospital de Egas Moniz, Centro Hospitalar Lisboa Ocidental, Lisbon, Portugal; Department of Neurosciences (T.P.e.M.), Hospital de Santa Maria-CHLN, North Lisbon University Hospital;
Hospital São José (A.P.N.), Centro Hospitalar Universitário de Lisboa Central, Lisbon; Department of
Neurology (M. Rodrigues), Hospital Garcia de Orta, Portugal; Department of Neurology (C.F.-P.),
Neurology.org/N
Copyright © 2021 American Academy of Neurology. Unauthorized reproduction of this article is prohibited.
Transilvania University, Brasov, Romania; Department of Neurology (G.K., M. Mako), Faculty Hospital
Trnava, Slovakia; Department of Neurology and Stroke Center (M.A.d.L., E.D.T.), Hospital Universitario La
Paz, Madrid; Department of Neurology (J.F.A.), Hospital Clı́nico Universitario, Universidad de Valladolid;
Department of Neurology (O.A.-M.), Complejo Hospitalario Universitario de Albacete; Department of
Neurology (A.C.C.), Unidad de Ictus, Hospital Universitario Ramon y Cajal, Madrid; Department of
Neurology (S.P.-S), Hospital Universitario Virgen Macarena & Neurovascular Research Laboratory (J.M.),
Instituto de Biomedicina de Sevilla-IbiS; Rio Hortega University Hospital (M.A.T.A.), University of Valladolid; Cerebrovascular Diseases (A.R.V.), Hospital Clinic of Barcelona, Spain; Department of Neurology
(M. Mazya), Karolinska University Hospital and Department of Clinical Neuroscience, Karolinska Institute,
Stockholm, Sweden; Department of Interventional Neuroradiology (G.B.), University Hospitals of Geneva;
Department of Interventional and Diagnostic Neuroradiology (A.B., M.-N.P.), Radiology and Nuclear
Medicine, University Hospital Basel; Department of Neurology (U.F.), University of Bern; Department of
Neuroradiology (J.G.), University of Bern; Department of Neuroscience (P.L.M., D.S.), Lausanne University Hospital, Switzerland; Department of Stroke Medicine (S.B., J. Kwan), Imperial College Healthcare
NHS Trust, Charing Cross Hospital, London; Department of Neurology (K.K.), Queen’s Medical Centre,
Nottingham University Hospitals NHS Trust, United Kingdom; Department of Neurology (A.B., A.
Shuaib), University of Alberta, Edmonton; Department of Neurology (L.C., A. Shoamanesh), McMaster
University, Hamilton; Department of Clinical Neurosciences and Hotchkiss Brain Institute (A.M.D.,
M.D.H.), University of Calgary; Department of Neurology (T.F., S.Y.), University of British Columbia,
Vancouver; Mackenzie Health (J.H., C.A.S.) Richmond Hill, Ontario; Department of Neurology (H.K.),
Sunnybrook Health Sciences Centre, University of Toronto; Department of Neurology (A. Mackey),
Hopital Enfant Jesus, Centre Hospitalier de l’Universite Laval, Quebec City; Department of Neurology
(A.P.), University of Toronto; Medicine (G.S.), St. Michael’s Hospital, University of Toronto, Canada;
Department of Neurosciences (M.A.B.), Hospital Dr. Rafael A. Calderon Guardia, CCSS. San Jose, Costa
Rica; Neurovascular Service (J.D.B.), Hospital General San Juan de Dios, Guatemala City; Department of
Neurologı́a (L.I.P.R.), Hospital General de Enfermedades, Instituto Guatemalteco de Seguridad Social,
Guatemala City, Guatemala; Department of Neurology (F.G.-R.), University Hospital Jose Eleuterio
Gonzalez, Universidad Autonoma de Nuevo Leon, Mexico; Pacı́fica Salud–Hospital Punta Pacı́fica (N.N.-E.,
A.B., R.K.), Panama; Department of Neurology, Radiology (M.A.), University of Kansas Medical Center;
Department of Neurointerventional Neurosurgery (D. Altschul), The Valley Baptist Hospital, Ridgewood,
New Jersey; Palmetto General Hospital (A.J.A.-O.), Tenet, Florida; Neurology (I.B., P.K.), University
Hospital Newark, New Jersey Medical School, Rutgers, Newark, New Jersey; Community Healthcare
System (A.B.), Munster, Indiana; Department of Neurology (N.B., C.B.N.), California Pacific Medical
Center, San Francisco; Department of Neurology (C.B.), Mount Sinai South Nassau, New York; University
of Toledo (A.C.), Ohio; Department of Neurology (S.C.), University of Maryland School of Medicine,
Baltimore, Maryland; Neuroscience (S.A.C.), Inova Fairfax Hospital, Virginia; Department of Neurology
(H.C.), Abington Jefferson Hospital, Pennsylvania; Department of Neurology (J.H.C.), Mount Sinai South
Nassau, New York; Baptist Health Medical Center (S.D.), Little Rock, Arkansas; Department of Neurology
(K.D.), HCA Houston Healthcare Clearlake, Texas; Department of Neurology (T.G.D., R.S.), Erlanger,
Tennessee; Wilmington North Carolina (V.T.D.); Department of Vascular and Neurointerventional Services (R.E.), St. Louis University, Missouri; Department of Neurology (M.E.), Massachusetts General
Hospital, Boston; Department of Neurology, Neurosurgery, and Radiology (M.F., S.O.-G., N.R.), University
of Iowa Hospitals and Clinics, Iowa City; Department of Radiology (D.F.), Swedish Medical Center,
Englewood, Colorado; Department of Radiology (D.G.), Neurosurgery, University of Maryland School of
Medicine, Baltimore, Maryland; Adventist Health Glendale Comprehensive Stroke Center (M.G.), Los
Angeles, California; Wellstar Neuroscience Institute (R.G.), Marietta, Georgia; Department of Neurology
(A.E.H.), University of Texas Rio Grande Valley-Valley Baptist Medical Center, Texas; Department of
Neurology (J.H., B.V.), Lahey Hospital & Medical Center, Beth Israel Lahey Health, Burlington, Massachusetts; Department of Neurology (A.M.K.), Wayne State, Detroit, Michigan; HSHS St. John’s Hospital
(N.N.K.), Southern Illinois University School of Medicine, Springfield; Virginia Hospital Center (B.S.K.),
Arlington; Department of Neurology, University of Michigan, Ann Arbor; Weill-Cornell Medical College
(D.O.K.), New York-Presbyterian Queens; Department of Neurology (V.H.L.), Ohio State University,
Columbus; Department of Neurology (L.Y.L.), Tufts Medical Center, Boston, Massachusetts; Vascular and
Neurointerventional Services (G.L.), St. Louis University, Missouri; Miami Cardiac & Vascular Institute
(I.L., A.K.S.), Florida; Department of Neurology (H.L.L.), Oregon Health & Science University, Portland;
Department of Emergency Medicine (L.M., M.S.), Steward Holy Family Hospital, Methuen, MA; Vidant
Medical Center (S.M.), Greenville, North Carolina; Department of Neurology (A.M.M., D.R.Y.) and
Neurosurgery (D.R.Y.), University of Miami Miller School of Medicine, Florida; Department of Neurology
(H.M.), SUNY Upstate New York, Syracuse; Memorial Neuroscience Institute (B.P.M.), Pembroke Pines,
Florida; Neurosciences (J.M., J.P.T.), Spectrum Health, Michigan State University College of Medicine,
Grand Rapids, Michigan; Sutter Health (M.M.), Sacramento, California; Department of Neurology
(J.G.M.), Maine Medical Center, Portland; Department of Neurology (S.S.M.), Bayhealth, Dover, Delaware;
Department of Neurology and Pediatrics (F.N.), Emory University, Atlanta, Georgia; Department of
Neurology (K.N.), University of Arkansas for Medical Sciences, Little Rock; Department of Radiology and
Neurology (R.N.-W.), UT Southwestern Medical Center, Dallas, Texas; Ascension St. John Medical Center
(R.H.R.), Tulsa, Oklahoma; Riverside Regional Medical Center (P.R.), Newport, Virginia; Department of
Neurology (J.R.R., T.N.N.), Boston University School of Medicine, MA; Department of Neurology (A.R.),
Hospital of the University of Pennsylvania, Philadelphia; Department of Neurology (M.S.), University of
Washington School Medicine, Seattle; Department of Neurology (B.S.), University of Massachusetts
Medical Center, Worcester; Department of Neurology (A.S.), CHI-Immanuel Neurological Institute,
Creighton University, Omaha, Nebraska; Holy Cross Hospital (S.L.S.), Fort Lauderdale, Florida; Department of Neurology (V.S.), Interventional Neuroradiology, University of California in Los Angeles;
Banner Desert Medical Center (M.T.), Mesa, Arizona; Hospital de Agudos Dr. Ignacio Privano (O.B., A.L.),
Argentina; Institute for Neurological Research, FLENI (V.A.P.L.), Buenos Aires, Argentina; Hospital das
Clinicas/São Paulo University (M.S.A., A.C.); Sumare State Hospital (F.B.C., L.V.), São Paulo; Hospital
Vera Cruz (L.D.D.S.), Deus Campinas; Irmanandade Santa Casa de Porto Alegre (L.V.G.); Stroke Unit
(F.O.L., F. Mont’alverne), Hospital Geral de Fortaleza; Stroke Unit (A.L.L., P.S.C.M.), Hospital Sao Jose,
Joinville, Santa Catarina; Stroke Unit (R.T.M.), Neurology, Nossa Senhora da Conceição Hospital, Porto
Alegre; Department of Neurology (D.L.M.C.), Hospital Moinhos de Vento, Porto Alegre; Department of
Neurology (L.C.R.), Hospital de Base do Distrito Federal; Hospital Ana (V.F.C.), Hospital Juliane, Federal
University of Parana, Curitiba, Brazil; Vascular Neurology Unit (P.M.L., V.V.O.), Neurology Service, Department of Neurology and Psychiatry, Clı́nica Alemana, Universidad del Desarrollo, Santiago; Hospital
Padre Hurtado (V.N., J.M.A.T.) Santiago, Chile; Fundación Valle del Lili (P.F.R.A.), Cali; Stroke Center
(H.B.), Fundación Santa Fe de Bogotá; Department of Neurology (A.B.C.-Q.), Hospital Departamental
Universitario del Quindio San Juan de Dios, Armenia; Clinica Universitaria Colombia (C.E.R.O.), Bogotá;
University Hospital of San Vicente Foundation (D.K.M.B.), Medellin; Barranquilla, Colombia (O.L.);
Hospital Infantil Universitario de San Jose (M.R.P.), Bogota; Stroke Unit (L.F.D.-E.), Hospital de Clı́nicas,
Facultad de Ciencias Médicas, Universidad Nacional de Asunción; Neurology Service (D.E.D.M.F., A.C.V.),
Neurology.org/N
Hospital Central del Instituto de Prevision Social, Paraguay; Internal Medicine Service (A.J.Z.Z.), Hospital
Central de Policia “Rigoberto Caballero”, Paraguay; National Institute of Neurological Sciences of Lima Peru
(D.M.B.I.); Hospital Edgardo Rebagliati Martins Lima-Peru (L.R.K.); Department of Neurology (B.C.),
Royal Melbourne Hospital; Department of Neurology (G.J.H.), Sir Charles Gairdner Hospital and Medical
School, Faculty of Health and Medical Sciences, The University of Western Australia, Perth; University of
Melbourne (C.H., R.S.), Ballarat Health Service, Australia University of Melbourne; Department of Neurology
(T.K.), Royal Adelaide Hospital; Department of Neurosurgery (A. Ma), Royal North Shore Hospital, Sydney;
Department of Neurology (R.T.M.), Mater Hospital, Brisbane; Department of Neurology (R.S.), Austin Health,
Victoria; Florey Institute of Neuroscience and Mental Health (R.S.), Parkville, Melbourne, Australia; Greymouth
Base Hospital (D.S.), New Zealand; Department of Neurology (T.Y.-H.W.), Christchurch Hospital, New
Zealand; Department of Neurology (D.L.), University of California in Los Angeles; and Department of Neurology (O.O.Z.), Mercy Health Neurosciences, Toledo, Ohio.
Study Funding
The authors report no targeted funding.
Disclosure
Dr. Nogueira reports consulting fees for advisory roles with
Anaconda, Biogen, Cerenovus, Genentech, Imperative Care,
Medtronic, Phenox, Prolong Pharmaceuticals, Stryker Neurovascular and stock options for advisory roles with Astrocyte,
Brainomix, Cerebrotech, Ceretrieve, Corindus Vascular Robotics, Vesalio, Viz-AI, and Perfuze. Dr. Martins reports receiving lecture fees from Bayer, Medtronic, Penumbra and
speaker / advisory board fees from Boehringer Ingelheim. Dr.
Czlonkowska reports service as Expert Witness. Dr. Siegler
served as a consultant for Ceribell and the institution of Dr.
Siegler has received research support from the National Institutes of Health. The institution of Dr. Czap has received
research support from the National Institutes of Health. Dr.
Holmstedt served as a consultant for Astrazeneca and the
institution of Dr. Holmstedt has received research support
from the National Institutes of Health, the Patient-Centered
Outcomes Research Institute, and CSPC Pharmaceuticals.
Dr. Holmstedt served as a Study Adjudicator with Ischemia
Care. Dr. Turan served on a scientific advisory or DSMB for
Pfizer/Merck and Gore Inc. and has received publishing
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institution of Dr. Alexandrov has received research support
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Raz served as an expert witness for law firms and has received
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support from Nico Corporation, Inc. Dr. Rahman served as a
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has served as a lecture honoralium with Asahi Intec. Dr. Yagita
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served as an expert witness for Daiichi-Sankyo and the institution of Dr. Ayo Martin has received research support
from Daiichi-Sankyo and the Spanish Society of Neurosonology. The institution of Dr. Montaner has received research support from the Spanish government and has received
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Appendix 2
(continued)
Name
Location
Role
Contribution
Thomas
Kraemer,
MD
University of
Melbourne, Ballarat
Health Service,
Australia
Collaborator
Contribution
of data
References
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
Publication History
Received by Neurology October 30, 2020. Accepted in final form
March 11, 2021.
11.
12.
13.
Appendix 1 Authors
14.
Authors, their locations, and their contributions are listed at links.lww.com/
WNL/B357
15.
16.
17.
18.
Appendix 2 Coinvestigators
Name
Location
Role
Contribution
19.
Judith Clark,
RN
Boston Medical Center
Collaborator
Contribution
of data
20.
Cheryl
Grant, RN
Neurology, Medical
University of South
Carolina, Charleston
Collaborator
Contribution
of data
Mazlina
Husin,
MMed
Hospital Sultanah Nur
Zahirah Kuala
Terengganu, Malaysia
Collaborator
Crivorucica
Igor, MD
Emergency Medicine
Institute, Chisinau,
Republic of Moldova
Collaborator
Steve
Withington,
MD, FRACP
Ashburton Hospital,
Ashburton, New
Zealand
Collaborator
Mandy Lau,
MD
University of
Melbourne, Ballarat
Health Service,
Australia
Collaborator
21.
22.
23.
e2838
Contribution
of data
24.
Contribution
of data
25.
Contribution
of data
26.
Contribution
of data
Neurology | Volume 96, Number 23 | June 8, 2021
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Global Impact of COVID-19 on Stroke Care and IV Thrombolysis
Raul G. Nogueira, Muhammad M. Qureshi, Mohamad Abdalkader, et al.
Neurology 2021;96;e2824-e2838 Published Online before print March 25, 2021
DOI 10.1212/WNL.0000000000011885
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