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ORIGINAL CONTRIBUTIONS
BACKGROUND AND PURPOSE: Patient care-seeking has likely changed during the coronavirus disease 2019 (COVID-19)
pandemic. In stroke, delayed or avoided care may translate to substantial morbidity. We sought to determine the effect of the
pandemic on patterns of stroke patient presentation and quality of care.
METHODS: We analyzed data from 25 New England hospitals: one urban, academic comprehensive stroke center and telestroke
hub, and 24 spoke hospitals in the telestroke network. We included all telestroke consultations from the 24 spokes, and all
stroke admissions to the comprehensive stroke center hub from November 1, 2019 through April 30, 2020. We compared
rates of presentation, timeliness presentation, and quality of care pre- versus post-March 1, 2020. We examined trends in
patient demographics, stroke severity, timeliness, diagnoses including large vessel occlusion, alteplase use, and endovascular
thrombectomy among eligible subjects. We compared proportions and bivariate comparisons to examine for changes pre-
versus post-March 1, 2020 and used linear regression to examine trends over time.
RESULTS: Among 1248 patient presentations (844 telestroke consultations, 404 comprehensive stroke center admissions),
telestroke consultations and ischemic stroke patient admissions decreased among the spokes and hub. Age and stroke
severity were unchanged over the study period. We found no change in alteplase administration at telestroke spoke hospitals
but did note a decrease in both alteplase use and thrombectomy at our comprehensive stroke center. Time metrics for patient
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presentation and care delivery were unchanged; however, rates of adherence for the quality measures dysphagia screening,
early antithrombotic initiation, and early venous thromboembolism prophylaxis were reduced during the pandemic.
CONCLUSIONS: In this regional analysis, we found decreasing telestroke consultations and ischemic stroke admissions, and
reduced performance on stroke quality of care measures during the COVID-19 pandemic. Contrary to prior reports, we
did not find an increase in thrombectomy nor decrease in clinical severity that might be expected if patients with milder
symptoms avoided hospitalization.
T
he management of patients with acute ischemic potential ramifications of this pandemic on acute stroke
stroke is predicated on the timely delivery of acute care.2 Many physicians and health care leaders have
stroke care.1 With the current outbreak of corona- expressed concern about the potential consequences
virus disease 2019 (COVID-19) and its impact on the of delayed care for time-critical diagnoses like stroke
medical system, there is significant concern about the and acute myocardial infarction.2–4 Understanding the
Correspondence to: Kori S. Zachrison, MD, MSc, Department of Emergency Medicine, Massachusetts General Hospital, 55 Fruit St, Boston, MA 02114. Email
kzachrison@partners.org
*Drs Etherton and Zachrison were co-first authors.
This manuscript was sent to Marc Fisher, Senior Consulting Editor, for review by expert referees, editorial decision, and final disposition.
The Data Supplement is available with this article at https://www.ahajournals.org/doi/suppl/10.1161/STROKEAHA.120.031300.
For Sources of Funding and Disclosures, see page XXX.
© 2021 American Heart Association, Inc.
Stroke is available at www.ahajournals.org/journal/str
Nonstandard Abbreviations and Acronyms stroke presentation, systems, and quality of care, we
used data from our academic hub-and-spoke telestroke
COVID-19 coronavirus disease 2019 network to examine patterns of telestroke consultations
CSC comprehensive stroke center and stroke patient presentations from 25 urban and rural
ED emergency department hospitals across New England during the course of the
EVT endovascular thrombectomy pandemic. We hypothesized that the volume of patients
LKW last known well presenting during the pandemic would be decreased,
LVO large vessel occlusion
that there would be delays in patient presentation, and
that median stroke severity might increase if patients
NIHSS National Institutes of Health Stroke
Scale
with more severe stroke symptoms would still present
early but those with minor symptoms would delay or avoid
TIA transient ischemic attack
seeking care. We also hypothesized that door to throm-
bolysis and thrombectomy might increase due to more
onerous infection control protocols, delayed activation
influence of the COVID-19 pandemic on stroke patient of the stroke team, and increased burden of high-acuity
presentation, and systems and quality of care, holds patients in EDs during the surge. Finally, we assessed
potential to improve stroke care moving forward. the impact of COVID-19-related process changes on
Recent reports from areas afflicted by COVID-19 acute and inpatient quality of stroke care.
at earlier stages of the pandemic have suggested a
potential impact on both the volume and timeliness of
stroke/transient ischemic attack (TIA) hospital pre- METHODS
sentation.5–7 In China, at the early epicenter of the
COVID-19 pandemic, an analysis of survey results Setting and Population
from >200 national stroke centers observed a 25% The Partners TeleNeurology Network consists of 2 academic
decrease in rates of thrombolysis and thrombectomy hub hospitals and 24 urban, suburban, and rural spoke hos-
cases at designated COVID-19 hospitals.5 However, pitals across 3 New England states that function at a level
equivalent to acute stroke ready or primary stroke center hos-
the generalizability of these results internationally is
pitals. Spoke hospitals are encouraged to call telestroke con-
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limited as this was a survey-based investigation of a sultations for all potential alteplase or thrombectomy cases, or
single country where >70% of hospitals reported at for complex stroke cases requiring CSC intervention. Details of
least a partial reduction in emergency stroke capac- the network have been previously described.10 Consultations
ity. Another small, single-site investigation of patients include phone and video; time metrics and National Institutes
presenting to a stroke center in Hong Kong during of Health Stroke Scale (NIHSS) are recorded for video consul-
COVID-19 showed an approximate 1-hour delay in tations. Performance of NIHSS by neurologists via telestroke
time from stroke onset to emergency department (ED) has been shown to have high-fidelity with in-person exam.11 All
arrival as well as a reduction in admissions for TIA.6 consultations are documented in a secure online TeleHealth
These findings are also provocative, however, as this Portal using structured data fields with embedded logic checks.
was a relatively small study of a single center, the The dataset includes all patients for whom a telestroke was
called whether from the ED or inpatient setting.
impact of the COVID-19 pandemic on other countries
In addition to the telestroke data from patients present-
like the United States is less clear. ing to the 24 spoke hospitals, we also analyzed data from the
Regarding the impact of the COVID-19 pandemic main telestroke hub, which supports these spokes. This urban,
on stroke case in the United States, a small study from academic CSC hub hospital uses the Get With the Guidelines-
a New Jersey comprehensive stroke center (CSC) Stroke registry as the CSC stroke database and all data were
reported a nearly 40% reduction in new stroke diagno- extracted from this source.12 Get With the Guidelines-Stroke
ses but no difference in stroke severity or times of stroke is a national stroke quality improvement registry developed by
onset to ED arrival, or door-to-needle.8 Importantly, this the American Heart Association and includes information on
was another relatively small and early investigation of the patients’ demographics, medical history, and hospital treatment
effect of COVID-19 in a single state at a single institu- characteristics and outcomes for all patients with a diagnosis
tion with no analysis of telestroke quality measures. A of stroke. This includes both ED and inpatient strokes. Hospital
personnel are trained in data abstraction and collect data on
small case series of 5 COVID-19 patients in New York
consecutively admitted patients with stroke.
also suggested increased prevalence of stroke in the We used data from the telestroke portal and CSC hospital
young secondary to large-vessel occlusion.9 These find- registry from November 1, 2019 through April 30, 2020. In
ings suggest that the COVID-19 outbreak may have Massachusetts, March 1 immediately preceded the first reported
impacted stroke patient presentation and systems of cases of community transmission,13 and the peak of reported
care in the United States but warrant further investiga- cases occurred on April 29.14 Thus, our analysis included 4
tion in a larger stroke network. months of prepandemic and 2 months of intrapandemic data.
The study was approved by the local IRB, and requirement for of TIA cases that are not admitted (ie, observation stays or
Original Contributions
informed consent was waived. A fully deidentified version of the ED discharges).
data that support the findings of this study are available from Analyses were performed separately for telestroke con-
the corresponding author upon reasonable request. sultations and for CSC stroke patient admissions with the
observations grouped by week. Comparison of the clinical
and quality outcomes of interest preversus post-March 1 were
Clinical Variables performed using χ2 test, Mann-Whitney U test, and Poisson
Details of patient age, sex, and stroke severity (NIHSS) were regression as appropriate. Given the small sample size for χ2
extracted from the TeleHealth Portal. We also collected the testing, we also performed a Monte Carlo version as a robust-
details of the acute stroke presentation including last known ness check and report significance tests from this version. We
well (LKW), time of ED arrival, consult request, and alteplase used Poisson regression analyses to study stroke incidence
treatment. Treatment rates for intravenous alteplase and over time in all patients and stratified by diagnosis subtype
transfer for endovascular thrombectomy (EVT) consideration (acute ischemic stroke, transient ischemic attack [TIA], and
were recorded. Final diagnosis after telestroke consultation hemorrhagic stroke). We also examined trends over time in
was recorded by the neurologist performing the teleconsulta- (1) telestroke consultations transferred for thrombectomy, (2)
tion and included acute ischemic stroke (defined as <9 hours large vessel occlusion (LVO) strokes at our CSC, (3) stroke
from LKW), subacute ischemic stroke (>9 hours from LKW), severity by NIHSS score. and (4) age.
TIA, or “other”. Next, in response to reports of increased LVO stroke
Get With the Guidelines-Stroke is a national stroke qual- among the young related to COVID, we were interested in
ity improvement registry developed by the American Heart examining whether this phenomenon was occurring in our
Association and includes information on patients’ demograph- own region. We identified the subgroup of young patients
ics, medical history, and hospital treatment characteristics and with stroke (defined as <50 years of age) among telestroke
outcomes. Hospital personnel are trained in data abstrac- consultations transferred for thrombectomy and CSC stroke
tion and collect data on consecutively admitted patients with admissions with LVO stroke and used simple descriptive
stroke. Quality measures collected included rates of adherence statistics to examine the proportion of patients presenting
to evidence-based measures in the acute, subacute, and dis- before versus after March 1, 2020.
charge phases of care as follows: acute (door to computed This study was approved by the Partners Institutional
tomography <25 minutes, patients treated with alteplase that Review Board.
arrive within 2 hours and treated with 3 hours or 3.5 hours and
treated within 4.5 hours, door to alteplase within 60 minutes of
arrival, dysphagia screen before oral feeding); subacute (anti- RESULTS
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Table 1. Patient Characteristics respectively, P=0.04; Figure 2). While there was not a
Original Contributions
Original Contributions
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time metrics were stable with respect to time from for patients with stroke with atrial fibrillation or flutter, or
arrival to alteplase administration and to groin puncture evaluation for rehabilitation services. The rate of stroke
for thrombectomy (Table 2). education was also reduced (Table 3).
Evaluation of the measures of stroke quality care at the
CSC, however, demonstrated reduced rates of alteplase
administration for patients arriving within 3.5 hours of DISCUSSION
LKW and treated by 4.5 hours during COVID (Table 3). In this analysis of a large urban and rural telestroke
In addition, rates of compliance with acute interventions network and large, urban CSC in the Northeastern
beyond alteplase such as dysphagia screening, early United States during the COVID-19 pandemic, we
antithrombotic initiation, and early venous thromboembo- found decreasing rates of telestroke consultations and,
lism prophylaxis were reduced during COVID (Table 3). as others have reported, decreasing ischemic stroke
No difference was observed in rates of prescription of a patient admissions.5,6,8 We also observed no delays in
statin or antithrombotic on discharge or anticoagulation patient presentation or in timeliness of in-hospital stroke
evaluation and treatment. Last, we observed an impact pandemic in our region. While we have not experienced
of the COVID pandemic on several measures of stroke the COVID-19 pandemic to the extent of our colleagues
quality of care. in New York, at the time of this submission, the state of
While we may have lacked statistical power for a Massachusetts was third only to New York and New Jer-
definitive conclusion, we did not find any change in age sey for state COVID-19 cases per capita and remained
or in stroke severity among telestroke consultations nor as one of the states with the highest number of COVID-
among our institutional stroke patients over time. Our 19 cases per capita to date.14,15 Nevertheless, it remains
findings stand in contrast to a small case series from possible that the number of cases in our sample was too
Mt. Sinai Hospital in New York, in which Oxley et al9 low to have detected the association.
described an association between large-vessel stroke Our findings of decreasing proportion of telestroke
and COVID-19 in 5 young patients with stroke. We also consultations with TIA during the pandemic are worri-
failed to find any examples of large-vessel occlusion some from a public health perspective and warrant fur-
stroke in patients <50 years during the height of the ther investigation. Stroke after TIA is of high likelihood,
Table 2. Timeliness of Patient Presentation and Stroke Care Delivery Before and During COVID-19 at a
Original Contributions
Comprehensive Stroke Center and Its 24 Telestroke Network Spoke Hospitals
COVID-19 indicates coronavirus disease 2019; CSC, comprehensive stroke center; ED, emergency department; IQR, interquartile range
presented as 25th to 75th percentile; and LKW, last known well.
*Among telestroke consultations, median times from LKW and symptom discovery to ED presentation are primarily collected among patients
who may be potential candidates for alteplase or thrombectomy. Among patients with CSC, these fields are recorded for all stroke and TIA
admissions.
especially in the short-term period, which is why urgent observed reduced rates of private vehicle/walk-in as the
medical evaluation is recommended.1,16,17 The results arrival mode.8 Furthermore, the Chinese national survey
from our large, regional telestroke network are in agree- results observed high rates of response for delays in
ment with those reported from a single Hong Kong stroke care due to patients and families fear of present-
stroke center, which also observed overall delays in ing to the hospital during the pandemic.5 In contrast, a
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stroke care during COVID-19.6 These findings suggest study of ambulance calls for stroke and acute myocardial
that during the COVID-19 outbreak, patients with TIAs infarction in the United Kingdom observed no change
and minor strokes may have deferred seeking medical during COVID suggesting decreased likelihood of delay
attention in contrast to those patients with more severe for more severe strokes.18 Along these lines, the results
stroke syndromes. In support of this hypothesis, analysis of the French national registry analysis of patients with
of patient mode of presentation from a New Jersey CSC LVO who underwent EVT showed no difference in time
VTE prophylaxis by end of hospital day 2 99.6 (242) 70.9 (90) <0.001*
CSC indicates comprehensive stroke center; CT, computed tomography; DTN, door to needle; LKW, last known well; and VTE,
venous thromboembolism.
*P<0.05.
from symptom onset to imaging during the pandemic.7 influences on referral patterns and patient behaviors.
Original Contributions
Assimilating the results of these multinational studies However, we suspect these potential factors did not
supports the hypothesis that the COVID-19 pandemic contribute significantly as our telestroke volumes have
contributed to decreased rates of presentation for non- previously increased annually,10 and we did not observe
disabling strokes or TIAs. For these reasons, a continued a significant reduction in our CSC transfer volume. Addi-
emphasis on public health campaigns for stroke and TIA tionally, the observed trend before February did not sug-
awareness is necessary. gest a decrease; it is possible that there were changes
Reassuringly, this large-scale analysis of telestroke in patient and physician behavior that preceded March 1
consultations and CSC stroke admissions demonstrates (the date when Massachusetts had its first reported case
that stroke severity and the timeliness of delivery of of community transmission). In addition, our discussion of
stroke care were similar during COVID-19. In the afore- stroke care quality metrics was limited to a single CSC
mentioned French study of patients who underwent EVT, and may not be generalizable to other settings. Never-
the observed 21% reduction in EVT rates during the theless, as one of the first reports to include an evalua-
pandemic was probably influenced, at least in part, by the tion of changes in stroke care delivery at a large-volume
observed increase in time from imaging to groin punc- CSC during the pandemic, we think these data serve
ture during the pandemic, especially in those individuals as a useful starting point for recognizing the impact of
requiring transfer (mean difference +29 minutes).7 In the this pandemic on stroke care quality measures. Finally,
United States, a small study from a New Jersey CSC also we may not have had adequate power to identify signifi-
reported no difference in stroke severity or times of LKW cant changes in trends over time; however, this analysis
to ED arrival, or door-to-needle.8 We did observe, how- of 1248 patients from 25 hospitals is one of the larger
ever, that several measures of stroke quality of care were regional analyses of this topic to date and adds substan-
affected during the COVID pandemic with reduced rates tial information to our current understanding of trends in
of dysphagia screening, early antithrombotic initiation stroke care in relation to the pandemic.
and venous thromboembolism prophylaxis, and stroke
education. Our institutional response to the COVID-19
pandemic was to convert our designated stroke unit to CONCLUSIONS
an intensive care unit for patients with COVID, resulting
in patients with stroke being distributed throughout the In this analysis of stroke patient presentations to 25
hospital. As a result, these observations likely reflect this New England hospitals, we found decreasing frequency
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restructuring of stroke patient flow to hospital units not of patient presentation in relation to the pandemic.
previously designated as stroke units and underscore the We did not replicate the previously reported findings
importance of stroke unit care for patients with stroke. of increased presentation of young patients with LVO
These findings suggest that the United States made stroke nor did we identify increased stroke severity or
great strides to adequately prepare its stroke systems of delays in presentation that would be expected if patients
care for the impending COVID-19 outbreak, but contin- with mild strokes avoided or delayed presenting acutely
ued efforts on delivery of high-quality care are necessary. to the hospital. We also found that timeliness of stroke
Our findings are limited as this was a retrospective care delivery was stable but that several measures of
analysis of 25 hospitals in the Northeast United States stroke quality of care were reduced during the pandemic.
that have worked closely together in a telestroke net- These findings suggest that the reorganization efforts of
work relationship for many years and may not be gen- stroke systems of care in preparation for the COVID-19
eralizable to other settings. We do not have additional surge were successful in mitigating the potential impact
details on patient demographics, radiographic features, on delays in acute stroke treatment but that continued
stroke subtypes, and total ischemic stroke admission emphasis on optimizing stroke quality care is essential.
volumes for our telestroke spoke hospitals, nor do we For the purposes of population awareness and recogni-
know basic information about patients presenting to the tion of stroke and TIA symptoms, a continued national
spoke hospitals for which telestroke consultations were emphasis will be important for stroke prevention and
not requested. These gaps preclude a population level public health.
estimate of stroke admissions or changes in presenta-
tion. However, it is our experience that spoke hospitals
routinely use the platform for the vast majority of acutely ARTICLE INFORMATION
presenting patients with suspected stroke. In addition, we Received June 11, 2020; final revision received November 4, 2020; accepted
November 24, 2020.
do not have reason to think that this would have changed
in response to the pandemic, as most of our spokes have Affiliations
no alternative stroke consultants. Similarly, the nature Department of Neurology (M.R.E., Z.Y., L.S., M.B., J.E., A.V., A.B.S., L.H.S.) and De-
partment of Emergency Medicine (K.S.Z.), Massachusetts General Hospital, Bos-
of these data also do not enable us to definitively dis- ton. Inserm U1171, Degenerative and Vascular Cognitive Disorders, University of
tinguish between secular trends and pandemic-related Lille, France (M.B.).
Acknowledgments the American College of Cardiology (ACC), and the American College of
Original Contributions
We thank Ms Joyce McIntyre and Ms Kiera Macdonald for their assistance Emergency Physicians (ACEP). J Am Coll Cardiol. 2020;96:336–345. doi:
in providing data from our Get With the Guidelines-Stroke database and 10.1002/ccd.28946
Telestroke portals. 4. Hsieh P. Do not delay urgent medical care due to the COVID-19 coro-
navirus pandemic. Forbes. 2020. https://www.forbes.com/sites/
Sources of Funding paulhsieh/2020/04/20/do-not-delay-urgent-medical-care-due-to-the-covid-
19-coronavirus-pandemic/#2e9c34a763ea.
This article was supported by Agency for Healthcare Research and Quality (Zach-
5. Zhao J, Li H, Kung D, Fisher M, Shen Y, Liu R. Impact of the COVID-19 epi-
rison, K08 HS024561).
demic on stroke care and potential solutions. Stroke. 2020;51:1996–2001.
Disclosures 6. Teo KC, Leung WCY, Wong YK, Liu RKC, Chan AHY, Choi OMY, Kwok
WM, Leung KK, Tse MY, Cheung RTF, et al. Delays in stroke onset to
Dr Zachrison reports grants from National Institutes of Health (NIH)-National In-
hospital arrival time during COVID-19. Stroke. 2020;51:2228–2231. doi:
stitute of Neurological Disorders and Stroke (NINDS), Controlled Risk Insurance
10.1161/STROKEAHA.120.030105
Company, Ltd (CRICO), and the American College of Emergency Physicians, as
7. Kerleroux B, Fabacher T, Bricout N, Moïse M, Testud B, Vingadassalom
well as personal fees from Portola Pharmaceuticals outside of the submitted work.
S, Ifergan H, Janot K, Consoli A, Ben Hassen W, et al; SFNR, the ETIS
Dr Bretzner received unrelated funding from the Société Française de Neurora-
registry, and the JENI-Research Collaborative. Mechanical thrombec-
diologie, Société Française de Radiologie and Fondation ISITE-ULNE. Dr Viswa-
tomy for acute ischemic stroke amid the COVID-19 outbreak: decreased
nathan reports grants from NIH, personal fees from Alynylam Pharmaceuticals,
activity, and increased care delays. Stroke. 2020;51:2012–2017. doi:
and personal fees from Biogen outside the submitted work. Dr Singhal reports
10.1161/STROKEAHA.120.030373
grants from NIH-NINDS during the conduct of the study; other from UpToDate
8. Siegler JE, Heslin ME, Thau L, Smith A, Jovin TG. Falling stroke rates during
(Wolters Kluwer Health, Inc), other from Medlink, Inc, personal fees from Omniox,
COVID-19 pandemic at a Comprehensive Stroke Center: cover title: falling
Inc, personal fees from Deck Therapeutics, Inc, personal fees from Biogen, other
stroke rates during COVID-19. J Stroke Cerebrovasc Dis. 2020;29:104953.
from American Academy of Neurology, and personal fees from Expert Testimony
9. Oxley TJ, Mocco J, Majidi S, Kellner CP, Shoirah H, Singh IP, De Leacy RA,
outside the submitted work. Dr Schwamm reports the following relationships rel-
Shigematsu T, Ladner TR, Yaeger KA, et al. Large-vessel stroke as a pre-
evant to research grants or companies that manufacture products for telemedi-
senting feature of Covid-19 in the young. N Engl J Med. 2020;382:e60. doi:
cine, thrombolysis, or thrombectomy: scientific consultant regarding trial design
10.1056/NEJMc2009787
and conduct on late window thrombolysis and member of steering committee
10. Sharma R, Zachrison KS, Viswanathan A, Matiello M, Estrada J, Anderson
for Genentech (TIMELESS, REGISTRATION: URL: https://www.clinicaltrials.gov;
CD, Etherton M, Silverman S, Rost NS, Feske SK, et al. Trends in telestroke
Unique identifier: NCT001747); user interface design and usability to LifeImage
care delivery: a 15-year experience of an academic hub and its net-
(privately held teleradiology company); stroke systems of care to the Massachu-
work of spokes. Circ Cardiovasc Qual Outcomes. 2020;13:e005903. doi:
setts Department of Public Health; member of a Data Safety Monitoring Board
10.1161/CIRCOUTCOMES.119.005903
(DSMB) for Penumbra (MIND NCT03342664); Diffusion Pharma PHAST-TSC
11. Wang S, Lee SB, Pardue C, Ramsingh D, Waller J, Gross H, Nichols FT
NCT03763929); PI, multicenter trial of stroke prevention for Medtronic (Stroke AF
3rd, Hess DC, Adams RJ. Remote evaluation of acute ischemic stroke: reli-
NCT02700945); PI, late window thrombolysis trial, NINDS (P50NS051343, MR
ability of National Institutes of Health Stroke Scale via telestroke. Stroke.
WITNESS NCT01282242); PI, StrokeNet Network NINDS (New England Region-
2003;34:e188–e191. doi: 10.1161/01.STR.0000091847.82140.9D
al Coordinating Center U24NS107243, CURENT); Co-I, The Impact of Telestroke
12. Zachrison KS, Leslie-Mazwi TM, Boulouis G, Goldstein JN, Regenhardt RW,
on Patterns of Care and Long-Term Outcomes, NINDS (R01NS111952); Co-I,
Viswanathan A, Lauer A, Siddiqui KA, Charidimou A, Rost N, et al. Frequency
REACH-PC tele-palliative care trial, PCORI (NCT03375489). The other authors
of early rapid improvement in stroke severity during interfacility transfer. Neu-
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report no conflicts.
rol Clin Pract. 2019;9:373–380. doi: 10.1212/CPJ.0000000000000667
13. Mapping COVID-19 - Dartmouth Atlas of Health Care. [Internet]. [Cited
2020 May 21]. https://www.dartmouthatlas.org/covid-19/hrr-mapping/.
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