Stroke ORIGINAL CONTRIBUTION Acute Stroke Care Is at Risk in the Era of COVID-19 Experience at a Comprehensive Stroke Center in Barcelona Salvatore Rudilosso, MD, PhD*; Carlos Laredo, MSc*; Víctor Vera, MD; Martha Vargas, PhD; Arturo Renú, MD, PhD; Laura Llull, MD, PhD; Víctor Obach, MD; Sergio Amaro, MD, PhD; Xabier Urra, MD, PhD; Ferrán Torres, MD, PhD; Francesc Xavier Jiménez-Fàbrega, MD; Ángel Chamorro , MD, PhD BACKGROUND AND PURPOSE: The purpose of the study is to analyze how the coronavirus disease 2019 (COVID-19) pandemic affected acute stroke care in a Comprehensive Stroke Center. METHODS: On February 28, 2020, contingency plans were implemented at Hospital Clinic of Barcelona to contain the COVID-19 pandemic. Among them, the decision to refrain from reallocating the Stroke Team and Stroke Unit to the care of patients with COVID-19. From March 1 to March 31, 2020, we measured the number of emergency calls to the Emergency Medical System in Catalonia (7.5 million inhabitants), and the Stroke Codes dispatched to Hospital Clinic of Barcelona. We recorded all stroke admissions, and the adequacy of acute care measures, including the number of thrombectomies, workflow metrics, angiographic results, and clinical outcomes. Data were compared with March 2019 using parametric or nonparametric methods as appropriate. RESULTS: At Hospital Clinic of Barcelona, 1232 patients with COVID-19 were admitted in March 2020, demanding 60% of the hospital bed capacity. Relative to March 2019, the Emergency Medical System had a 330% mean increment in the number of calls (158 005 versus 679 569), but fewer Stroke Code activations (517 versus 426). Stroke admissions (108 versus 83) and the number of thrombectomies (21 versus 16) declined at Hospital Clinic of Barcelona, particularly after lockdown of the population. Younger age was found in stroke admissions during the pandemic (median [interquartile range] 69 [64–73] versus 75 [73–80] years, P=0.009). In-hospital, there were no differences in workflow metrics, angiographic results, complications, or outcomes at discharge. CONCLUSIONS: The COVID-19 pandemic reduced by a quarter the stroke admissions and thrombectomies performed at a Comprehensive Stroke Center but did not affect the quality of care metrics. During the lockdown, there was an overload of emergency calls but fewer Stroke Code activations, particularly in elderly patients. Hospital contingency plans, patient transport systems, and population-targeted alerts must act concertedly to better protect the chain of stroke care in times of pandemic. Key Words: COVID-19 ◼ pandemic ◼ Spain ◼ thrombectomy ◼ workflow I n December 2019, the emergence of a novel corona- depending on the local intensity of the crisis, there is virus, severe acute respiratory syndrome coronavirus a high risk of preventing the application of well-estab- 2 (SARS-CoV-2), in Wuhan, China, has evolved into a lished therapies to patients with prevalent conditions, pandemic with reported cases in >200 countries.1 The such as cancer,2 acute myocardial infarction,3 or acute crisis is straining the healthcare system worldwide, and ischemic stroke.4 Correspondence to: Ángel Chamorro, MD, PhD, Department of Neuroscience, Hospital Clinic of Barcelona, 170 Villarroel, 08036 Barcelona, Spain. Email achamorro@ clinic.cat *Dr Rudilosso and C. Laredo contributed equally. For Sources of Funding and Disclosures, see page xxx. © 2020 American Heart Association, Inc. Stroke is available at www.ahajournals.org/journal/str Stroke. 2020;51:00–00. DOI: 10.1161/STROKEAHA.120.030329 July 2020   1 Rudilosso et al Acute Stroke Care in the Era of COVID-19 out-patient and in-patient services and the progressive opening Original Contribution Nonstandard Abbreviations and Acronyms of quarantine wards according to changing needs. As part of its general planning, HCB refrained from limiting the full capacity COVID-19 coronavirus disease 2019 and personnel of the Stroke Team and the Stroke Unit, including in-patient speech therapy and rehabilitation. The 24/7 availability ECASS II European Cooperative Acute Stroke of multimodal brain imaging, computed tomography–angiography, Study II and endovascular treatment for eligible patients was guaranteed. EMS Emergency Medical System The availability of brain magnetic resonance imaging was main- HCB Hospital Clinic of Barcelona tained during hospitalization, although the use of ultrasonography was replaced by vessel imaging studies. To further limit the risk of infection among the stroke personnel, we also abbreviated the The coronavirus disease 2019 (COVID-19) pandemic neurological exam to minimize physical contact with the patient, challenges hospital leaders to make time-sensitive, criti- and we limited the performance of transthoracic echocardiog- cal decisions about clinical operations, and resource allo- raphy by stroke neurologists or petitions of transesophageal cations.5 The impact of the ongoing crisis on acute stroke echocardiography to the Cardiology Department. Other perfor- care is not settled, and it may not be dependent only mance quality indicators were maintained mostly unchanged, on in-hospital decisions, but it may also depend on how including swallowing assessment, and in-hospital rehabilitation. efficient is the prehospital care system to provide opti- Symptomatic severe carotid stenosis requiring urgent revascular- ization was treated with stenting, whereas carotid endarterectomy mized prehospital triage and equitable access to acute was put on hold during the study period. Stable outpatients await- treatments.6 Here, we aimed to analyze the impact of the ing elective revascularization or other procedures to reduce stroke COVID-19 outbreak on the chain of acute stroke care or hemorrhagic risk (eg, incidental aneurysms) were deferred. in a Comprehensive Stroke Center in Barcelona, a city Out-patient services as discharge to rehabilitation centers were hard hit by the pandemic. The study paid special atten- maintained, whereas out-patient visits were performed only by tion to the number of Stroke Code activations, stroke telephone contact. All the ongoing randomized clinical trials that admissions, and the number of reperfusion therapies the Comprehensive Stroke Center was participating were also performed in eligible patients, highlighting the depen- put on hold, with the exception of the CHOICE trial (Chemical dence of efficient prehospital care for maximization of Optimization of Cerebral Embolectomy).9 the benefits of in-hospital care. Exceptionally, 2 stroke neurologists were relocated to the care of patients with COVID-19 during some days of March, and in-patient rehabilitation was not available during a week for a sick leave. The admission of new patients into the Stroke Unit was METHODS sectorized to limit contamination. Thus, patients with fever or pul- Acute Stroke Care in Catalonia monary symptoms were first admitted into an isolated bed and were transferred to the clean Stroke Unit only once a positive In Catalonia (total population of 7.5 million inhabitants), acute COVID-19 test was excluded. A chest computed tomography stroke care is provided through a network of 26 acute hospitals, scan to rule out findings suggesting COVID-19 was performed including 6 Comprehensive Stroke Center.7 The Emergency to patients before thrombectomy. It was only on April 1, 2020, Medical System (EMS) is the main activator of the Stroke Code that COVID-19 testing was available and mandatory before any and the patient transport system that guarantees the urgent new stroke admission. Early at the onset of the crisis, the hyper- and priority transfer of a patient with suspected acute stroke to acute assessment and management of patients was delivered the nearest hospital with the appropriate diagnostic and thera- under a Protected Stroke Code,10 which included the use of full peutic capacity. All Stroke Codes in Catalonia are prospectively personal protective equipment. A lockdown of Catalonia was recorded by EMS personnel and stored in the regionwide Codi started on March 15, and still it is maintained as on April 30. Ictus Catalunya Register.8 Hospital Clinic of Barcelona (HCB) is a public University Hospital with 713 hospital beds, including 48 intensive care Outcomes beds, serving as a community hospital to a population of The primary outcome of the study was the Stroke Code activa- 540 000 inhabitants and providing tertiary acute stroke care tions, stroke admissions, and reperfusion therapies (intravenous to a population of 2 200 000. The Stroke Service at HCB has thrombolysis or thrombectomy) performed in eligible patients a Stroke Unit with 8 semi-intensive care beds and 10 con- at HCB11 in March 2020. Other outcome measures included ventional hospital beds managed by a multidisciplinary team workflow metrics, such as time from symptom onset to hospital of vascular neurologists, neurosurgeons, neurointerventional- arrival, and time from hospital arrival to brain imaging, onset of ists, anesthesiologists, and emergency physicians. On aver- intravenous thrombolysis, or groin puncture. Efficacy and safety age, 1000 Stroke Codes are dispatched to our center every outcomes included the severity of stroke National Institutes of year, where roughly 300 acute reperfusion treatments are per- Health Stroke Scale at day 5 or hospital discharge, functional sta- formed, of which 200 are thrombectomies. tus (modified Rankin Scale score) at day 5 or hospital discharge, On February 15, 2020, the first patient with COVID-19 was and rates of successful recanalization (modified Thrombolysis in admitted at HCB (and in Catalonia). On February 28, HCB imple- Cerebral Infarction perfusion score 2b-3), and symptomatic hem- mented contingency plans to contain the pandemic, including orrhagic transformation (ECASS II [European Cooperative Acute suspension of all nonessential visits and adjustment of clinical Stroke Study II] criteria). All outcome variables were compared 2   July 2020 Stroke. 2020;51:00–00. DOI: 10.1161/STROKEAHA.120.030329 Rudilosso et al Acute Stroke Care in the Era of COVID-19 with data of March 2019 and were prospectively collected into Table 1. Effects of the Pandemic on the Number of Original Contribution local databases and in the regionwide Codi Ictus Catalunya Emergency Calls, Stroke Code Activations, and Stroke Registry. Data that support the findings of this study are available Admissions in Catalonia and at Hospital Clinic from the corresponding author on reasonable request. March 2019 March 2020 P Value The study protocol was approved by the local Clinical Research EMS Coordination Center Ethics Committee from HCB under the requirements of Spanish Monthly calls 158.005 679.569 <0.0001 legislation in the field of biomedical research, the protection of personal data, and the standards of Good Clinical Practice, as well Daily calls 5.056 23.266 <0.0001 as with the Helsinki Declaration (Reg. HCB/2020/0390). The Stroke Codes board waived the need for patients' consent. Catalonia 517 426 <0.01 Hospital Clinic 83 68 0.22 Statistical Methods Stroke admissions at HCB Continuous variables were reported as mean and SD or as median All admissions 108 (100) 83 (82) 0.07 and interquartile range and were compared with the Student t   Before lockdown* … 50 (60) or Mann-Whitney tests. Categorical variables were reported as   After lockdown* … 33 (40) proportions and compared with the χ2 and Fisher exact test. The Notification modality 0.53 analysis was performed using SPSS Version 25.0, and the level of significance was established at a 0.05 level (2-sided). EMS notifications 73 (68) 57 (69) Intramural notifications 10 (9) 11 (13) No notifications 25 (23) 15 (18) RESULTS Numbers are n (%) or median (IQR) as appropriate. EMS indicates Emergency From March 1 to March 31, 2020, 1232 patients with Medical System; HCB, Hospital Clinic of Barcelona; and IQR, interquartile range. *March 15, 2020. COVID-19 were admitted at HCB, and this overflow of admissions required a gradual opening of 31 quaran- tine areas in the hospital with 300 conventional beds, at our center between March 15 and 17, although there and 120 intensive care beds. As shown in Table 1, the was an average of 30 to 40 thousand emergency calls EMS Coordination Center received in Catalonia 158.005 during these 3 days in Catalonia. There was a slight fall in emergency calls in March 2019 and 679.569 in March the number of stroke admissions without previous notifi- 2020 (overall 330% increment). The number of daily cation compared with March 2019 (15 and 25; Table 1). emergency phone calls increased from 5.056 in March Stroke admissions in 2020 were significantly younger 2019 to 23.266 in March 2020 (360% increment; than in 2019, also in the subgroup of patients dispatched Table 1). Paradoxically, there was an 18% reduction in by the EMS, but these patents did not have other differen- the number of Stroke Codes activated in Catalonia (517 tial traits, including the sex, initial severity of stroke, stroke in 2019 and 426 in 2020), and a similar 18% reduction subtype, wake-up strokes, or stroke mimics (Table 2). in the Stroke Codes dispatched to HCB (83 in 2019 and Fewer intravenous thrombolysis and fewer thrombecto- 68 in 2020). In agreement with these declines, the num- mies were performed in eligible patients compared with ber of stroke admissions at HCB also showed in March March 2019, although there were no differences in pre- 2020 a 23% decline compared with March 2019 (83 hospital or in-hospital workflow metrics, including the and 108). The number of stroke admissions was further delay of arrival to hospital after symptom onset, the time reduced in the second fortnight of March 2020, after the delay in performing a diagnostic brain computed tomog- lockdown of Catalonia on March 15 (50 and 33 admis- raphy scan, the delay in implementing intravenous throm- sions); the reduction of stroke admissions was most bolysis or in performing thrombectomy (Table 2). The rates noticeable during the higher peaks of emergency calls of successful recanalization, hemorrhagic complications, (Figure). Indeed, there was not a single stroke admission and neurological impairment, and functional status at day Figure. Superposition of data in the period between March 1 and March 31, 2019 and 2020. On the left axis, the cumulative stroke admissions at Hospital Clinic during March 2019 (empty circles) and March 2020 (black squares) are shown. On the right axis, daily calls to Emergency Medical System (EMS) during March 2019 (gray dots) and March 2020 (gray squares) are shown. Stroke. 2020;51:00–00. DOI: 10.1161/STROKEAHA.120.030329 July 2020   3 Rudilosso et al Acute Stroke Care in the Era of COVID-19 Table 2. Main Characteristics of the Patients Admitted All these patients were transferred to a specific COVID Original Contribution Through Stroke Code Activation and Quality Measures of the ward. None of the COVID-19 negative patients on Acute Care Provided During the Pandemic in Relation to the Previous Year admission had to be transferred to a quarantine zone for developing COVID-19 symptoms at follow-up. March 2019; March 2020; N=83 N=68 P Value Baseline traits DISCUSSION Age, y There are little data informing how the COVID-19 pan-    All stroke codes 75 (73–80) 69 (64–73) 0.009 demic is affecting the care provided to patients with    EMS stroke codes 77 (74–81) 70 (64–75) 0.03 acute stroke. At HCB, with 1232 COVID-19 admis- Males 46 (55) 38 (56) 0.95 sions occurring in one month, the pandemic resulted Baseline NIHSS 9 (8–14) 6 (4–10) 0.41 in the occupation of 60% of the hospital bed capacity Wake-up strokes 20 (24) 17 (25) 0.85 and 150% increment in the number of intensive care Diagnosis beds. Meanwhile, the study also found declines in the Ischemic stroke 53 (64) 42 (62) 0.44 number of Stroke Code activations, stroke admissions, Hemorrhagic stroke 11 (13) 7 (9) and thrombectomies performed at our center of 18%, Stroke mimics 19 (23) 19 (28) 23%, and 24%, respectively. Nevertheless, during the Reperfusion therapy in eligible patients* pandemic it was possible to maintain, when not improve, IV thrombolysis 9 (17) 3 (7) 0.57 prehospital time delays, and in-hospital workflow metrics compared with 2019. The length of hospital stay, the rate Thrombectomy 21 (40) 16 (38) 0.87 of successful reperfusion after thrombectomy, and the None 23 (43) 23 (55) 0.27 rate of good clinical outcome at hospital discharge were Time delay (min) workflow similar to those attained in 2019. However, although the Stroke onset to hospital arrival 126 (95–216) 135 (86–217) 0.64 outcome at hospital discharge did not worsen during Hospital arrival to imaging 21 (19–26) 22 (20–27) 0.61 the pandemic period, we cannot exclude that limitations Hospital arrival to thrombolysis 28 (22–33) 23 (21–48) 0.92 in the availability of a thorough etiological workup in all Hospital arrival to puncture 61 (58–90) 56 (48–72) 0.35 admitted patients and the reduction in out-patient ser- Length of stay, days 5 (5–7) 4 (3–6) 0.92 vices could have influenced the long-term outcome or Angiographic and early clinical course the stroke recurrence rate. Thrombectomy procedural time 55 (37–65) 36 (30–66) 0.31 The decline of Stroke Codes observed at our center mTICI score 2b/3 14 (67) 13 (81) 0.32 was similar to the general reduction of Stroke Codes in NIHSS score day 5 4 (2–2) 6 (3–4) 0.22 Catalonia. As we had protected the in-hospital chain of stroke, the decline in stroke admissions during the pan- mRS score 0–2, day 5 40 (48) 41 (60) 0.13 demic resulted in the unusual finding of having several Death, day 5 6 (9.2) 8 (11.8) 0.33 Stroke Unit beds available most days of the month. The Symptomatic hemorrhagic 1 (3) 0 1.00 transformation underutilization of the Stroke Unit beds when there was an overload of hospital admissions was an undesirable Numbers are n (%), median (IQR) as appropriate. EMS indicates Emergency Medical System; IQR, interquartile range; IV, intravenous; mRS, modified Rankin result that should be prevented in future crises. Readap- Scale; mTICI, modified Thrombolysis in Cerebral Infarction; and NIHSS, National tation of the protocols of the patient transport systems, Institutes of Health Stroke Scale. giving preference to the dispatch of patients to centers *Patients with acute ischemic stroke and excluding from the numerator stroke mimics or hemorrhagic strokes. willing to protect the chain of acute stroke care, would facilitate the access to stroke care to many patients who 5 or at hospital discharge, were similar to those found in may remain untreated under strained healthcare condi- 2019. During the study period, none of the patients who tions. Therefore, we concur with recent claims support- ing the need of establishing centralized stroke treatment were awaiting an elective procedure were admitted at our centers where sufficient stroke care resource can be center with an impending acute stroke. secured, particularly at times of medical crisis, and to Mandatory COVID-19 testing for all acute stroke have stroke services that can continue to function.12 patients was implemented at HCB on April 1. Thus, only Arguably, the overload of emergency calls during the 8 of 83 (10%) patients were tested in March 2020, of pandemic in Catalonia, with peaks of >41.000 emergency which 4 (5%) patients were COVID-19+ on admission. calls at a single day, could have caused difficulty in the cor- Of the latter, 2 patients had a final diagnosis of confu- rect activation of the Stroke Code at an overloaded EMS sional state, one had encephalitis, and only one patient Coordination Center. For the stroke admissions at HCB with atrial fibrillation that presented with central facial were significantly younger during the pandemic, it is also palsy and respiratory symptoms had an ischemic stroke. possible that fewer Stroke Codes were activated because 4   July 2020 Stroke. 2020;51:00–00. DOI: 10.1161/STROKEAHA.120.030329 Rudilosso et al Acute Stroke Care in the Era of COVID-19 older patients were more reluctant to demand emergency Sources of Funding Original Contribution assistance for the fear of COVID-19, as it carries a higher We thank the support of the Spanish Ministry of Economy and Competitiveness for grant to Dr Chamorro (project RD/0019/0014 RETIC Invictus plus, funded risk of severe infection and death rates in older patients.13 by Instituto de Salud Carlos III and cofunded by European Regional Development Certainly, we cannot either exclude that isolation among Fund [ERDF]). Salvatore Rudilosso received funding from Instituto de Salud Car- los III, with a Grant for Health Research (CM18/00116). Carlos Laredo received the elderly could have played a role in the relatively younger funding from Instituto de Salud Carlos III, with a Predoctoral Grant for Health age of the admitted patients. The lockdown of Catalonia on Research (PFIS, FI16/00231). Xabier Urra is sponsored by the Instituto de Salud March 15 was also associated with a rocketing increment Carlos III, reference number INT19/00020, and by the European Social Fund The ESF—Investing in your future. This work was partially developed at the build- of emergency calls and a more marked decline of stroke ing Centro Esther Koplowitz, Barcelona, Research Centers of Catalonia (CERCA) admissions. In anticipation of the decline in acute stroke Program/Generalitat de Catalunya. care in future crises, it is advisable to activate early during Disclosures the crisis media reminders to the population of the impor- None. tance of acting quickly and calling the EMS in the face of suspicion of a stroke. Interventions and activities aimed at reducing social isolation and loneliness particularly of older REFERENCES 1. Mahase E. Covid-19: WHO declares pandemic because of “alarm- adults are also required.14 ing levels” of spread, severity, and inaction. BMJ. 2020;368:m1036. doi: Only 5% of the patients in this series were found 10.1136/bmj.m1036 to be COVID-19+ on admission, and no patient devel- 2. Schrag D, Hershman DL, Basch E. Oncology practice during the COVID-19 pandemic. JAMA. doi: 10.1001/jama.2020.6236 oped the disease at follow-up, but only 10% of the 3. Tam CF, Cheung KS, Lam S, Wong A, Yung A, Sze M, et al. Impact of Corona- patients were properly screened. 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DOI: 10.1161/STROKEAHA.120.030329 July 2020   5