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Long-term evaluation of the COVID-19 pandemic impact on acute stroke management: an analysis of the 21-month data from a medical facility in Tokyo

Long-term evaluation of the COVID-19 pandemic impact on acute stroke management: an analysis of... Introduction The coronavirus disease 2019 (COVID-19) pandemic has caused a global public health crisis and profoundly impacted acute treatment delivery. This study conducted long-term evaluations of the impact of the pandemic on acute stroke management. Methods Data from a university-owned medical facility in Tokyo, Japan, were retrospectively analyzed. The number of hos- pital admissions for stroke and time metrics in the management of patients with acute ischemic stroke were evaluated. A year- over-year comparison was conducted using data from April 2019 to December 2021 to assess the impact of the pandemic. Results The year-over-year comparison demonstrated that the number of admissions of patients with stroke and patients who underwent magnetic resonance imaging (MRI), intravenous recombinant tissue plasminogen activator (rt-PA), and thrombectomy during the pandemic remained comparable to the pre-COVID data. However, we found a decrease in the number of admissions of patients with stroke alerts and stroke when hospital cluster infection occurred at this facility and when the region hosted the Tokyo Olympics games during the surge of infection. The door-to-computed tomography time in 2021 was affected. This is plausibly due to the reorganization of in-hospital stroke care pathways after hospital cluster infection. However, no significant difference was observed in the onset-to-door, door-to-MRI, door-to-needle, or door-to- groin puncture times. Conclusions We did not observe long-term detrimental effects of the pandemic at this site. Prevention of hospital cluster infections remains critical to provide safe and timely acute stroke management during the pandemic. Keywords COVID-19 · Pandemic impacts · Stroke care pathways · Admissions · Time measures Abbreviations rt-PA Intravenous recombinant tissue plasminogen COVID-19 Coronavirus disease 2019 activator MRI Magnetic resonance imaging MW Mann–Whitney non-parametric U tests CT Computerized tomography Introduction An acute ischemic stroke is a critical event. For early restora- * Hitoshi Mitsuhashi tion of blood flow in acute ischemic stroke, arterial recanali- hm18@waseda.jp zation must be provided by administering recombinant tissue Takashi Mitsuhashi plasminogen activator (rt-PA) or performing thrombectomy t.mitsuhashi@juntendo-nerima.jp in a timely and safe manner. As the coronavirus disease 2019 Joji Tokugawa (COVID-19) pandemic requires restrictive contact precau- j.tokugawa@juntendo-nerima.jp tions and reorganizations of established stroke care path- 1 ways, it is important to evaluate the pandemic impact on Department of Neurosurgery, Juntendo University Nerima acute stroke management and present findings to healthcare Hospital, Takanodai 3-1-10, Nerima, Tokyo 177-8521, Japan 2 providers and policymakers to optimize pre- and in-hospital School of Commerce, Waseda University, Nishi-Waseda workflows. 1-6-1, Shinjuku, Tokyo 169-8050, Japan Vol.:(0123456789) 1 3 Acta Neurologica Belgica Table 1 summarizes 32 papers on the global pandemic potential reason for this inconclusiveness might be varia- impacts published in 2020 and 2021. These studies evalu- tions in healthcare systems across different countries and ated the number of stroke-related admissions and key time regions. Another reason might be the use of short-term data, process measures such as onset-to-door time, door-to-com- with some exceptions [5, 30], which might capture imme- puted tomography (CT) time, and door-to-groin puncture diate responsive effects shortly after the beginning of the time because delays in these measures limit the restoration pandemic [3, 31]. of perfusion in acute ischemic stroke. Therefore, this study aimed to analyze the pandemic’s Although most studies agreed upon a decline in the long-term effects by comparing the data after the begin - number of admissions during the pandemic, their findings ning of the COVID-19 pandemic regarding acute treatment regarding key process time measures are inconclusive. A delivery for patients with stroke with the pre-COVID data in 2019. Table 1 Previous studies on the impacts of the pandemic in acute stroke management Data Admissions Onset-to-door Door-to-CT Door- to-groin puncture Agarwal et al. [1] March 1 to May 15, 2020, New York ↓ → ↑ ↑ Amukoutuwa et al. 2] March 1 to May 10, 2020, Australia ↓ n.a n.a n.a Brunetti et al. [3] March 11 to May 4, 2020, Rome Italy ↓ ↑ n.a ↑ D'Anna et al. [4] March 23 to June 30, 2020, London ↓ ↑ → → Drenck et al. [5] March 13, 2020 to February 28, 2021, Denmark ↓ n.a n.a n.a Frisullo et al. [6] March 11 to April 11, Rome, Italy ↓ ↑ → ↑ Fuentes et al. [7] February 25 to April 25, 2020, Madrid, Spain ↓ n.a n.a ↑ Ghoreishi et al. [8] February 18 to July 18, 2020, Zanjan Province, Iran ↓ n.a n.a n.a Jasne et al. [9] January to April, 2020, New Haven, Connecticut ↓ → n.a → Kansagra et al. [10] February to April, 2020, US ↓ n.a n.a n.a Katsanos et al. [11] March 1 to April 30, 2020, Ontario, Canada n.a → ↑ → Kim et al. [12] March 1, 2020 to February 28, 2021, Busan, Korea ↓ n.a n.a n.a Koge et al. [13] April to July, 2020, Japan ↓ → ↑ ↑ Kristoffersen et al. [14] January to September, 2020, Norway ↓ n.a n.a n.a Kwan et al. [15] January to April, 2020, UK ↓ → → → Lee et al. [16] February 18 to April 17, 2020, Daegu, Korea n.a ↑ → → Nogueira et al. [17] March 1 to May 31, 2020, 40 countries ↓ n.a n.a n.a Nogueira et al. [18] March 1 to June 30, 2020, 70 countries ↓ n.a n.a n.a Padmanabhan et al. [19] March 15 to April 14, 2020, UK ↓ → n.a → Raymaekers et al. [20] March to May, 2020, Belgium ↓ n.a n.a → Richter et al. [21] March 16 to May 15, 2020, Germany ↓ n.a n.a n.a Rudilosso et al. [22] March 1 to 31, 2020, Barcelona ↓ → → → Sharma et al. [23] March 23 to April 19, 2020, Boston ↓ → n.a n.a Siegler et al. [24] March to July, 2020, US n.a n.a ↓ → Teo et al. [25] January 23 to March 25, 2020, Hong Kong ↓ → n.a → Tiedt et al. [26] March to May 2020, Germany → → → ↑ Uchino et al. [27] March 9 to April 2, 2020, Ohio ↓ → → → Velez et al. [28] March 11 to April 2020, Chicago ↓ ↑ n.a n.a Velilla-Alonso et al. [29] March 14 to May 14, 2020, Spain ↓ ↑ → → Vollmuth et al. (2021) March to June, 2020, Germany ↓ n.a n.a n.a Wong et al. [30] April, 2020 to January, 2021, North Carolina ↓ n.a n.a n.a Wu et al. [31] January 24 to April 29, 2020, Beijing ↓ → n.a → ↓: decreased, ↑ increased, → did not change 1 3 Acta Neurologica Belgica puncture. These measures indicate the time frame for acute Methods stroke treatment. Onset-to-door time represents the time interval from stroke onset to hospital admission. Door- Data site to-CT and door-to-MR imaging represent time intervals from hospital admission to the first two phases of in- The data used in this study are available from the corre- hospital care pathways. At this facility, after initial triage sponding author upon reasonable request. and examination, a CT scan is first performed for patients This was a retrospective single-center observational with suspected acute stroke, followed by MR imaging if study at a medium-sized facility owned by a medical uni- CT images show no hemorrhagic lesion. The physicians versity hospital in Tokyo, Japan. This is the only primary perform thrombolysis and thrombectomy in patients with 24/7 medical center in the locality. We used all the data ischemic lesions, with or without large vessel occlusion of the patients with stroke alerts admitted to this facility. on MR imaging. The facility’s emergency room and CT In 2020 and 2021, metropolitan Tokyo experienced four room co-locate with the emergency entrance on the first waves of the COVID-19 pandemic. During the pandemic, floor. The distances to the emergency room and CT room the Japanese government issued four country-wide stay- were 10 and 15 m, respectively. The MR imaging room at-home orders: (1) April 7–May 25, 2020; (2) January was located adjacent to the CT room. We also evaluated 7–March 21, 2021; (3) April 25–June 20, 2021; and (4) the door-to-needle time (the time interval from hospital July 12–September 30, 2021. We used the 21-month data admission to the initiation of recombinant tissue plasmino- from April 1, 2020, to December 31, 2021, as the pan- gen activator (rt-PA) drug treatment) and the door-to-groin demic period data and from January 1, 2019, to December puncture time of patients who underwent thrombectomy. 31, 2019, as the baseline data for making year-over-year comparisons. Since the pandemic, this facility has optimized stroke Statistical analysis care pathways to protect frontline healthcare workers against infections. In April 2020, it implemented standard In the first analysis, we assessed the pandemic effects by precautions, required the workers to use protective equip- reporting the monthly averages of the aforementioned num- ment, set up multiple hygienic barriers outside the facility bers in 2019, 2020 (from April to December), and 2021. to triage transported patients with COVID-like symptoms, We used the 2019 data as the baseline pre-COVID data and and made a dedicated pathway for patients “suspected” to compared them with those of the 2020 and 2021 data as the have COVID-19. Moreover, in August 2020, the facility pandemic data. We performed Mann–Whitney non-paramet- implemented decontamination procedures in a depressur- ric U tests (MW tests) to assess statistical differences. As all ized room. Despite these efforts, hospital cluster infection patients admitted to this facility with stroke alerts underwent occurred in September 2020, whereby the facility closed CT scans, we did not report the door-to-CT statistics. Addi- emergency admission from September 30 to October 17, tionally, to capture potential seasonal fluctuations in patient 2020. After the reopening, all the transported patients were volumes during the pandemic, we reported the number of required to undergo triage in the clean booths outside. transported patients and patients with stroke per day in each month and conducted t-tests and MW tests. In the second analysis, we reported the results of t-tests and MW tests and reported whether the means of the time Measurements measures during the treatment periods were significantly dif- ferent from those of the control periods. This study comprised two analyses. In the first analysis, this study compared the number of stroke-related admis- sions and acute treatments from April 2020 to December Results 2021 with the number in the same period in 2019. We evaluated the number of patients admitted to the facility Analysis 1: volume with stroke alerts, patients diagnosed with a stroke, and patients who underwent magnetic resonance (MR) imag- In 2019, the monthly average of patients presenting with ing, rt-PA, and thrombectomy. signs of a stroke or transient ischemic attack (TIA) was In the second analysis, this study used key process time 29.75 patients (Table 2). We observed a decrease in this measures for stroke care, including time intervals from number in both 2020 (23.33 patients, MW statistics = 80.5, (1) symptom onset-to-door, (2) door-to-CT, (3) door-to- p = 0.064) and 2021 (27.00 patients, MW statistics = 89.5, MR imaging, (4) door-to-needle, and (5) door-to-groin p = 0.325), but these differences from the baseline 1 3 Acta Neurologica Belgica pre-COVID data were not statistically significant at the To further understand the significant decline in the num - α = 0.05 level. We also found a decrease in the monthly ber of patients with stroke alerts, we made month-to-month average number of patients treated with rt-PA from 3.83 in comparisons between the pre-COVID and COVID periods 2019 to 2.67 in 2020 (MW statistics = 59.5, p = 0.385) and (Table 3 and Fig. 1). The daily average number of patients 2.25 in 2021 (MW statistics = 93.5, p = 0.090), but these admitted to the facility decreased from 0.94 in July 2019 to results were not statistically significant at the α = 0.05 0.55 in July 2020 (t-statistics = 2.249, p = 0.029, MW sta- level. The number of patients who were diagnosed with tistics = 602.0, p = 0.059); however, the number of patients stroke and underwent MRI and thrombectomy remained with stroke did not decrease statistically (t-statistics = 1.447, constant throughout the study period (Table 2). p = 0.154, MW statistics = 555.5, p = 0.232), suggesting a decrease in the admissions of stroke mimics only. Table 2 Monthly average All patients Stroke patients MRI rt-PA Thrombectomy number of patients and stroke care treatments 2019, 1/1 to 12/31 29.75 22.75 19.17 3.83 1.42 2020, 4/1 to 12/31 23.33 17.78 16.67 2.67 1.56 MW 80.5 75.0 69.5 59.5 16.0 p 0.063 0.143 0.284 0.385 0.405 2021, 1/1 to 12/31 27.00 20.17 19.50 2.25 1.75 MW 89.5 88.0 72.5 93.5 36.0 p 0.325 0.368 1.000 0.090 0.711 MW Mann–Whitney non-parametric U test statistics Table 3 The number of patients All patients Stroke patients per day N N in 2019 t-stats p MW p N N in 2019 t-stats p MW p 2020-04 0.90 1.13 1.013 0.316 495.5 0.480 0.73 0.73 0.000 1.000 427.0 0.718 2020-05 1.06 0.90 0.643 0.523 437.5 0.526 0.77 0.77 0.000 1.000 499.5 0.777 2020-06 0.77 0.90 0.592 0.556 501.0 0.424 0.73 0.73 0.000 1.000 467.0 0.790 2020-07 0.55 0.94 2.249 0.029 602.0 0.059 0.42 0.65 1.447 0.154 555.5 0.232 2020-08 1.13 0.61 2.300 0.025 329.5 0.024 0.87 0.55 1.533 0.131 389.5 0.164 2020-09 0.67 0.93 1.267 0.211 507.0 0.363 0.53 0.63 0.574 0.568 478.0 0.650 2020-10 0.13 0.94 4.702 0.000 742.5 0.000 0.03 0.68 4.671 0.000 730.0 0.000 2020-11 0.93 1.17 0.903 0.370 514.0 0.324 0.63 1.07 1.793 0.078 575.0 0.048 2020-12 0.74 1.13 1.646 0.105 573.5 0.167 0.52 0.84 1.597 0.116 570.5 0.167 2021-01 0.74 0.97 0.830 0.410 566.0 0.195 0.55 0.74 0.894 0.375 557.5 0.229 2021-02 1.11 1.11 0.000 1.000 388.5 0.959 0.93 0.93 0.000 1.000 392.0 1.000 2021-03 1.23 1.03 -0.747 0.458 417.0 0.340 0.90 0.68 -1.125 0.265 375.5 0.108 2021-04 1.13 1.13 0.000 1.000 444.0 0.930 0.80 0.73 -0.325 0.747 404.0 0.468 2021-05 1.23 0.90 -1.048 0.300 445.5 0.608 0.90 0.77 -0.499 0.620 470.0 0.879 2021-06 0.93 0.90 -0.151 0.881 447.5 0.975 0.63 0.73 0.531 0.597 474.0 0.704 2021-07 0.55 0.94 1.980 0.052 610.0 0.049 0.35 0.65 1.800 0.077 591.0 0.076 2021-08 0.58 0.61 0.177 0.860 468.5 0.857 0.35 0.55 1.186 0.241 540.5 0.326 2021-09 0.67 0.93 1.153 0.254 524.0 0.241 0.63 0.63 0.000 1.000 466.5 0.793 2021-10 0.71 0.94 1.113 0.270 538.5 0.382 0.48 0.68 1.068 0.290 552.0 0.263 2021-11 1.00 1.17 0.681 0.499 495.0 0.490 0.73 1.07 1.522 0.134 535.0 0.184 2021-12 0.81 1.13 1.267 0.210 566.0 0.206 0.71 0.84 0.603 0.549 512.0 0.638 The table compares the daily average number of transported patients and patients with stroke for each month during the coronavirus disease (COVID) periods with the corresponding monthly pre-COVID data. t-stats means t statistics of two-group comparisons of means (two-sided) t-stats t statistics of two group mean comparison (two-sided), MW Mann–Whitney non-parametric U test statistics 1 3 Acta Neurologica Belgica patients dropped from 0.94 in 2019 to 0.55 in 2021 (t-sta- tistics = 1.980, p = 0.052, MW statistics = 610.0, p = 0.049), while that of patients with stroke decreased from 0.65 in 2019 to 0.35 in 2021 (t-statistics = 1.800, p = 0.077, MW statistics = 591.0, p = 0.076). Analysis 2: key process time measures We evaluated the pandemic impact on five key process time measures (Fig. 2 and Table 4). The only time measure that worsened was the door-to-CT time in 2021. In 2019, the door-to-CT time was 15.19 min with a standard deviation of 5.56 min, whereas, in 2021, it was 17.55 min with a stand- ard deviation of 12.91 min. The mean difference, 2.36 min, was statistically significant (t-statistics = − 3.030, p = 0.003, Fig. 1 Patients with stroke alerts per day. This figure shows changes MW statistics = 54,544.0, p = 0.249). However, we found no in the monthly average of the number of patients with stroke alerts significant difference in the door-to-MR imaging, door-to- per day. The solid line indicates the pandemic data. The observa- needle, and door-to-groin puncture times, suggesting that tion periods during the pandemic started in April 2020 and ended in the overall quality of acute stroke care measured with time December 2021. The dotted line represents the baseline data in 2019. The number of patients dropped sharply in October 2020 due to hos- intervals did not decrease during the pandemic. pital cluster infection Discussion Substantial drops were observed in October 2020 (Table 3 and Fig. 1). The number of patients admitted and patients The COVID-19 pandemic has threatened global and national with stroke dropped from 0.94 in 2019 to 0.13 in 2020 and healthcare systems. As the pandemic gave rise to the need from 0.68 in 2019 to 0.03 in 2020, respectively. We also for reorganization of pre- and in-hospital stroke care path- found a systematic decline in July 2021. The number of ways, one of the threats that previous studies [1, 6] reported Fig. 2 Key process time measures. The figures show the five key pro- 2021, respectively. As not all patients admitted to the facility received cess time measures of each patient in minutes. The white areas rep- the same treatment, the numbers of patients included in each of these resent the baseline data in 2019, whereas the lighter and darker grey panels are different areas indicate the pandemic data in 2020 (April to December) and 1 3 Acta Neurologica Belgica is the reduced quality of acute stroke management. Previous studies evaluated pre- and in-hospital performance indica- tors such as the number of patients admitted who presented with signs of stroke or TIA and door-to-groin puncture time. The findings in these studies are rather mixed, with some reporting detrimental impacts [28, 29], whereas others report limited impacts [26]. One potential source of such disagree- ments is the duration of the observation periods. The mean of the observation periods in 32 papers was 3.63 months with a standard deviation of 2.94 months (Table 1). Drenck et  al. [5] and Kim et  al. [12] used the longest observa- tion period data of 12 months. In this study, we used the 21-month pandemic data at a medical facility in Tokyo, Japan, evaluated the long-term pandemic impacts, and con- ducted a retrospective single-center observational study. In our first analysis, we studied the effects of the monthly average number of patients and stroke care treatments. We demonstrated a significant decline in the number of admis- sions of patients with stroke alerts in 2020. In October 2020, the daily average number of patients with stroke alerts and patients with stroke dropped by 42% and 36%, respectively. We attribute the decline in 2020 to the hospital cluster infec- tion in October 2020, which caused the facility to close emergency admission from September 30 to October 17, Another systematic decline occurred in July 2021. In addition to the surge of infections from 12,977 in June 2021 to 44,448 in July 2021 (342% increase), the region hosted the Olympic games in that month. Games during the pandemic sparked intense public debates. There is a possibility that social anxiety might raise patients’ fear of COVID-19, which might cause delays in seeking help. This finding suggests that healthcare providers and policymakers should evaluate the value of hosting large social events such as the Olympic games with a consideration of this indirect effect. Despite these significant differences, we did not observe any systematic differences in other periods between the pre-COVID and COVID periods, leading us to conclude that COVID-19 did not have any substantial impacts on the number of hospital admissions as well as that of stroke care treatments. In our analysis using daily average data, we found no initial decline even shortly after the beginning of the pandemic in April 2020. This might be due to the limited magnitude of the pandemic and the resulting low social fear of in-hospital infections in this region. The highest daily number of COVID-19 cases in metropolitan Tokyo during the observation period was 5908 (August 13, 2021), whereas that in New York State and California was 85,476 (Decem- ber 31, 2021) and 50,913 (December 31, 2021), respectively. Our interpretation based on the low social fears of in- hospital infections is in line with our findings in the sec- ond analysis (Table 4). The onset-to-door time would sig- nificantly increase if patients developed fear; however, we 1 3 Table 4 Effects on the key process time measures 2019, 1/1 to 12/31 2020, 4/1 to 12/31 2021, 1/1 to 12/31 Time interval N Mean SD N Mean SD t-test p MW p N Mean SD t-test p MW p Onset-to-Door 329 311.56 330.33 189 193.05 283.90 4.304 0.000 39,870.5 0.000 308 276.63 353.20 1.287 0.199 54,815.5 0.074 Door-to-CT 357 15.19 5.56 204 15.99 6.31 1.507 0.133 33,697.5 0.140 322 17.55 12.91 -3.030 0.003 54,544.0 0.249 Door-to-MRI 230 31.89 16.57 147 32.69 20.60 -0.397 0.691 16,592.5 0.762 234 34.11 17.39 -1.405 0.161 24,852.0 0.154 Door-to-needle 46 65.98 17.40 24 66.46 16.00 -0.116 0.908 539.5 0.882 27 72.15 36.93 -0.817 0.420 646.0 0.779 Door-to-groin puncture 17 90.00 27.39 14 103.79 26.93 -1.408 0.170 84.0 0.171 21 94.57 39.06 -0.423 0.675 177.0 0.977 SD standard deviations, t-stats t statistics of two group mean comparison (two-sided), MW Mann–Whitney non-parametric U test statistics Acta Neurologica Belgica observed that it decreased in 2020 and 2021. The decline to provide safe and timely acute stroke management during in the onset-to-door time suggests that the decrease in the the pandemic. number of patients treated with rt-PA in 2021 (Table 2) did not result from delays in the onset-to-door time. Author contributions Concept and design: MT, JT and MH. Acquisi- In the second analysis, we studied the effects of other key tion of data: MT. Analysis of data: MH. Drafting of the manuscript: process time measures. Almost all the measures remained MT and MH. Critical revision of the manuscript for important intel- constant throughout the study period, suggesting that the lectual content: JT. Obtained funding: MH, MT, and JT. facility managed to avoid any hazardous delays in in-hospital stroke care that COVID-19 could cause. We did not find sub- Funding This work was supported by JSPS KAKENHI (Grant Num- bers 18K18584 and 21K18443). stantial increases in the onset-to-door, door-to-MR imaging, door-to-needle, or door-to-groin puncture times. Our results Data availability The data used in this study are available from the are consistent with other studies that did not report such a corresponding author upon reasonable request. delay [15, 22]. However, we observed significant delays in the door-to-CT time in 2021, which is plausibly due to the Declarations facility’s optimization of the stroke care pathways after hos- pital cluster infection in October 2021. The renewed proto- Conflict of interest The authors declare that they have no competing cols enhanced the protection of frontline healthcare workers interests. against infections but could have increased the mean door- Ethical approval This study was conducted retrospectively using data to-CT time in 2021. obtained for clinical purposes. Approval was obtained from the ethics An implication of our study is the importance of prevent- committee of Waseda University (2020-382) and Juntendo University ing hospital cluster infections. The cluster infection not only Nerima Hospital (2018-43). reduced the number of admissions but also required addi- Consent for publication Not applicable. tional reorganization in stroke care pathways. As a result of the hospital cluster infection, the facility made responsive Open Access This article is licensed under a Creative Commons Attri- and reactive actions, requiring longer adaptations and learn- bution 4.0 International License, which permits use, sharing, adapta- ing than preventive actions. The pandemic impacts could be tion, distribution and reproduction in any medium or format, as long reduced further if medical facilities take preemptive rather as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes than remedial actions. Healthcare providers and policymak- were made. The images or other third party material in this article are ers should encourage medical facilities to allocate more included in the article's Creative Commons licence, unless indicated resources to prevent hospital cluster infections. otherwise in a credit line to the material. If material is not included in Our study had several limitations. First, this study was the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will based on data collected from a single medical facility in a need to obtain permission directly from the copyright holder. To view a specific area. Further research using long-term data from copy of this licence, visit http://cr eativ ecommons. or g/licen ses/ b y/4.0/ . other countries and regions is needed to enhance generaliz- ability. Second, although the number of stroke admissions and the time metrics are important to assess the pandemic effects, this study did not examine the quality of treatment References received by patients and their overall health and welfare. The 1. Agarwal S, Scher E, Rossan-Raghunath N, Marolia D, Butnar M, goal of acute stroke management is to decrease morbidity Torres J, Zhang C, Kim S, Sanger M, Humbert K, Tanweer O, and mortality [8, 9]. 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Nogueira RG, Abdalkader M, Qureshi MM, Frankel MR, Mansour OY, Yamagami H, Qiu Z, Farhoudi M, Siegler JE, Yaghi S, Raz 1 3 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Acta Neurologica Belgica Springer Journals

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Publisher
Springer Journals
Copyright
Copyright © The Author(s) 2022
ISSN
0300-9009
eISSN
2240-2993
DOI
10.1007/s13760-022-01979-0
Publisher site
See Article on Publisher Site

Abstract

Introduction The coronavirus disease 2019 (COVID-19) pandemic has caused a global public health crisis and profoundly impacted acute treatment delivery. This study conducted long-term evaluations of the impact of the pandemic on acute stroke management. Methods Data from a university-owned medical facility in Tokyo, Japan, were retrospectively analyzed. The number of hos- pital admissions for stroke and time metrics in the management of patients with acute ischemic stroke were evaluated. A year- over-year comparison was conducted using data from April 2019 to December 2021 to assess the impact of the pandemic. Results The year-over-year comparison demonstrated that the number of admissions of patients with stroke and patients who underwent magnetic resonance imaging (MRI), intravenous recombinant tissue plasminogen activator (rt-PA), and thrombectomy during the pandemic remained comparable to the pre-COVID data. However, we found a decrease in the number of admissions of patients with stroke alerts and stroke when hospital cluster infection occurred at this facility and when the region hosted the Tokyo Olympics games during the surge of infection. The door-to-computed tomography time in 2021 was affected. This is plausibly due to the reorganization of in-hospital stroke care pathways after hospital cluster infection. However, no significant difference was observed in the onset-to-door, door-to-MRI, door-to-needle, or door-to- groin puncture times. Conclusions We did not observe long-term detrimental effects of the pandemic at this site. Prevention of hospital cluster infections remains critical to provide safe and timely acute stroke management during the pandemic. Keywords COVID-19 · Pandemic impacts · Stroke care pathways · Admissions · Time measures Abbreviations rt-PA Intravenous recombinant tissue plasminogen COVID-19 Coronavirus disease 2019 activator MRI Magnetic resonance imaging MW Mann–Whitney non-parametric U tests CT Computerized tomography Introduction An acute ischemic stroke is a critical event. For early restora- * Hitoshi Mitsuhashi tion of blood flow in acute ischemic stroke, arterial recanali- hm18@waseda.jp zation must be provided by administering recombinant tissue Takashi Mitsuhashi plasminogen activator (rt-PA) or performing thrombectomy t.mitsuhashi@juntendo-nerima.jp in a timely and safe manner. As the coronavirus disease 2019 Joji Tokugawa (COVID-19) pandemic requires restrictive contact precau- j.tokugawa@juntendo-nerima.jp tions and reorganizations of established stroke care path- 1 ways, it is important to evaluate the pandemic impact on Department of Neurosurgery, Juntendo University Nerima acute stroke management and present findings to healthcare Hospital, Takanodai 3-1-10, Nerima, Tokyo 177-8521, Japan 2 providers and policymakers to optimize pre- and in-hospital School of Commerce, Waseda University, Nishi-Waseda workflows. 1-6-1, Shinjuku, Tokyo 169-8050, Japan Vol.:(0123456789) 1 3 Acta Neurologica Belgica Table 1 summarizes 32 papers on the global pandemic potential reason for this inconclusiveness might be varia- impacts published in 2020 and 2021. These studies evalu- tions in healthcare systems across different countries and ated the number of stroke-related admissions and key time regions. Another reason might be the use of short-term data, process measures such as onset-to-door time, door-to-com- with some exceptions [5, 30], which might capture imme- puted tomography (CT) time, and door-to-groin puncture diate responsive effects shortly after the beginning of the time because delays in these measures limit the restoration pandemic [3, 31]. of perfusion in acute ischemic stroke. Therefore, this study aimed to analyze the pandemic’s Although most studies agreed upon a decline in the long-term effects by comparing the data after the begin - number of admissions during the pandemic, their findings ning of the COVID-19 pandemic regarding acute treatment regarding key process time measures are inconclusive. A delivery for patients with stroke with the pre-COVID data in 2019. Table 1 Previous studies on the impacts of the pandemic in acute stroke management Data Admissions Onset-to-door Door-to-CT Door- to-groin puncture Agarwal et al. [1] March 1 to May 15, 2020, New York ↓ → ↑ ↑ Amukoutuwa et al. 2] March 1 to May 10, 2020, Australia ↓ n.a n.a n.a Brunetti et al. [3] March 11 to May 4, 2020, Rome Italy ↓ ↑ n.a ↑ D'Anna et al. [4] March 23 to June 30, 2020, London ↓ ↑ → → Drenck et al. [5] March 13, 2020 to February 28, 2021, Denmark ↓ n.a n.a n.a Frisullo et al. [6] March 11 to April 11, Rome, Italy ↓ ↑ → ↑ Fuentes et al. [7] February 25 to April 25, 2020, Madrid, Spain ↓ n.a n.a ↑ Ghoreishi et al. [8] February 18 to July 18, 2020, Zanjan Province, Iran ↓ n.a n.a n.a Jasne et al. [9] January to April, 2020, New Haven, Connecticut ↓ → n.a → Kansagra et al. [10] February to April, 2020, US ↓ n.a n.a n.a Katsanos et al. [11] March 1 to April 30, 2020, Ontario, Canada n.a → ↑ → Kim et al. [12] March 1, 2020 to February 28, 2021, Busan, Korea ↓ n.a n.a n.a Koge et al. [13] April to July, 2020, Japan ↓ → ↑ ↑ Kristoffersen et al. [14] January to September, 2020, Norway ↓ n.a n.a n.a Kwan et al. [15] January to April, 2020, UK ↓ → → → Lee et al. [16] February 18 to April 17, 2020, Daegu, Korea n.a ↑ → → Nogueira et al. [17] March 1 to May 31, 2020, 40 countries ↓ n.a n.a n.a Nogueira et al. [18] March 1 to June 30, 2020, 70 countries ↓ n.a n.a n.a Padmanabhan et al. [19] March 15 to April 14, 2020, UK ↓ → n.a → Raymaekers et al. [20] March to May, 2020, Belgium ↓ n.a n.a → Richter et al. [21] March 16 to May 15, 2020, Germany ↓ n.a n.a n.a Rudilosso et al. [22] March 1 to 31, 2020, Barcelona ↓ → → → Sharma et al. [23] March 23 to April 19, 2020, Boston ↓ → n.a n.a Siegler et al. [24] March to July, 2020, US n.a n.a ↓ → Teo et al. [25] January 23 to March 25, 2020, Hong Kong ↓ → n.a → Tiedt et al. [26] March to May 2020, Germany → → → ↑ Uchino et al. [27] March 9 to April 2, 2020, Ohio ↓ → → → Velez et al. [28] March 11 to April 2020, Chicago ↓ ↑ n.a n.a Velilla-Alonso et al. [29] March 14 to May 14, 2020, Spain ↓ ↑ → → Vollmuth et al. (2021) March to June, 2020, Germany ↓ n.a n.a n.a Wong et al. [30] April, 2020 to January, 2021, North Carolina ↓ n.a n.a n.a Wu et al. [31] January 24 to April 29, 2020, Beijing ↓ → n.a → ↓: decreased, ↑ increased, → did not change 1 3 Acta Neurologica Belgica puncture. These measures indicate the time frame for acute Methods stroke treatment. Onset-to-door time represents the time interval from stroke onset to hospital admission. Door- Data site to-CT and door-to-MR imaging represent time intervals from hospital admission to the first two phases of in- The data used in this study are available from the corre- hospital care pathways. At this facility, after initial triage sponding author upon reasonable request. and examination, a CT scan is first performed for patients This was a retrospective single-center observational with suspected acute stroke, followed by MR imaging if study at a medium-sized facility owned by a medical uni- CT images show no hemorrhagic lesion. The physicians versity hospital in Tokyo, Japan. This is the only primary perform thrombolysis and thrombectomy in patients with 24/7 medical center in the locality. We used all the data ischemic lesions, with or without large vessel occlusion of the patients with stroke alerts admitted to this facility. on MR imaging. The facility’s emergency room and CT In 2020 and 2021, metropolitan Tokyo experienced four room co-locate with the emergency entrance on the first waves of the COVID-19 pandemic. During the pandemic, floor. The distances to the emergency room and CT room the Japanese government issued four country-wide stay- were 10 and 15 m, respectively. The MR imaging room at-home orders: (1) April 7–May 25, 2020; (2) January was located adjacent to the CT room. We also evaluated 7–March 21, 2021; (3) April 25–June 20, 2021; and (4) the door-to-needle time (the time interval from hospital July 12–September 30, 2021. We used the 21-month data admission to the initiation of recombinant tissue plasmino- from April 1, 2020, to December 31, 2021, as the pan- gen activator (rt-PA) drug treatment) and the door-to-groin demic period data and from January 1, 2019, to December puncture time of patients who underwent thrombectomy. 31, 2019, as the baseline data for making year-over-year comparisons. Since the pandemic, this facility has optimized stroke Statistical analysis care pathways to protect frontline healthcare workers against infections. In April 2020, it implemented standard In the first analysis, we assessed the pandemic effects by precautions, required the workers to use protective equip- reporting the monthly averages of the aforementioned num- ment, set up multiple hygienic barriers outside the facility bers in 2019, 2020 (from April to December), and 2021. to triage transported patients with COVID-like symptoms, We used the 2019 data as the baseline pre-COVID data and and made a dedicated pathway for patients “suspected” to compared them with those of the 2020 and 2021 data as the have COVID-19. Moreover, in August 2020, the facility pandemic data. We performed Mann–Whitney non-paramet- implemented decontamination procedures in a depressur- ric U tests (MW tests) to assess statistical differences. As all ized room. Despite these efforts, hospital cluster infection patients admitted to this facility with stroke alerts underwent occurred in September 2020, whereby the facility closed CT scans, we did not report the door-to-CT statistics. Addi- emergency admission from September 30 to October 17, tionally, to capture potential seasonal fluctuations in patient 2020. After the reopening, all the transported patients were volumes during the pandemic, we reported the number of required to undergo triage in the clean booths outside. transported patients and patients with stroke per day in each month and conducted t-tests and MW tests. In the second analysis, we reported the results of t-tests and MW tests and reported whether the means of the time Measurements measures during the treatment periods were significantly dif- ferent from those of the control periods. This study comprised two analyses. In the first analysis, this study compared the number of stroke-related admis- sions and acute treatments from April 2020 to December Results 2021 with the number in the same period in 2019. We evaluated the number of patients admitted to the facility Analysis 1: volume with stroke alerts, patients diagnosed with a stroke, and patients who underwent magnetic resonance (MR) imag- In 2019, the monthly average of patients presenting with ing, rt-PA, and thrombectomy. signs of a stroke or transient ischemic attack (TIA) was In the second analysis, this study used key process time 29.75 patients (Table 2). We observed a decrease in this measures for stroke care, including time intervals from number in both 2020 (23.33 patients, MW statistics = 80.5, (1) symptom onset-to-door, (2) door-to-CT, (3) door-to- p = 0.064) and 2021 (27.00 patients, MW statistics = 89.5, MR imaging, (4) door-to-needle, and (5) door-to-groin p = 0.325), but these differences from the baseline 1 3 Acta Neurologica Belgica pre-COVID data were not statistically significant at the To further understand the significant decline in the num - α = 0.05 level. We also found a decrease in the monthly ber of patients with stroke alerts, we made month-to-month average number of patients treated with rt-PA from 3.83 in comparisons between the pre-COVID and COVID periods 2019 to 2.67 in 2020 (MW statistics = 59.5, p = 0.385) and (Table 3 and Fig. 1). The daily average number of patients 2.25 in 2021 (MW statistics = 93.5, p = 0.090), but these admitted to the facility decreased from 0.94 in July 2019 to results were not statistically significant at the α = 0.05 0.55 in July 2020 (t-statistics = 2.249, p = 0.029, MW sta- level. The number of patients who were diagnosed with tistics = 602.0, p = 0.059); however, the number of patients stroke and underwent MRI and thrombectomy remained with stroke did not decrease statistically (t-statistics = 1.447, constant throughout the study period (Table 2). p = 0.154, MW statistics = 555.5, p = 0.232), suggesting a decrease in the admissions of stroke mimics only. Table 2 Monthly average All patients Stroke patients MRI rt-PA Thrombectomy number of patients and stroke care treatments 2019, 1/1 to 12/31 29.75 22.75 19.17 3.83 1.42 2020, 4/1 to 12/31 23.33 17.78 16.67 2.67 1.56 MW 80.5 75.0 69.5 59.5 16.0 p 0.063 0.143 0.284 0.385 0.405 2021, 1/1 to 12/31 27.00 20.17 19.50 2.25 1.75 MW 89.5 88.0 72.5 93.5 36.0 p 0.325 0.368 1.000 0.090 0.711 MW Mann–Whitney non-parametric U test statistics Table 3 The number of patients All patients Stroke patients per day N N in 2019 t-stats p MW p N N in 2019 t-stats p MW p 2020-04 0.90 1.13 1.013 0.316 495.5 0.480 0.73 0.73 0.000 1.000 427.0 0.718 2020-05 1.06 0.90 0.643 0.523 437.5 0.526 0.77 0.77 0.000 1.000 499.5 0.777 2020-06 0.77 0.90 0.592 0.556 501.0 0.424 0.73 0.73 0.000 1.000 467.0 0.790 2020-07 0.55 0.94 2.249 0.029 602.0 0.059 0.42 0.65 1.447 0.154 555.5 0.232 2020-08 1.13 0.61 2.300 0.025 329.5 0.024 0.87 0.55 1.533 0.131 389.5 0.164 2020-09 0.67 0.93 1.267 0.211 507.0 0.363 0.53 0.63 0.574 0.568 478.0 0.650 2020-10 0.13 0.94 4.702 0.000 742.5 0.000 0.03 0.68 4.671 0.000 730.0 0.000 2020-11 0.93 1.17 0.903 0.370 514.0 0.324 0.63 1.07 1.793 0.078 575.0 0.048 2020-12 0.74 1.13 1.646 0.105 573.5 0.167 0.52 0.84 1.597 0.116 570.5 0.167 2021-01 0.74 0.97 0.830 0.410 566.0 0.195 0.55 0.74 0.894 0.375 557.5 0.229 2021-02 1.11 1.11 0.000 1.000 388.5 0.959 0.93 0.93 0.000 1.000 392.0 1.000 2021-03 1.23 1.03 -0.747 0.458 417.0 0.340 0.90 0.68 -1.125 0.265 375.5 0.108 2021-04 1.13 1.13 0.000 1.000 444.0 0.930 0.80 0.73 -0.325 0.747 404.0 0.468 2021-05 1.23 0.90 -1.048 0.300 445.5 0.608 0.90 0.77 -0.499 0.620 470.0 0.879 2021-06 0.93 0.90 -0.151 0.881 447.5 0.975 0.63 0.73 0.531 0.597 474.0 0.704 2021-07 0.55 0.94 1.980 0.052 610.0 0.049 0.35 0.65 1.800 0.077 591.0 0.076 2021-08 0.58 0.61 0.177 0.860 468.5 0.857 0.35 0.55 1.186 0.241 540.5 0.326 2021-09 0.67 0.93 1.153 0.254 524.0 0.241 0.63 0.63 0.000 1.000 466.5 0.793 2021-10 0.71 0.94 1.113 0.270 538.5 0.382 0.48 0.68 1.068 0.290 552.0 0.263 2021-11 1.00 1.17 0.681 0.499 495.0 0.490 0.73 1.07 1.522 0.134 535.0 0.184 2021-12 0.81 1.13 1.267 0.210 566.0 0.206 0.71 0.84 0.603 0.549 512.0 0.638 The table compares the daily average number of transported patients and patients with stroke for each month during the coronavirus disease (COVID) periods with the corresponding monthly pre-COVID data. t-stats means t statistics of two-group comparisons of means (two-sided) t-stats t statistics of two group mean comparison (two-sided), MW Mann–Whitney non-parametric U test statistics 1 3 Acta Neurologica Belgica patients dropped from 0.94 in 2019 to 0.55 in 2021 (t-sta- tistics = 1.980, p = 0.052, MW statistics = 610.0, p = 0.049), while that of patients with stroke decreased from 0.65 in 2019 to 0.35 in 2021 (t-statistics = 1.800, p = 0.077, MW statistics = 591.0, p = 0.076). Analysis 2: key process time measures We evaluated the pandemic impact on five key process time measures (Fig. 2 and Table 4). The only time measure that worsened was the door-to-CT time in 2021. In 2019, the door-to-CT time was 15.19 min with a standard deviation of 5.56 min, whereas, in 2021, it was 17.55 min with a stand- ard deviation of 12.91 min. The mean difference, 2.36 min, was statistically significant (t-statistics = − 3.030, p = 0.003, Fig. 1 Patients with stroke alerts per day. This figure shows changes MW statistics = 54,544.0, p = 0.249). However, we found no in the monthly average of the number of patients with stroke alerts significant difference in the door-to-MR imaging, door-to- per day. The solid line indicates the pandemic data. The observa- needle, and door-to-groin puncture times, suggesting that tion periods during the pandemic started in April 2020 and ended in the overall quality of acute stroke care measured with time December 2021. The dotted line represents the baseline data in 2019. The number of patients dropped sharply in October 2020 due to hos- intervals did not decrease during the pandemic. pital cluster infection Discussion Substantial drops were observed in October 2020 (Table 3 and Fig. 1). The number of patients admitted and patients The COVID-19 pandemic has threatened global and national with stroke dropped from 0.94 in 2019 to 0.13 in 2020 and healthcare systems. As the pandemic gave rise to the need from 0.68 in 2019 to 0.03 in 2020, respectively. We also for reorganization of pre- and in-hospital stroke care path- found a systematic decline in July 2021. The number of ways, one of the threats that previous studies [1, 6] reported Fig. 2 Key process time measures. The figures show the five key pro- 2021, respectively. As not all patients admitted to the facility received cess time measures of each patient in minutes. The white areas rep- the same treatment, the numbers of patients included in each of these resent the baseline data in 2019, whereas the lighter and darker grey panels are different areas indicate the pandemic data in 2020 (April to December) and 1 3 Acta Neurologica Belgica is the reduced quality of acute stroke management. Previous studies evaluated pre- and in-hospital performance indica- tors such as the number of patients admitted who presented with signs of stroke or TIA and door-to-groin puncture time. The findings in these studies are rather mixed, with some reporting detrimental impacts [28, 29], whereas others report limited impacts [26]. One potential source of such disagree- ments is the duration of the observation periods. The mean of the observation periods in 32 papers was 3.63 months with a standard deviation of 2.94 months (Table 1). Drenck et  al. [5] and Kim et  al. [12] used the longest observa- tion period data of 12 months. In this study, we used the 21-month pandemic data at a medical facility in Tokyo, Japan, evaluated the long-term pandemic impacts, and con- ducted a retrospective single-center observational study. In our first analysis, we studied the effects of the monthly average number of patients and stroke care treatments. We demonstrated a significant decline in the number of admis- sions of patients with stroke alerts in 2020. In October 2020, the daily average number of patients with stroke alerts and patients with stroke dropped by 42% and 36%, respectively. We attribute the decline in 2020 to the hospital cluster infec- tion in October 2020, which caused the facility to close emergency admission from September 30 to October 17, Another systematic decline occurred in July 2021. In addition to the surge of infections from 12,977 in June 2021 to 44,448 in July 2021 (342% increase), the region hosted the Olympic games in that month. Games during the pandemic sparked intense public debates. There is a possibility that social anxiety might raise patients’ fear of COVID-19, which might cause delays in seeking help. This finding suggests that healthcare providers and policymakers should evaluate the value of hosting large social events such as the Olympic games with a consideration of this indirect effect. Despite these significant differences, we did not observe any systematic differences in other periods between the pre-COVID and COVID periods, leading us to conclude that COVID-19 did not have any substantial impacts on the number of hospital admissions as well as that of stroke care treatments. In our analysis using daily average data, we found no initial decline even shortly after the beginning of the pandemic in April 2020. This might be due to the limited magnitude of the pandemic and the resulting low social fear of in-hospital infections in this region. The highest daily number of COVID-19 cases in metropolitan Tokyo during the observation period was 5908 (August 13, 2021), whereas that in New York State and California was 85,476 (Decem- ber 31, 2021) and 50,913 (December 31, 2021), respectively. Our interpretation based on the low social fears of in- hospital infections is in line with our findings in the sec- ond analysis (Table 4). The onset-to-door time would sig- nificantly increase if patients developed fear; however, we 1 3 Table 4 Effects on the key process time measures 2019, 1/1 to 12/31 2020, 4/1 to 12/31 2021, 1/1 to 12/31 Time interval N Mean SD N Mean SD t-test p MW p N Mean SD t-test p MW p Onset-to-Door 329 311.56 330.33 189 193.05 283.90 4.304 0.000 39,870.5 0.000 308 276.63 353.20 1.287 0.199 54,815.5 0.074 Door-to-CT 357 15.19 5.56 204 15.99 6.31 1.507 0.133 33,697.5 0.140 322 17.55 12.91 -3.030 0.003 54,544.0 0.249 Door-to-MRI 230 31.89 16.57 147 32.69 20.60 -0.397 0.691 16,592.5 0.762 234 34.11 17.39 -1.405 0.161 24,852.0 0.154 Door-to-needle 46 65.98 17.40 24 66.46 16.00 -0.116 0.908 539.5 0.882 27 72.15 36.93 -0.817 0.420 646.0 0.779 Door-to-groin puncture 17 90.00 27.39 14 103.79 26.93 -1.408 0.170 84.0 0.171 21 94.57 39.06 -0.423 0.675 177.0 0.977 SD standard deviations, t-stats t statistics of two group mean comparison (two-sided), MW Mann–Whitney non-parametric U test statistics Acta Neurologica Belgica observed that it decreased in 2020 and 2021. The decline to provide safe and timely acute stroke management during in the onset-to-door time suggests that the decrease in the the pandemic. number of patients treated with rt-PA in 2021 (Table 2) did not result from delays in the onset-to-door time. Author contributions Concept and design: MT, JT and MH. Acquisi- In the second analysis, we studied the effects of other key tion of data: MT. Analysis of data: MH. Drafting of the manuscript: process time measures. Almost all the measures remained MT and MH. Critical revision of the manuscript for important intel- constant throughout the study period, suggesting that the lectual content: JT. Obtained funding: MH, MT, and JT. facility managed to avoid any hazardous delays in in-hospital stroke care that COVID-19 could cause. We did not find sub- Funding This work was supported by JSPS KAKENHI (Grant Num- bers 18K18584 and 21K18443). stantial increases in the onset-to-door, door-to-MR imaging, door-to-needle, or door-to-groin puncture times. Our results Data availability The data used in this study are available from the are consistent with other studies that did not report such a corresponding author upon reasonable request. delay [15, 22]. However, we observed significant delays in the door-to-CT time in 2021, which is plausibly due to the Declarations facility’s optimization of the stroke care pathways after hos- pital cluster infection in October 2021. The renewed proto- Conflict of interest The authors declare that they have no competing cols enhanced the protection of frontline healthcare workers interests. against infections but could have increased the mean door- Ethical approval This study was conducted retrospectively using data to-CT time in 2021. obtained for clinical purposes. Approval was obtained from the ethics An implication of our study is the importance of prevent- committee of Waseda University (2020-382) and Juntendo University ing hospital cluster infections. The cluster infection not only Nerima Hospital (2018-43). reduced the number of admissions but also required addi- Consent for publication Not applicable. tional reorganization in stroke care pathways. As a result of the hospital cluster infection, the facility made responsive Open Access This article is licensed under a Creative Commons Attri- and reactive actions, requiring longer adaptations and learn- bution 4.0 International License, which permits use, sharing, adapta- ing than preventive actions. The pandemic impacts could be tion, distribution and reproduction in any medium or format, as long reduced further if medical facilities take preemptive rather as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes than remedial actions. Healthcare providers and policymak- were made. The images or other third party material in this article are ers should encourage medical facilities to allocate more included in the article's Creative Commons licence, unless indicated resources to prevent hospital cluster infections. otherwise in a credit line to the material. If material is not included in Our study had several limitations. First, this study was the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will based on data collected from a single medical facility in a need to obtain permission directly from the copyright holder. To view a specific area. Further research using long-term data from copy of this licence, visit http://cr eativ ecommons. or g/licen ses/ b y/4.0/ . other countries and regions is needed to enhance generaliz- ability. Second, although the number of stroke admissions and the time metrics are important to assess the pandemic effects, this study did not examine the quality of treatment References received by patients and their overall health and welfare. The 1. Agarwal S, Scher E, Rossan-Raghunath N, Marolia D, Butnar M, goal of acute stroke management is to decrease morbidity Torres J, Zhang C, Kim S, Sanger M, Humbert K, Tanweer O, and mortality [8, 9]. 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Journal

Acta Neurologica BelgicaSpringer Journals

Published: Apr 1, 2023

Keywords: COVID-19; Pandemic impacts; Stroke care pathways; Admissions; Time measures

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