Literature DB >> 35753763

Impact of COVID-19 on the Volume of Acute Stroke Admissions: A Nationwide Survey in Japan.

Takeshi Yoshimoto1, Hiroshi Yamagami2, Nobuyuki Sakai3, Kazunori Toyoda4, Yoichiro Hashimoto5, Teruyuki Hirano6, Toru Iwama7, Rei Goto8, Kazumi Kimura9, Satoshi Kuroda10, Yuji Matsumaru11, Susumu Miyamoto12, Kuniaki Ogasawara13, Yasushi Okada14, Yoshiaki Shiokawa15, Yasushi Takagi16, Teiji Tominaga17, Masaaki Uno18, Shinichi Yoshimura19, Nobuyuki Ohara20, Hirotoshi Imamura3, Chiaki Sakai3.   

Abstract

This study aimed to measure the impact of the COVID-19 pandemic on the volumes of annual stroke admissions compared with those before the pandemic in Japan. We conducted an observational, retrospective nationwide survey across 542 primary stroke centers in Japan. The annual admission volumes for acute stroke within 7 days from onset between 2019 as the pre-pandemic period and 2020 as the pandemic period were compared as a whole and separately by months during which the epidemic was serious and prefectures of high numbers of infected persons. The number of stroke patients declined from 182,660 in 2019 to 178,083 in 2020, with a reduction rate of 2.51% (95% confidence interval [CI], 2.58%-2.44%). The reduction rates were 1.92% (95% CI, 1.85%-2.00%; 127,979-125,522) for ischemic stroke, 3.88% (95% CI, 3.70%-4.07%, 41,906-40,278) for intracerebral hemorrhage, and 4.58% (95% CI, 4.23%-4.95%; 13,020-12,424) for subarachnoid hemorrhage. The admission volume declined by 5.60% (95% CI, 5.46%-5.74%) during the 7 months of 2020 when the epidemic was serious, whereas it increased in the remaining 5 months (2.01%; 95% CI, 1.91%-2.11%). The annual decline in the admission volume was predominant in the five prefectures with the largest numbers of infected people per million population (4.72%; 95% CI, 4.53%-4.92%). In conclusion, the acute stroke admission volume declined by 2.51% in 2020 relative to 2019 in Japan, especially during the months of high infection, and in highly infected prefectures. Overwhelmed healthcare systems and infection control practices may have been associated with the decline in the stroke admission volume during the COVID-19 pandemic.

Entities:  

Keywords:  Japan; admission; coronavirus disease-2019; nationwide survey; stroke

Mesh:

Year:  2022        PMID: 35753763      PMCID: PMC9464481          DOI: 10.2176/jns-nmc.2022-0099

Source DB:  PubMed          Journal:  Neurol Med Chir (Tokyo)        ISSN: 0470-8105            Impact factor:   2.036


Introduction

On March 11, 2020, the World Health Organization declared coronavirus disease-2019 (COVID-19) a pandemic,[1],[2]) which triggered an increase in emergency medical system activation. COVID-19 variants are still rampant worldwide,[3]) and the pandemic has induced profound changes in healthcare system organization.[4],[5]) In Japan, the first COVID-19 infected patient was found on January 16, 2020, and 1727013 people were infected with COVID-19 in the two years up to 2021. Despite geographic variations, COVID-19 has been associated with a global decline[6]) in the volume of overall stroke admissions-from comprehensive stroke centers in highly resourced countries[7],[8]) to primary stroke centers (PSCs) without endovascular capability in low- or middle-income countries.[9],[10]) The reasons for such a decline are unclear. There is little information about the worldwide changes in stroke admissions during the pandemic and pre-pandemic periods obtained using an annual survey involving a large population. The present study aimed to measure the impact of COVID-19 on stroke care assessed by the changes in annual admission volumes to stroke centers for overall stroke and each stroke type across the pre-pandemic (2019) and pandemic periods (2020) in Japan.

Materials and Methods

Our data are available upon request to the corresponding author. The present study conforms to the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) guidelines.[11]) A completed STROBE checklist is included in the Data Supplement.

Study design

Between January 2019 and December 2020, we conducted a cross-sectional, observational, retrospective survey across Japan on the monthly volumes of consecutive patients admitted to PSCs certified by the Japan Stroke Society within 7 days of ischemic stroke (IS), intracerebral hemorrhage, or subarachnoid hemorrhage onset. The certified centers in Japan include both PSCs and comprehensive stroke centers. A physician or stroke coordinator verified the cases.

Setting, participants, variables, and outcome measures

The Japan Stroke Society conducted the present survey regarding the admission volume for acute stroke. The questionnaire was sent via e-mail to 974 PSCs in Japan (Figure S1). The responses were sent to the Japan Stroke Society, which provided a complete dataset for the 2-year period, including any associated analyses. The survey protocol conformed to the Declaration of Helsinki. The institutional review boards from the coordinating sites (Kobe City Medical Center General Hospital and National Hospital Organization Osaka National Hospital) considered that the investigators did not have access to identifiable protected health information, and thus, no informed consent or institutional review board oversight was required because the study did not meet the Japanese Ethical Guidelines for Medical and Biological Research Involving Human Subjects. The monthly volumes of admissions for overall stroke and its subtypes were compared between the pre-pandemic (January-December 2019) and pandemic periods (January-December 2020).

Statistical analyses

As a primary analysis, we compared the annual numbers of hospitalized stroke patients (any stroke, IS, intracerebral hemorrhage, or subarachnoid hemorrhage) between 2019 and 2020. We calculated the percentage change in patient numbers between the two periods and their 95% confidence intervals (CIs) using the Wilson method without continuity correction.[12]) Subsequently, we repeated the analyses by dividing the 12 months of 2020 into two-time groups according to the pandemic severity as a secondary analysis. In Japan, there were three waves of COVID-19 in 2020: March-May, July-August, and November-December. We defined those 7 months as the spreading months (Fig. 1) and January-February, June, and September-October as the non-spreading months.
Fig. 1

Monthly volume of stroke admissions and cumulative number of COVID-19 patients in 542 Japanese PSCs during the study period.

(A) Monthly volume of stroke admissions and cumulative number of COVID-19 patients per month in Japan. (B) Difference in stroke admissions between 2019 and 2020.

A state of emergency was declared on April 7, 2020, and was lifted on May 25, 2020. Based on openly available data from the Ministry of Health, Labour and Welfare, Japan.

Monthly volume of stroke admissions and cumulative number of COVID-19 patients in 542 Japanese PSCs during the study period. (A) Monthly volume of stroke admissions and cumulative number of COVID-19 patients per month in Japan. (B) Difference in stroke admissions between 2019 and 2020. A state of emergency was declared on April 7, 2020, and was lifted on May 25, 2020. Based on openly available data from the Ministry of Health, Labour and Welfare, Japan. Furthermore, as a third analysis, according to the cumulative infection rate in 2020, we repeated the analyses by dividing Japan's 47 prefectures into highly infected prefectures and other prefectures. We defined highly infected prefectures as the top five with the highest cumulative number of infected people per million population as of December 31, 2020.[13]) Furthermore, we expressed the relative changes in admissions for all types of stroke or its subtype (IS, intracerebral hemorrhage, and subarachnoid hemorrhage) as an incidence rate ratio (IRR) along with its two-sided 95% CI: IRR = incidence rate 2020/incidence rate 2019 (where the incidence rate 2020 = number of event admissions in the spreading months in 2020/number of event admissions in the non-spreading months of 2020, and where the incidence rate 2019 = number of event admissions in the spreading months of 2019/number of event admissions in the non-spreading months of 2019). Then, we calculated the IRR using mixed Poisson regression[14]) to test whether the rate of events changed by year (2019 or 2020), spreading status (spreading or non-spreading months), and interaction of year and spreading status (reflecting the impact of COVID-19) (model 1). Finally, we repeated our analyses separately by trisected groups of PSCs (low-, intermediate-, and high-volume PSCs) according to the annual number of stroke admissions in 2019, depending on the number of stroke admissions in the same year for each PSC. We evaluated the descriptive statistics for differences in the measures between the pandemic and pre-pandemic periods in all analyses other than the percentage changes using the Wilcoxon signed-rank test. The percentage changes in the overall stroke and its subtype admission volume were tested using the two-proportion Z-test. All studies were conducted using StataMP 17 (StataCorp LLC, College Station, TX), and significance was tested at P < 0.05 for the two-tailed tests.

Results

Of the 974 PSCs, 576 responded; of those, 34 were excluded due to incomplete data. Thus, we analyzed the data from the remaining 542 PSCs (55.6%).

Overall analysis

The annual volumes of stroke admissions were 182,660 in 2019 and 178,083 in 2020-indicating a decline of 2.51% (95% CI, 2.44%-2.58%, P < 0.0001, Fig. 1). Of the 542 PSCs, 235 (43.4%) had more stroke admissions in 2020 than in 2019. The monthly volumes for admissions according to stroke type are presented in Figure S2. The admission volume for IS decreased from 127,979 in 2019 to 125,522 in 2020; the adjusted mean (standard error) monthly number of IS patients per center declined from 19.68 ± 0.53 to 19.30 ± 0.53 (P = 0.0054), which correspond to a 1.92% (95% CI, 1.85%-2.00%, P = 0.0025) reduction (Table 1). The admission volume for intracerebral hemorrhage decreased from 41,906 to 40,278 (6.44 ± 0.18 to 6.20 ± 0.17 monthly per center, P = 0.0003), which correspond to a 3.88% (95% CI, 3.70%-4.07%, P < 0.0001) decline. The admission volume for subarachnoid hemorrhage decreased from 13,020 to 12,424 (2.00 ± 0.07 to 1.91 ± 0.06 monthly per center, P = 0.0086), which correspond to a 4.58% (95% CI, 4.23%-4.95%, P < 0.0001) decline.
Table 1

Annual and monthly volume of acute stroke during the pre-pandemic (2019) and pandemic (2020) periods

Annual volumeMonthly volumes per stroke center
N20192020Percent change (95% CI), % 2019, mean ± SE 2020, mean ± SE P value*
All stroke542182,660178,083–2.51 (–2.58 to –2.44)28.08 ± 0.7127.38 ± 0.69<0.0001
Stroke type
Ischemic stroke542127,979125,522–1.92 (–2.00 to –1.85)19.68 ± 0.5319.30 ± 0.530.0054
Intracerebral hemorrhage54241,90640,278–3.88 (–4.07 to –3.70)6.44 ± 0.186.20 ± 0.170.0003
Subarachnoid hemorrhage54213,02012,424–4.58 (–4.95 to –4.23)2.00 ± 0.071.91 ± 0.060.0086

Abbreviations: CI, confidence interval; N, number of hospitals; SE, standard error.

* P-value with reference to monthly volume per primary stroke center in 2019 using the Wilcoxon signed-rank test.

Annual and monthly volume of acute stroke during the pre-pandemic (2019) and pandemic (2020) periods Abbreviations: CI, confidence interval; N, number of hospitals; SE, standard error. * P-value with reference to monthly volume per primary stroke center in 2019 using the Wilcoxon signed-rank test.

Subgroup analyses

The number of stroke admissions decreased by 5.60% (95% CI, 5.46%-5.74%) during the spreading months in 2020 compared with that during the same months in 2019; however, it increased by 2.01% (95% CI, 1.91%-2.11%) in the non-spreading months (P < 0.0001, Table 2). These results were similar for IS and subarachnoid hemorrhage.
Table 2

Comparison of acute stroke admission volumes between the spreading and non-spreading months during the pre-pandemic (2019) and pandemic (2020) periods

Annual volume*Monthly volumes per stroke center*
20192020Change (95% CI), %2019, mean ± SE 2020, mean ± SE Change (95% CI), %
All stroke
Spreading months108,409102,339–5.60 (–5.74 to –5.46)16.67 ± 0.4215.73 ± 0.40–4.27 (–6.00 to –2.54)
Non-spreading months74,25175,7442.01 (1.91 to 2.11)11.42 ± 0.4911.65 ± 0.304.69 (2.43 to 6.95)
Ischemic stroke
Spreading months76,01572,103–5.15 (–5.31 to –4.99)11.71 ± 0.3211.15 ± 0.30–3.05 (–5.04 to –1.07)
Non-spreading months51,77453,3743.09 (2.94 to 3.24)7.98 ± 0.228.24 ± 0.236.69 (4.19 to 9.19)
Intracerebral hemorrhage
Spreading months24,58023,226–5.51 (–5.80 to –5.23)3.79 ± 0.113.58 ± 0.10–0.82 (–3.78 to 2.13)
Non-spreading months17,23517,118–0.68 (–0.57 to –0.81)2.65 ± 0.072.64 ± 0.079.24 (3.74 to 14.76)
Subarachnoid hemorrhage
Spreading months15,49414,097–9.02 (–9.48 to –8.58)2.38 ± 1.192.18 ± 1.098.02 (0.54 to 15.49)
Non-spreading months10,54610,7321.76 (1.53 to 2.03)1.62 ± 0.811.65 ± 0.8322.78 (14.80 to 30.76)

The spreading months were Mar.–May, July.–Aug., Nov.–Dec. 2020, and the non-spreading months were Jan.–Feb., June, Sept.–Oct. 2020. Each month was compared with the same month of the previous year (2019).

Abbreviations: CI, confidence interval; SE, standard error.

* P < 0.0001 between the spreading and non-spreading months for any events using the z-test or Wilcoxon signed-rank test.

Comparison of acute stroke admission volumes between the spreading and non-spreading months during the pre-pandemic (2019) and pandemic (2020) periods The spreading months were Mar.–May, July.–Aug., Nov.–Dec. 2020, and the non-spreading months were Jan.–Feb., June, Sept.–Oct. 2020. Each month was compared with the same month of the previous year (2019). Abbreviations: CI, confidence interval; SE, standard error. * P < 0.0001 between the spreading and non-spreading months for any events using the z-test or Wilcoxon signed-rank test. Among the 47 prefectures in Japan, Tokyo, Okinawa, Osaka, Hokkaido, and Kanagawa had the highest cumulative number of infected people per 1 million population (Figure S3). We considered these as the five highly infected prefectures, and the cumulative number of infected people per 1 million population exceeded 2,300. The number of stroke admissions decreased by 4.72% (95% CI, 4.53%-4.92%) between 2019 and 2020 in these prefectures and by 1.75% (95% CI, 1.68%-1.82%) in the other 42 prefectures (P < 0.0001, Table 3). These results were similar for each stroke type. The IRR (95% CI) of stroke admissions using mixed Poisson regression was 0.9899 (0.9977-0.9998), and similar analysis revealed a significant decrease in the number of stroke admission in the highly infected prefectures (IRR, 0.9987; 95% CI, 0.9974-0.9998). The IRR for stroke and each stroke subtype admissions between highly infected prefectures and other prefectures is presented in Table S1.
Table 3

Comparison of stroke admission volumes between highly infected and other prefectures during the pre-pandemic (2019) and pandemic (2020) periods

Annual volume *Monthly volumes per stroke center **
20192020Change (95% CI), %2019, mean ± SE 2020, mean ± SE Change (95% CI), %
Stroke
Highly infected prefectures46,34844,161–4.72 (–4.92 to –4.53)30.17 ± 1.5228.75 ± 1.44–4.83 (–7.56 to –2.10)
Other prefectures136,312133,922–1.75 (–1.82 to –1.68)27.44 ± 0.8026.96 ± 0.79–0.09 (–2.00 to 1.83)
Ischemic stroke
Highly infected prefectures32,03930,574–4.57 (–4.81 to –4.35)20.86 ± 1.1419.90 ± 1.10–4.28 (–7.22 to –1.35)
Other prefectures95,94094,948–1.03 (–1.10 to –0.97)19.31 ± 0.6019.11 ± 0.601.03 (–1.18 to 3.23)
Intracerebral hemorrhage
Highly infected prefectures11,18910,632–4.98 (–5.40 to –4.58)7.28 ± 0.386.92 ± 0.352.00 (–6.97 to 10.97)
Other prefectures30,71729,646–3.49 (–3.70 to –3.29)6.18 ± 0.205.98 ± 0.193.01 (–6.97 to 10.97)
Subarachnoid hemorrhage
Highly infected prefectures3,2743,096–5.44 (–6.27 to –4.71)2.13 ± 0.142.02 ± 0.130.41 (–7.66 to 8.58)
Other prefectures9,7469,328–4.29 (–4.71 to –3.90)1.96 ± 0.081.88 ± 0.0710.05 (1.83 to 18.28)

Abbreviations: CI, confidence interval; SE, standard error.

* P < 0.0001 between the highly infected and other prefectures for any events using the z-test.

** P < 0.0001 between the highly infected and other prefectures for any events using the Wilcoxon signed-rank test.

Comparison of stroke admission volumes between highly infected and other prefectures during the pre-pandemic (2019) and pandemic (2020) periods Abbreviations: CI, confidence interval; SE, standard error. * P < 0.0001 between the highly infected and other prefectures for any events using the z-test. ** P < 0.0001 between the highly infected and other prefectures for any events using the Wilcoxon signed-rank test. The tertiles of the stroke admission volumes in each PSC were 231 and 380 in 2019. High-volume PSCs with ≥380 stroke admissions in 2019 indicated a significant decline in stroke admissions in 2020 (3.21%; 95% CI, 3.10%-3.22%, P = 0.0001), whereas the intermediate-volume PSCs (1.51%; 95% CI, 1.41%-1.62%; P = 0.1399) and low-volume PSCs did not exhibit a significant decline in acute stroke admission volume in 2020 (1.87%; 95% CI, 1.72%-2.04%, P = 0.0785, Table 4). The annual and monthly volumes of stroke admissions by different scales of stroke centers during the pre-pandemic (2019) and pandemic (2020) periods are presented in Table 4.
Table 4

Annual and monthly volume of stroke admissions by different scales of primary stroke centers during the pre-pandemic (2019) and pandemic (2020) periods

Annual admission volumesMonthly volumes per center
N20192020Percent change (95% CI), %2019, mean ± SE 2020, mean ± SE P-value *
All stroke **
Low-volume PSCs18028,07927,554–1.87 (–2.04 to –1.72)13.11 ± 0.3412.85 ± 0.350.0771
Intermediate-volume PSCs18253,73552,922–1.51 (–1.62 to –1.41)24.84 ± 0.2724.44 ± 0.360.1360
High-volume PSCs180100,84697,607–3.21 (–3.10 to –3.22)46.34 ± 1.1044.89 ± 1.080.0001
Stroke subtype
Ischemic stroke ***
Low-volume PSCs18018,92318,9510.15 (0.10 to 0.21)8.76 ± 0.258.78 ± 0.270.9696
Intermediate-volume PSCs18237,18836,442–2.01 (–2.15 to –1.88)17.03 ± 0.1916.68 ± 0.290.1526
High-volume PSCs18071,86870,129–2.42 (–2.53 to –2.31)33.27 ± 0.8532.47 ± 0.850.0025
Intracerebral hemorrhage****
Low-volume PSCs1805,4105,565–2.87 (–3.35 to –2.45)2.50 ± 0.082.58 ± 0.090.2091
Intermediate-volume PSCs18212,57912,192–3.08 (–3.39 to –2.79)5.76 ± 0.085.59 ± 0.120.1097
High-volume PSCs18023,91722,521–5.84 (–6.14 to –5.55)11.07 ± 0.2610.48 ± 0.25<0.0001
Subarachnoid hemorrhage *****
Low-volume PSCs1801,3401,63622.09 (19.95 to 24.39)0.62 ± 0.020.76 ± 0.040.0002
Intermediate-volume PSCs1823,4993,361–3.94 (–4.64 to –3.35)1.60 ± 0.021.54 ± 0.050.0580
High-volume PSCs1808,1817,427–9.22 (–9.86 to –8.61)3.79 ± 0.113.44 ± 0.11<0.0001

Abbreviations: CI, confidence interval; N, number of hospitals; PSC, primary stroke center; SE, standard error.

High-, intermediate-, and low-volume PSCs were categorized according to the number of hospitalizations for each stroke center in 2019.

* P-value with reference to monthly volumes per PSC in 2019 using Wilcoxon’s signed-rank test.

** Low vs. intermediate, P = 0.7917; low vs. high, P = 0.2570; intermediate vs. high, P = 0.1456.

*** Low vs. intermediate, P = 0.1679; low vs. high, P = 0.0030; intermediate vs. high, P = 0.3799.

**** Low vs. intermediate, P = 0.0073; low vs. high, P < 0.0001; intermediate vs. high, P = 0.0954.

***** Low vs. intermediate, P < 0.0001; low vs. high, P < 0.0001; intermediate vs. high, P = 0.1473.

Annual and monthly volume of stroke admissions by different scales of primary stroke centers during the pre-pandemic (2019) and pandemic (2020) periods Abbreviations: CI, confidence interval; N, number of hospitals; PSC, primary stroke center; SE, standard error. High-, intermediate-, and low-volume PSCs were categorized according to the number of hospitalizations for each stroke center in 2019. * P-value with reference to monthly volumes per PSC in 2019 using Wilcoxon’s signed-rank test. ** Low vs. intermediate, P = 0.7917; low vs. high, P = 0.2570; intermediate vs. high, P = 0.1456. *** Low vs. intermediate, P = 0.1679; low vs. high, P = 0.0030; intermediate vs. high, P = 0.3799. **** Low vs. intermediate, P = 0.0073; low vs. high, P < 0.0001; intermediate vs. high, P = 0.0954. ***** Low vs. intermediate, P < 0.0001; low vs. high, P < 0.0001; intermediate vs. high, P = 0.1473.

Discussion

This was a temporal analysis of ≈180,000 annual stroke admissions in Japan. The major finding was that there was a global decrease in stroke admissions by 2.51% in 2020, the pandemic period, compared with 2019, the pre-pandemic period. A drop in stroke admission volume was also seen concerning the equivalent period in the prior year for all stroke subtypes. Notably, the number of stroke admissions declined during the spreading months in 2020 but increased in the remaining months. The number of stroke admissions in the five prefectures with relatively severe pandemic significantly declined over the same period. To reduce the bias in the change in the number of stroke admissions annually with or without the impact of COVID-19, the IRR verification also confirmed a decrease in stroke admission in the pandemic period-especially in those five prefectures. Furthermore, the declines in stroke admissions were predominant among high-volume stroke centers. Several infections have long been recognized to increase the risk of stroke, and stroke was also found to induce immune suppression, which increases the risk of infection.[15]) Initial reports from Wuhan, China, revealed a high risk of stroke among COVID-19-infected patients, with a frequency of ≈5%, especially those with severe infection.[16],[17]) Contrarily, consistent declines in the absolute volumes of IS admissions due to COVID-19 have been reported; however, the magnitude of the reduction varied according to the severity of the pandemic in the studied countries and the observation period. Studies involving a few months of observation in early 2020 observed reductions in visits or consultations among patients with acute IS by 30%-40%.[18-20]) One study with a longer observation period found recovery of stroke volumes in the second quarter of 2020 following an initial steep decline.[21]) Thus, the decrease in the initial volume did not seem to have been caused by decreased stroke incidence. In this study, we observed that in 2020, the number of stroke admissions decreased during the 7 months when the epidemic was relatively serious. Behavioral modifications against the spread of COVID-19 by the general population appeared to have both decreased and increased the risk of stroke. Stroke patients-especially those with mild neurological deficits-may have avoided visiting healthcare facilities because of concerns about infection risk.[22-26]) Going outside less often may have offered protection against the cold in winter, which could have decreased the risk of hemorrhagic stroke; in summer, staying indoors more often could have provided protection from dehydration, thereby decreasing the risk of thrombotic IS. Conversely, staying inside more often could have reduced physical exercise opportunities and also led to noncompliance with medication owing to reduced regular medical checkups, thereby increasing the risk of stroke.[27],[28]) Estimates of changes in the volume of IS and its subtypes were reported to have been affected by hospital characteristics and cohort case-mix.[29]) In this regard, COVID-19 appears to have had a greater effect in larger cohorts that included a greater proportion of high-volume PSCs than in smaller cohorts with intermediate- and low-volume PSCs;[21],[30-35]) these findings are supported by the results of the present study. Most high-volume PSCs were core hospitals in a city and needed to devote considerable care for COVID-19 patients; thus, the capacity for stroke care may have decreased in such institutions. Conversely, intermediate- and low-volume PSCs may have contributed more to stroke care. As a result, the number of stroke admissions in 2020 might have increased in 47% of the PSCs compared with that in 2019. About 47% of the PSCs were found to have increased stroke admissions in 2020. The influence was also clearly observed in the metropolitan areas, such as the Tokyo, Osaka, and Kanagawa prefectures and the prefectures with regiments of tourists, such as Okinawa and Hokkaido. In these prefectures, the medical staffs and sources originally for stroke care might be partly exploited for COVID-19 patients. The strength of this study was the participation of geographically evenly distributed 542 PSCs, which are more than half the certified PSCs in Japan. Furthermore, 180,000 patients were investigated annually, which was about 75% of the annual number of acute stroke patients in Japan. To the best of our knowledge, this is currently the most extensive nationwide survey evaluating the impact of the COVID-19 pandemic on stroke care. This study has several limitations. First, 44.4% of Japan's PSCs did not respond to the survey or submitted incomplete data. Second, data on stroke patients who visited hospitals and clinics other than the certified PSCs (probably mainly because of mild stroke severity) were unavailable. Third, we did not obtain detailed individual data, such as stroke severity, therapy, and functional outcome. Fourth, the spreading months of COVID-19 varied among the prefectures.

Conclusion

The volume of acute stroke admissions declined in 2020 relative to 2019 in certified primary stroke centers (PSCs) in Japan, especially in high-volume centers, during the COVID-19 spreading months, and in highly infected prefectures. Overwhelmed healthcare systems and infection control practices may have been associated with the reduced number of acute stroke patients during the COVID-19 pandemic.

Sources of Funding

This research was funded by the Health Labor Sciences Research Grant (20FA1201) of the Ministry of Health, Labour and Welfare Japan and endorsed by the Japan Stroke Society.

Conflicts of Interest Disclosure

All the following conflicts relate to this study. Yoshimoto. T is supported by lecture fees from Takeda Pharmaceutical and Nippon Boehringer Ingelheim. Yamagami. H is supported by research grants from Bristol-Myers Squibb and lecture fees from Stryker, Terumo, Medtronic, Medico's Hirata, Johnson & Johnson, Bayer Yakuhin, Daiichi-Sankyo, Bristol-Myers Squibb, Nippon Boehringer Ingelheim, and Otsuka Pharmaceutical. Sakai. N is supported by the following: a research grant from Biomedical Solutions, NeuroVasc, and Terumo; lecturer's fees from Asahi-Intec, Biomedical Solutions, Medtronic, and Terumo; and membership on the advisory boards for Johnson & Johnson, Medtronic, and Terumo unrelated to this manuscript. Toyoda. K is supported by lecture fees from Daiichi Sankyo, Otsuka Pharmaceutical, Novartis Japan, Abbott Medical, Bayer Yakuhin, and Bristol-Myers Squibb. Hashimoto. Y, is supported by lecture fees from Daiichi Sankyo, Pfizer Japan, Bayer Yakuhin, and Otsuka Pharmaceutical. Hirano. T is supported by lecturer's fee from Bayer Yakuhin, Nippon Boehringer Ingelheim, Daiichi-Sankyo, and Pfizer. Iwama. T is supported by a research grant from Ohgaki Tokusyukai Hospital. Goto. R, none. Kimura. K is supported by lecture fees from Bristol-Myers Squibb, Nippon Boehringer Ingelheim, Bayer Yakuhin, and Daiichi Sankyo as well as by research funding from Nippon Boehringer Ingelheim, Daiichi Sankyo, Pfizer Japan, Medtronic, and Teijin Pharma. Kuroda. S, none. Matsumaru. Y is supported by lecturer fees from Medtronic, Stryker, Terumo, Kaneka, E.P. Medical, Daiichi Sakyo, Takeda Pharmaceutical, and Bayer Yakuhin. Miyamoto. S is supported by the following: a research grant from Chugai Pharmaceutical and Philips Japan. Ogasawara. K, none. Okada. Y is supported by lecture fees from Bayer Yakuhin. Shiokawa. Y is supported by Daiichi Sankyo and lecturer's fees from Ohtsuka Pharmaceutical. Takagi. Y, none. Tominaga. T, none. Uno. M, none. Yoshimura. S is supported by lecturer's fees from Medtronic, Johnson & Johnson, Terumo, Bristol-Myers Squibb, Otsuka Pharmaceutical, Boehringer Ingelheim, Daiichi Sankyo, Bayer Yakuhin, Sanofi, Biomedical Solutions, Kaneka Medics, and Stryker. Ohara. T, none. Imamura. H is supported by lecturer's fees from Asahi-Intec, Johnson & Johnson, Medtronic, Stryker, and Terumo. Sakai. C, none. All authors who are members of the Japan Neurosurgical Society have registered online self-reported conflict of interest. Click here for additional data file.
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4.  Acute Stroke in Times of the COVID-19 Pandemic: A Multicenter Study.

Authors:  Carolin Hoyer; Anne Ebert; Hagen B Huttner; Volker Puetz; Bernd Kallmünzer; Kristian Barlinn; Christian Haverkamp; Andreas Harloff; Jochen Brich; Michael Platten; Kristina Szabo
Journal:  Stroke       Date:  2020-06-09       Impact factor: 7.914

5.  Interactive Web-based Graphs of Coronavirus Disease 2019 Cases and Deaths per Population by Country.

Authors:  Masashi Idogawa; Shoichiro Tange; Hiroshi Nakase; Takashi Tokino
Journal:  Clin Infect Dis       Date:  2020-07-28       Impact factor: 9.079

Review 6.  Infection as a Stroke Risk Factor and Determinant of Outcome After Stroke.

Authors:  Mitchell S V Elkind; Amelia K Boehme; Craig J Smith; Andreas Meisel; Marion S Buckwalter
Journal:  Stroke       Date:  2020-09-08       Impact factor: 7.914

7.  Global impact of COVID-19 on stroke care.

Authors:  Raul G Nogueira; Mohamad Abdalkader; Muhammed M Qureshi; Michael R Frankel; Ossama Yassin Mansour; Hiroshi Yamagami; Zhongming Qiu; Mehdi Farhoudi; James E Siegler; Shadi Yaghi; Eytan Raz; Nobuyuki Sakai; Nobuyuki Ohara; Michel Piotin; Laura Mechtouff; Omer Eker; Vanessa Chalumeau; Timothy J Kleinig; Raoul Pop; Jianmin Liu; Hugh S Winters; Xianjin Shang; Alejandro Rodriguez Vasquez; Jordi Blasco; Juan F Arenillas; Mario Martinez-Galdamez; Alex Brehm; Marios-Nikos Psychogios; Pedro Lylyk; Diogo C Haussen; Alhamza R Al-Bayati; Mahmoud H Mohammaden; Luísa Fonseca; M Luís Silva; Francisco Montalverne; Leonardo Renieri; Salvatore Mangiafico; Urs Fischer; Jan Gralla; Donald Frei; Chandril Chugh; Brijesh P Mehta; Simon Nagel; Markus Mohlenbruch; Santiago Ortega-Gutierrez; Mudassir Farooqui; Ameer E Hassan; Allan Taylor; Bertrand Lapergue; Arturo Consoli; Bruce Cv Campbell; Malveeka Sharma; Melanie Walker; Noel Van Horn; Jens Fiehler; Huy Thang Nguyen; Quoc T Nguyen; Daisuke Watanabe; Hao Zhang; Huynh V Le; Viet Q Nguyen; Ruchir Shah; Thomas Devlin; Priyank Khandelwal; Italo Linfante; Wazim Izzath; Pablo M Lavados; Veronica V Olavarría; Gisele Sampaio Silva; Anna Verena de Carvalho Sousa; Jawad Kirmani; Martin Bendszus; Tatsuo Amano; Ryoo Yamamoto; Ryosuke Doijiri; Naoki Tokuda; Takehiro Yamada; Tadashi Terasaki; Yukako Yazawa; Jane G Morris; Emma Griffin; John Thornton; Pascale Lavoie; Charles Matouk; Michael D Hill; Andrew M Demchuk; Monika Killer-Oberpfalzer; Fadi Nahab; Dorothea Altschul; Anna Ramos-Pachón; Natalia Pérez de la Ossa; Raghid Kikano; William Boisseau; Gregory Walker; Steve M Cordina; Ajit Puri; Anna Luisa Kuhn; Dheeraj Gandhi; Pankajavalli Ramakrishnan; Roberta Novakovic-White; Alex Chebl; Odysseas Kargiotis; Alexandra Czap; Alicia Zha; Hesham E Masoud; Carlos Lopez; David Ozretic; Fawaz Al-Mufti; Wenjie Zie; Zhenhui Duan; Zhengzhou Yuan; Wenguo Huang; Yonggang Hao; Jun Luo; Vladimir Kalousek; Romain Bourcier; Romain Guile; Steven Hetts; Hosam M Al-Jehani; Adel AlHazzani; Elyar Sadeghi-Hokmabadi; Mohamed Teleb; Jeremy Payne; Jin Soo Lee; Ji Man Hong; Sung-Il Sohn; Yang-Ha Hwang; Dong Hoon Shin; Hong Gee Roh; Randy Edgell; Rakesh Khatri; Ainsley Smith; Amer Malik; David Liebeskind; Nabeel Herial; Pascal Jabbour; Pedro Magalhaes; Atilla Ozcan Ozdemir; Ozlem Aykac; Takeshi Uwatoko; Tomohisa Dembo; Hisao Shimizu; Yuri Sugiura; Fumio Miyashita; Hiroki Fukuda; Kosuke Miyake; Junsuke Shimbo; Yusuke Sugimura; Andre Beer-Furlan; Krishna Joshi; Luciana Catanese; Daniel Giansante Abud; Octavio Giansante Neto; Masoud Mehrpour; Amal Al Hashmi; Mahar Saqqur; Abdulrahman Mostafa; Johanna T Fifi; Syed Hussain; Seby John; Rishi Gupta; Rotem Sivan-Hoffmann; Anna Reznik; Achmad Fidaus Sani; Serdar Geyik; Eşref Akıl; Anchalee Churojana; Abdoreza Ghoreishi; Mohammad Saadatnia; Ehsan Sharifipour; Alice Ma; Ken Faulder; Teddy Wu; Lester Leung; Adel Malek; Barbara Voetsch; Ajay Wakhloo; Rodrigo Rivera; Danny Moises Barrientos Iman; Aleksandra Pikula; Vasileios-Arsenios Lioutas; Gotz Thomalla; Lee Birnbaum; Paolo Machi; Gianmarco Bernava; Mollie McDermott; Dawn Kleindorfer; Ken Wong; Mary S Patterson; Jose Antonio Fiorot; Vikram Huded; William Mack; Matthew Tenser; Clifford Eskey; Sumeet Multani; Michael Kelly; Vallabh Janardhan; Oriana Cornett; Varsha Singh; Yuichi Murayama; Maxim Mokin; Pengfei Yang; Xiaoxi Zhang; Congguo Yin; Hongxing Han; Ya Peng; Wenhuo Chen; Roberto Crosa; Michel Eli Frudit; Jeyaraj D Pandian; Anirudh Kulkarni; Yoshiki Yagita; Yohei Takenobu; Yuji Matsumaru; Satoshi Yamada; Ryuhei Kono; Takuya Kanamaru; Hidekazu Yamazaki; Manabu Sakaguchi; Kenichi Todo; Nobuaki Yamamoto; Kazutaka Sonoda; Tomoko Yoshida; Hiroyuki Hashimoto; Ichiro Nakahara; Elena Cora; David Volders; Celina Ducroux; Ashkan Shoamanesh; Johanna Ospel; Artem Kaliaev; Saima Ahmed; Umair Rashid; Leticia C Rebello; Vitor Mendes Pereira; Robert Fahed; Michael Chen; Sunil A Sheth; Lina Palaiodimou; Georgios Tsivgoulis; Ronil Chandra; Feliks Koyfman; Thomas Leung; Houman Khosravani; Sushrut Dharmadhikari; Giovanni Frisullo; Paolo Calabresi; Alexander Tsiskaridze; Nino Lobjanidze; Mikayel Grigoryan; Anna Czlonkowska; Diana Aguiar de Sousa; Jelle Demeestere; Conrad Liang; Navdeep Sangha; Helmi L Lutsep; Óscar Ayo-Martín; Antonio Cruz-Culebras; Anh D Tran; Chang Y Young; Charlotte Cordonnier; Francois Caparros; Maria Alonso De Lecinana; Blanca Fuentes; Dileep Yavagal; Tudor Jovin; Laurent Spelle; Jacques Moret; Pooja Khatri; Osama Zaidat; Jean Raymond; Sheila Martins; Thanh Nguyen
Journal:  Int J Stroke       Date:  2021-03-29       Impact factor: 5.266

Review 8.  COVID-19 and stroke-Understanding the relationship and adapting services. A global World Stroke Organisation perspective.

Authors:  Hugh S Markus; Sheila Martins
Journal:  Int J Stroke       Date:  2021-04       Impact factor: 5.266

9.  Decline in stroke alerts and hospitalisations during the COVID-19 pandemic.

Authors:  Malveeka Sharma; Vasileios-Arsenios Lioutas; Tracy Madsen; Judith Clark; Jillian O'Sullivan; Mitchell S V Elkind; Joshua Z Willey; Randolph S Marshall; Magdy H Selim; David Greer; David L Tirschwell; Tina Burton; Amelia Boehme; Hugo J Aparicio
Journal:  Stroke Vasc Neurol       Date:  2020-08-27

10.  Stroke Code Presentations, Interventions, and Outcomes Before and During the COVID-19 Pandemic.

Authors:  Adam S Jasne; Pola Chojecka; Ilavarasy Maran; Razaz Mageid; Mohamed Eldokmak; Qiang Zhang; Karin Nystrom; Kelsey Vlieks; Michael Askenase; Nils Petersen; Guido J Falcone; Charles R Wira; Paul Lleva; Neer Zeevi; Reshma Narula; Hardik Amin; Dhasakumar Navaratnam; Caitlin Loomis; David Y Hwang; Joseph Schindler; Ryan Hebert; Charles Matouk; Harlan M Krumholz; Serena Spudich; Kevin N Sheth; Lauren H Sansing; Richa Sharma
Journal:  Stroke       Date:  2020-07-31       Impact factor: 7.914

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  1 in total

1.  Vertebral artery dissecting aneurysm rupture under severe COVID-19.

Authors:  Takenori Sato; Yoichi Miura; Ryuta Yasuda; Naoki Toma; Hidenori Suzuki
Journal:  Brain Hemorrhages       Date:  2022-08-12
  1 in total

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