Relationship between Social Distancing and Admissions for Cerebrovascular Accidents at a Tertiary Medical Center during the COVID-19 Pandemic: A Retrospective, Community-Based Study

We evaluated the trend of admission of patients with acute cerebrovascular accidents (CVAs) during social distancing measures implemented during the coronavirus disease 2019 (COVID-19) era. The data of patients admitted with transient ischemic attack, ischemic stroke, intracerebral hemorrhage (ICH), and subarachnoid hemorrhage (SAH) to the emergency department of the Hanyang University Seoul Hospital were retrospectively analyzed. The data were compared between the pre-COVID-19 and COVID-19 periods. Poisson regression analysis was performed to evaluate changes in admission rates as a function of the year, social distancing level, and the interaction between the year and social distancing level. The number of admissions for CVAs dropped from 674 in the pre-COVID-19 period to 582 in the COVID-19 period. The decline in the number of admissions for ICH during social distancing measures was statistically significant, while the declines in SAH and ischemic stroke admissions were not. When the social distancing level was raised, admissions for CVAs dropped by 19.8%. The correlation between social distancing and decreased admissions for CVAs is a paradoxical relationship that may be of interest to the field of public health.


Introduction
The coronavirus disease 2019 (COVID- 19) pandemic, which emerged in Wuhan, China, in December 2019, has had a major impact on healthcare systems. To reduce the spread of the virus, numerous countries have enforced lockdowns. In South Korea, mask-wearing and social distancing were implemented to mitigate the rapid viral spread. The government has gradually tightened restrictions, and in turn, individual activity has decreased, and lifestyles have changed since the start of the COVID-19 pandemic. Subsequently, people have avoided public places, such as restaurants, department stores, sports stadiums, and, most importantly, hospitals, which has reduced the number of patients admitted to the emergency department [1]. Despite the emergency department being a place where people visit for urgent help [2], there has been a decline in admissions for acute coronary syndrome and orthopedic emergencies, as well as admissions to neurosurgery and neurology [3][4][5][6].
Herein, we evaluated the trend of admission of patients with acute CVAs during social distancing measures implemented during the COVID-19 era based on community-based tertiary medical centers.

Materials and Methods
We retrospectively analyzed the data of patients admitted to the Hanyang University Seoul Hospital. This regional emergency medical center primarily caters to patients from southeastern Seoul. Patients transferred from other regions of South Korea, especially from the nearby Gyeonggi-do Province, are also treated here.
Patients admitted to the emergency department with ischemic stroke (I63, I64), intracerebral hemorrhage (ICH [I61, I62]), and subarachnoid hemorrhage (SAH [I60]) were included in this study. All diagnoses were made based on disease classification according to the International Statistical Classification of Diseases and Related Health Problems, 10th revision.
We included transient ischemic attack (TIA) as a component of ischemic stroke and ICH as a part of hemorrhagic stroke. Patients with SAH were also included in this study. Patients with traumatic brain hemorrhage were excluded from this study to ensure the evaluation of spontaneous cerebrovascular events. Each patient's chart was reviewed to evaluate and compare risk factors for CVA.
This study aimed to investigate COVID-19 in uninfected patients to reduce possible sources of variance. Therefore, in 2020, we followed the treatment guidelines recommended by the Korean Neurosurgical Society during the COVID-19 pandemic, and none of our patients tested positive for the disease.
The period from 1 January to 31 December 2019 was considered the pre-COVID-19 period, whereas 1 January to 31 December 2020 was considered the COVID-19 period. The number of patients confirmed to have COVID-19 was released by the Korean government [11].
In 2020, there were three COVID-19 outbreaks, and the government increased the social distancing level each time (Table 1) [12,13]. We categorized these levels based on the time period and designated them as strength 1 (18 February to 5 May; social distancing levels were yet to be defined; instead, strongest social distancing came into effect), strength 2 (12 August to 12 November; three levels of national social distancing were defined), and strength 3 (13 November and onward; four levels of social distancing were defined).
Considering several diseases wax and wane with the seasons, this factor was included in the analysis. The seasons' definition was followed by the previous study as spring (March to May), summer (June to August), fall (September to November), and winter (December to February) [14]. These seasons are referred to as Korean climate change.

Statistical Analysis
A Poisson regression analysis was used to test whether the rate of admissions changed during the strength 1, 2, and 3 periods. As social distancing was implemented in 2020, this logistic was applied only to the 2020 data using the formula: The change in admission rate in association with seasonal variation was analyzed using the Poisson regression model as follows: These regression models suggest that by exponentiating the coefficient on Year and Season, we obtain the multiplicative factor by which the count changes.
The mean monthly admission numbers were compared using the paired t-test and reported as means with standard deviations. Differences were considered statistically significant at p < 0.05. All statistical analyses were conducted using R software, version 4.1.2 downloadable at http://cran.r-project.org/ (accessed on 1 December 2021) (R Foundation for Statistical Computing, Vienna, Austria).

Results
The first case of COVID-19 in South Korea was reported in January 2020. The pandemic has affected healthcare centers worldwide, and each country's government is implementing measures to arrest the spread of this disease. In South Korea, social distancing was implemented to mitigate the viral spread. During rapid increases in COVID-19 cases, the government tightened its restrictions with additional rules, such as prohibiting group meetings and restricting the maximum number of people using restaurants. Clubs and gyms faced similar restrictions, and religious activities were prohibited. Furthermore, numerous companies instituted telecommuting, which led to lifestyle changes in the population.
From January to December 2019, 674 patients (mean age, 65.38 years; 47% women) with ischemic stroke, ICH, or SAH were admitted to the emergency room ( Table 2). The mean monthly admission number was 56.17 ± 7.6. In 2020, the total number of admissions dropped to 582, and the mean monthly admission number also declined to 48.5 ± 9.68 (Table 2, Figure 1). There were no significant differences in patient characteristics between the groups.   Of the total cases in 2019, ischemic stroke, including TIA, accounted for 57.9%; ICH, 25.7%; and SAH, 16.5%. In 2020, the corresponding values were 62.6%, 19.2%, and 18.6%, respectively ( Figure 1).
The overall trend for all three CVA groups showed decreased admission rates; however, this was only statistically significant in the ICH group (Table 3). Of the total cases in 2019, ischemic stroke, including TIA, accounted for 57.9%; ICH, 25.7%; and SAH, 16.5%. In 2020, the corresponding values were 62.6%, 19.2%, and 18.6%, respectively ( Figure 1).
The overall trend for all three CVA groups showed decreased admission rates; however, this was only statistically significant in the ICH group (Table 3). During social distancing measures, the number of admissions for CVA was significantly affected by a factor of year, which dropped by 13.65% (rate ratio is exp [−0.14676] = 0.86350) ( Table 4, p = 0.0095). Moreover, the number of admissions was significantly affected by a factor of the season fall. It dropped by 15.97% (rate ratio is exp [−0.173923] = 0.84036) compared to spring. However, it is not significantly different from other seasons. Figure 2 shows the comparison of monthly admission numbers. While all the CVA groups demonstrated decreased admissions during social distancing, the number of admissions for ICH was significantly affected by the factor of Year, which dropped by 35.3% (rate ratio is exp (−0.4348) = 0.64739) ( Table 5, p = 0.000337). Furthermore, the number of admissions was significantly affected by the factor of the season fall. The number dropped by 35.53% (rate ratio is exp (−0. 4389) = 0.64475) compared to spring. However, it was not significantly different from other seasons. Figure 3 shows the comparison of monthly admission numbers. However, these findings are different from those of a previous study [14].  While all the CVA groups demonstrated decreased admissions during social di ing, the number of admissions for ICH was significantly affected by the factor of which dropped by 35.3% (rate ratio is exp (−0.4348) = 0.64739) ( Table 5, p = 0.000337 thermore, the number of admissions was significantly affected by the factor of the s fall. The number dropped by 35.53% (rate ratio is exp (−0. 4389) = 0.64475) compa spring. However, it was not significantly different from other seasons. Figure 3 show comparison of monthly admission numbers. However, these findings are differen       In 2020, when social distancing levels were raised, the admission numbers drop by 19.8% (p = 0.02435). Moreover, the admission number decreased by 27.3% in the w (p = 0.00629, Table 6). When the time periods corresponding to strengths 1, 2, and 3 studied, the strength 1 period showed the largest decline of 34.2% (p = 0.0014, Table In 2020, when social distancing levels were raised, the admission numbers dropped by 19.8% (p = 0.02435). Moreover, the admission number decreased by 27.3% in the winter (p = 0.00629, Table 6). When the time periods corresponding to strengths 1, 2, and 3 were studied, the strength 1 period showed the largest decline of 34.2% (p = 0.0014, Table 7).

Discussion
Previous studies have reported a decreased number of patients visiting emergency rooms during the COVID-19 era [16], including transient ischemic attacks and strokes [10]. We confirmed that the COVID-19 pandemic was associated with decreased mean monthly admissions for patients with acute CVA. Although there was no significant difference in patient characteristics between different types of strokes, stricter social distancing measures were associated with decreased admission rates of patients with CVAs, especially ICH. However, the reductions in ischemic stroke and SAH admissions were not statistically significant, contradicting previous findings, which showed decreased demand for care [17]. A recent meta-analysis reported that SAH occurrence was low in summer than in winter months [18]. Paradoxically, during the COVID-19 era, our data show that CVA incidents were lowest during the winter months.
In 2020, there were three waves of COVID-19 in South Korea, and the levels of social distancing were increased each time; we analyzed admissions for CVAs during these periods designated as strengths 1, 2, and 3. On implementing social distancing measures, the number of admissions decreased compared with that during the rest of the year. In the strength 1 period, there was the greatest reduction in admissions.
Based on our results, we may think of the extra effect of social distancing. During the rapid increase in COVID-19 cases, the government tightened its restrictions, decreasing individual physical activity. Physical activity is well known for preventive measures for ischemic stroke [19]. The decrease in admissions for CVA during the COVID-19 era presents a paradox because the COVID-19 pandemic resulted in decreased levels of physical activity. Potential explanations for this discrepancy include increased happiness during the COVID-19 pandemic, reduced stress [20] and decreased social activity [21].
Our study had a limitation; namely, it was a single-center study. Nevertheless, considering that our hospital is a community-based tertiary care center and a regional emergency medical center that covers Southeastern Seoul, the changing trend of admissions that we observed could represent the overall pattern in South Korea. However, further studies need to be conducted, including more recent data and multiple medical centers, to validate our findings.

Conclusions
The onset of COVID-19 has made the South Korean government implement maskwearing and social distancing to mitigate the viral spread. In South Korea, and likewise in other countries worldwide, acute stroke admissions have dropped in the COVID-19 era. Especially when social distancing levels were strict, the admission number of strokes dropped significantly. Several vaccines against COVID-19 have been approved in South Korea, and vaccination drives have been conducted. By steadily increasing these rates, the South Korean government is now preparing to adopt the 'With COVID-19' scheme as soon as 80% of adults are fully vaccinated. Based on this plan, the government seeks a gradual return to normal life with relaxed social distancing measures. This study demonstrates that stringent social distancing measures are correlated with a decrease in admissions for CVAs at a regional hospital in South Korea. Our findings highlight a paradoxical relationship that may be of interest to the field of public health.

Institutional Review Board Statement:
The study was conducted in accordance with the Declaration of Helsinki and approved by the Institutional Review Board of Hanyang University medical center (protocol code 2022-03-001).

Informed Consent Statement:
The requirement for informed consent was waived by the IRB, as data were extracted retrospectively in an anonymized form.