Stroke leads to long-term neurological disability and is the second most common cause of death worldwide. Studies have shown that although its incidence, prevalence, and mortality have declined, its overall burden on society has increased (1, 2). Intracerebral hemorrhage (ICH), a subtype of stroke, accounts for 15–20% of all strokes and contributes significantly to the high morbidity and mortality rates worldwide (3, 4). Therefore, the diagnosis and treatment of ICH are necessary.

Coronavirus disease 2019 (COVID-19) and its associated neurological comorbidities (cerebrovascular diseases and cognitive impairment) have posed several challenges for global healthcare (5). The disease was first reported in Wuhan (Hubei Province, China) in December 2019 (6). At the end of January 2020, more than 90,000 people returned to Wenzhou city (located in the south of China; permanent population: 9.25 million) from Wuhan during the Spring Festival. Thus, Wenzhou became one of the most heavily affected areas during the COVID-19 pandemic outside the Hubei Province (7). The prevention and control strategies for the COVID-19 pandemic have led to significant declines in the efficiencies of diagnoses and treatments in hospitals in Wenzhou. Therefore, in this study, we observed the diagnosis and treatment of patients with acute ICH in Wenzhou during the COVID-19 pandemic. We aimed to determine the characteristics and prognoses of these patients in the hope that our data will provide evidence for improved management of ICH during the pandemic.

Early detection and intervention are essential for the survival of patients with ICH (11). The COVID-19 pandemic has increased the burdens and challenges faced by healthcare systems worldwide. In the present study, we have provided real-world data of patients diagnosed with ICH during January and June 2020 (i.e., during the COVID-19 pandemic) in Wenzhou (China), and have compared these data with those from the same period in 2019. We observed a significant impact of the pandemic and associated lockdown measures on the admission rates for ICH; a 35.1% decrease was noted in these rates in February 2020. The referenced period is featured with the peak of COVID-19 cases in China; the rate exceeded 3,000 infections/day for the first time on 2 February 2020 and rose to a peak of nearly 14,000 infections/day on 11 February 2020. The rate stabilized to <200 infections/day from 1 March 2020 onwards. A similar study in Germany showed that the admission rates for ICH fell by 42.1% due to an underutilization of the healthcare system (12). Another study conducted in Italy also noted that cases of ischemic stroke seemed to have almost disappeared from the Casualty Department of the authors' institution (13). This situation was observed for not only neurological diseases but also for other diseases, such as ST-segment elevation myocardial infarction (14). Our data, collected from the biggest governmental hospital in Wenzhou, showed that the number of patients diagnosed with ICH reduced significantly after the COVID-19 outbreak; however, this number rebounded in March 2020. Restrictions on traffic would have been an important factor for patients living in villages and towns around Wenzhou, who could have arrived at the hospital originally. An important reason might be a reluctance to seek medical care for the fear of infection, especially in crowded places. Thus, patients would have preferred to go to their local hospital to receive conservative treatment.

We compared whether there were any other differences between the two groups of different years and determined whether these differences were related to the COVID-19 pandemic. There were no significant differences in the sex, age, and timeliness of treatment between the 2019 and 2020 groups. However, we found that the domicile locations of the patients differed significantly between the groups, with only seven patients who were from the non-Wenzhou area of the Zhejiang Province.

The baseline mRS also differed significantly between the two groups; the incidence of mRS ≥3 was higher in the 2020 group than in the 2019 group. We noted that the rates of emergency surgery for ICH and poor outcomes in the ER were also higher in the 2020 group than in the 2019 group (Table 1); however, these differences were not significant. During the pandemic, it was reasonable that more patients with mild ICH chose to be treated locally rather than being sent to our center; the prolonged time for receiving prompt treatment would have caused more severe nerve function damage (15). The most common cause of ICH in both groups was hypertension; therefore, strict management of hypertension is extremely important and imminent for people in the Wenzhou area. Massive cerebral hemorrhage constituted a high proportion of cases in the two groups (43% in the 2019 group and 41% in the 2020 group); supratentorial ICH was the predominant type. There were no significant intergroup differences in the economic state and risk of infection (16, 17). Furthermore, despite traffic restrictions, most patients (72%) arrived at the ER within 6 h of ICH onset in 2020.

The COVID-19 pandemic also affected the patients' outcomes. Our data revealed that the risk of death for patients diagnosed between January and June 2020 was the highest within the first year after ICH, particularly during the first 5 days. According to previous literature, the cumulative mortality rates for ICH were 10.8–31%, 43–54%, and 22.5–71% at 1 month, 1 year, and 5 years after the ICH episode, respectively (18–23). Our data showed a moderate cumulative mortality rate in the first year after ICH (28.9%). Figure 3 shows a comparison of the 1-year mRS, which reflects the long-term functional prognosis for acute ischemic stroke (AIS), between the different months of 2020. It was reasonable to assume that the prognosis improved gradually after the lockdown period. The rebound in June might be attributed to the fluctuation in the COVID-19 cases following a return to work in China.

We also tried to identify the significant determinants of poor post-ICH outcomes and death after adjusting for confounding factors. Age, baseline mRS, postoperative complications, massive supratentorial hemorrhage, and creatinine were significantly associated with a poor prognosis. Hematoma volume seemed to be the supreme risk factor for not only an early outcome but also for long-term prognosis (21, 23, 24). Notably, neurosurgery was a protective factor, whereas massive supratentorial hemorrhage was a harmful factor for the survival of those with large-sized hematomas; however, these factors could not predict further functional outcomes. This observation is in line with those of a previous study conducted in India (25).

The strengths of our study included the large sample size from the Wenzhou medical health system caring for patients, which was the second impaired epicenter during the China epidemic. We used existing infrastructure and expanded with follow-up data collection according to a well-established methodology. Our data demonstrated a relatively high follow-up rate (88%). However, there were still several limitations in our current study. First, data on 1-year survival and functional outcome were only available in the 2020 group. Second, the 1-year outcome was estimated from information provided by the patients or their caregivers and there may be some subjective selection bias. Third, other related factors such as a history of medication with antiplatelet agents or anticoagulants were not acquired. Fourth, the exclusion of COVID-19 positive patients may also contribute to selection bias. Finally, even though there was a trend suggesting that 30-day mortality was higher during the lockdown period, the trend did not achieve significance. Further validation in larger cohorts with longer follow up is warranted.

Overall, the COVID-19 pandemic caused a sudden decline in the admission rates and high mortality and disability rates for ICH in Wenzhou. However, the total number of patients with ICH was almost the same between 2019 and 2020; this suggests a transfer of admissions, rather than missed admissions, in the lockdown period. Therefore, it is important to allocate resources and divert patients when necessary (26, 27). In order to improve the long-term prognosis and survival rates of patients with ICH during the pandemic, ensuring a “green channel” for stroke and allocating adequate medical resources will help in timely neurosurgery. As vaccination becomes more widespread, gradual deregulation of traffic restrictions would effectively improve the prognosis of patients with stroke. Simultaneously, for the high proportion of hypertensive cerebral hemorrhage cases, strengthening the prevention, and control of hypertension before and after ICH is also important (28, 29).

The original contributions presented in the study are included in the article/Supplementary Material, further inquiries can be directed to the corresponding authors.

The studies involving human participants were reviewed and approved by the First Affiliated Hospital of Wenzhou Medical University. Written informed consent for participation was not required for this study in accordance with the national legislation and the institutional requirements.

LF, JH, and GH conceived and designed the study. LF analyzed and interpreted the data. GL and XX collected the basic data, checked the medical records, and investigated the survival state of the patients in the green channel. XL and HQ screened the subjects in the ER. SS checked the nursing records in the ER. QW searched for cases in the online emergency registration system. WX provided advice on the prevention and control of the COVID-19 pandemic. All authors participated in the critical review and editing of the manuscript and approved the final manuscript.

The infrastructure for the study was funded by the Wenzhou Municipal Sci-Tech Bureau Programme (Y2020427).

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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