The characteristics of overseas imported COVID-19 cases and the effectiveness of screening strategy in Beijing, China

While great success in the coronavirus disease 2019 (COVID-19) control has been achieved in China, imported cases have become a major challenge. This study aimed to describe the epidemiological and clinical characteristics of imported COVID-19 cases and to assess the effectiveness of screening strategy in Beijing, China. This retrospective study included all imported COVID-19 cases from Beijing Ditan Hospital from 29 February to 20 March 2020, who were screened by both chest computed tomography (CT) and reverse-transcriptase-polymerase chain reaction (RT-PCR) at initial presentation. Demographic, clinical and laboratory data, in addition to chest CT imaging were were collected and analyzed.


Conclusions
The number of overseas imported COVID-19 cases continues to rise in China. The combination of screening tools, particularly CT and RT-PCR, can detect imported COVID-19 cases e ciently.

Background
In December 2019, a cluster of patients with pneumonia of unknown cause was occurred in Wuhan, Hubei Province, China [1][2][3][4][5].The novel coronavirus, identi ed as the causative agent, is now formally named as severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and the disease caused by this novel coronavirus is called coronavirus disease 2019  [6,7]. Due to the lack of immunity to SARS-CoV-2 virus in humans, as well as the e cient transmission between humans, this virus spread rapidly across the world. Concerning COVID-19, the World Health Organization (WHO) raised the threat to the CoV epidemic to the "very high" level on February 28, 2020 [8].
Data provided by the WHO Health Emergency Dashboard (24 March 2020, 10:00AM CET) report 332930 con rmed cases of COVID-19 worldwide since the beginning of the epidemic [9]. Outside of China, the main endemic areas are Europe, Americas and Eastern Mediterranean Region. Due to global economic integration, large numbers of Chinese people travel to these endemic countries for trade, tourism, labour, study and other purposes. Subsequently, with the outbreak of COVID-19 abroad and the control of the epidemic in China, importation of COVID-19 from highly endemic areas into China is inevitable.
In recent days, there has been a rise in imported COVID-19 cases in Beijing. In order to address this new challenge, the rapid and accurate detection of imported cases is of great signi cance. In this study, we implemented border entry screening (BES) for overseas travellers and in-hospital screening for suspected cases. This provided us with a good opportunity to describe the characteristics of imported COVID-19 cases and to to assess the effectiveness of screening strategy in Beijing, China.

Study design and subjects
A retrospective analysis of 71 con rmed overseas COVID-19 cases (a history of travel from affected geographic areas within 14 days of symptom onset), who were transferred to Beijing Ditan Hospital from 29 February to 20 March 2020 was carried out. All COVID-19 cases were diagnosed according to the Seventh Revised Trial Version of the Novel Coronavirus Pneumonia Diagnosis and Treatment Guidance [10]. A laboratory COVID-19 case was de ned as positive for SARS-CoV-2 nucleic acid of nasopharyngeal swab or/and sputum specimens by reverse transcription polymerase chain reaction (RT-PCR).
Screening process and data collection Imported COVID-19 cases admitted to our hospital were detected using 2 detection routes in fever clinic ( Figure 1): 1. Border entry screening: When an overseas ight arrived at Beijing international airport, travellers were required to complete body temperature monitoring and self-health declare during the customs check.
Any traveller who was deemed to have symptoms of COVID-19 (including close contacts) was transferred to our hospital.
2. In-hospital screening: First, the travellers screened on arrival at airport would have been placed under respiratory isolation conditions. Then, in addition to medical history and laboratory tests, SARS-CoV-2 test and chest computed tomography (CT) were performed for further con rmation.
Data including demographic data (ie, gender, age, cluster, country from where the infection was acquired), clinical, laboratory ndings and chest CT features at initial presentation were collected on each of the laboratory-con rmed cases. Laboratory results included complete blood count, C-reactive protein (CRP) and procalcitonin (PCT).

Statistical Analysis
We described the categorical variables as frequency rates and percentages (%), and continuous variables as mean and standard deviation (SD) or median and interquartile range (IQR) values, as appropriate. All statistical analyses were performed using SPSS (Statistical Package for the Social Sciences) version 22.0 software (SPSS Inc. According to laboratory ndings at initial presentation, the white blood cell (WBC) count of 7 (9.90%) cases was lower than the normal range (4×10 9 /L), and 4 cases (5.63%) had lymphocytopenia (the lymphocyte count was less than 1.0×10 9 /L). 8(11.27%) cases had platelets higher than the normal range (300×10 9 /L), and no case had lower platelets than the normal range (100×10 9 /L). There were 13 (18.31%) cases with high CRP. There was a normal PCT value.
During the diagnostic procedure, we found that 59 cases (83.10%) got a positive result in the rst RT-PCR test at initial presentation. However, the remaining 12 cases(16.9%) were further con rmed after admitting to the isolation ward. 5 cases (7.04%) got a positive result in the second RT-PCR test. 7 cases (9.86%) didn't obtained positive results until 3-5 round of tests later (Figure 4).
The effectiveness of screening strategy suggests that dynamic epidemiological history is of paramount importance for alert and early detection of COVID-19 patients.
All imported cases were screened rst at the customs via temperature monitoring and self-health declaration and then transferred to emergency department of infectious diseases in Beijing Ditan Hospital. In this study, the most common symptoms were fever and cough, similar to the cohorts reported in current available literatures [11][12][13]. Only 2 cases were asymptomatic, but SARS-CoV-2 nucleic acid were positive. Fever is less frequent in those infected with SARS-CoV-2 than those with SARS-CoV (99%) and MERS-CoV (98%) [14]. Furthermore, asymptomatic carriers are potential sources of SARS-CoV-2 transmission and cannot be ignored [15,16]. As screening heavily on syndromic detection, a substantial proportion of asymptomatic cases may be missed.
Previous studies have shown that chest CT scan is of great signi cance to screen the suspected cases of COVID-19 [17]. In the early stage, there were ground-glass opaci cation with or without consolidative abnormalities, especially showed with a peripheral distribution. In severe cases, lung consolidation may occur, but pleural effusion was rare [18]. In our study, nearly half of imported cases showed abnormal chest CT images, with GGO and consolidation. This was consistent with the study by Huang et al [19].Therefore, in clinical practice, when SARS-CoV-2 nucleic acid is negative or the result cannot be returned in time, chest CT images can be used as an important alert and help to quarantine the patient at the very rst time. Notably, normal chest CT imaging was found in 36(50.70%) cases compared to 17% of a recently study by Pan et al [20]. Therefore, a normal result from the initial CT scan does not rule out COVID-19 completely. The imaging features of COVID-19 were diverse and depended on the stage of infection after the onset of symptoms. A retrospective analysis of chest CT in 121 patients with COVID-19 by Bernheim et al [21] showed more frequent normal CT ndings (56%) in the early stages of the disease (0-2 days). In this regard, we suggest that follow-up CT scan should be performed with an interval of 3 days to show the pulmonary dynamic changes.
In this study, all cases received SARS-CoV-2 test at initial presentation. The sum of nucleic acid test prior to a positive diagnosis for each patient was analyzed. However, 7 cases didn't obtained positive results until 3-5 rounds of testing later. These negatives could result from improper sampling techniques or low viral load in the area sampled [22,23]. Therefore, for patients with high clinical suspicion, specimens should be continuously collected for multiple tests to avoid missed diagnosis.
There are several limitations to our study. First, due to the limited number of patients, our conclusions need to be further veri ed by large samples and multi-center data. Secondly, due to time constraints, those who were excluded from COVID-19 at initial presentation had not been followed up for longer periods of time. Therefore, continued attention needs to be paid to the report of local CDC on COVID-19 outbreaks for further veri cation.

Conclusions
Currently, SARS-CoV-2 continues to spread globlly. The epidemiologic study of imported cases showed that incoming travellers should not be overlooked as a source of imported infectious diseases. In order to accurately detect imported COVID-19 cases, the following aspects should be strengthened: We thank all cases included in this study. We are really grateful to all the health workers around the world.

Figure 2
The daily screened and con rmed overseas imported cases in Beijing, China, from 29 February to 20 March 2020.