Coronavirus Disease 2019 (COVID-2019) Infection Among Health Care Workers and Implications for Prevention Measures in a Tertiary Hospital in Wuhan, China

IMPORTANCE Health care workers (HCWs) have high infection risk owing to treating patients with coronavirus disease 2019 (COVID-19). However, research on their infection risk and clinical characteristics is limited. OBJECTIVES To explore infection risk and clinical characteristics of HCWs with COVID-19 and to discuss possible prevention measures. DESIGN, SETTING, AND PARTICIPANTS This single-center case series included 9684 HCWs in Tongji Hospital, Wuhan, China. Data were collected from January 1 to February 9, 2020. EXPOSURES Confirmed COVID-19. MAIN OUTCOMES AND MEASURES Exposure, epidemiological, and demographic information was collected by a structured questionnaire. Clinical, laboratory, and radiologic information was collected from electronic medical records. A total of 335 medical staff were randomly sampled to estimate the prevalence of subclinical infection among a high-risk, asymptomatic population. Samples from surfaces in health care settings were also collected. RESULTS Overall, 110 of 9684 HCWs in Tongji Hospital tested positive for COVID-19, with an infection rate of 1.1%. Of them, 70 (71.8%) were women, and they had a median (interquartile range) age of 36.5 (30.0-47.0) years. Seventeen (15.5%) worked in fever clinics or wards, indicating an infection rate of 0.5% (17 of 3110) among first-line HCWs. A total of 93 of 6574 non–first-line HCWs (1.4%) were infected. Non–first-line nurses younger than 45 years were more likely to be infected compared with first-line physicians aged 45 years or older (incident rate ratio, 16.1; 95% CI, 7.1-36.3; P < .001). The prevalence of subclinical infection was 0.74% (1 of 135) among asymptomatic first-line HCWs and 1.0% (2 of 200) among non–first-line HCWs. No environmental surfaces tested positive. Overall, 93 of 110 HCWs (84.5%) with COVID-19 had nonsevere disease, while 1 (0.9%) died. The 5 most common symptoms were fever (67 [60.9%]), myalgia or fatigue (66 [60.0%]), cough (62 [56.4%]), sore throat (55 [50.0%]), and muscle ache (50 [45.5%]). Contact with indexed patients (65 [59.1%]) and colleagues with infection (12 [10.9%]) as well as community-acquired infection (14 [12.7%]) were the main routes of exposure for HCWs. CONCLUSIONS AND RELEVANCE In this case series, most infections among HCWs occurred during the early stage of disease outbreak. That non–first-line HCWs had a higher infection rate than firstline HCWs differed from observation of previous viral disease epidemics. Rapid identification of staff with potential infection and routine screening among asymptomatic staff could help protect HCWs. JAMA Network Open. 2020;3(5):e209666. doi:10.1001/jamanetworkopen.2020.9666 Key Points Question What are the exposure details and clinical characteristics of health care workers with coronavirus disease (COVID-19) in Wuhan, China? Findings In this single-center case series including 9684 health care workers, 110 of whom had COVID-19, a higher rate of infection was found among those working in the low-contagion area during the early stage of the disease outbreak, especially among nurses younger than 45 years. Most health care workers with COVID-19 had nonsevere disease, with an asymptomatic carrier prevalence of 0.9% and a mortality rate of 0.9%. Meaning In this study, most infections among health care workers occurred during the early stage of the COVID-19 outbreak and in low-contagion areas; routine screening may be helpful in identifying asymptomatic carriers.


Introduction
The outbreak of coronavirus disease 2019  first emerged in Wuhan, Hubei Province, China, in December 2019. [1][2][3][4] Person-to-person transmission has been confirmed. [5][6][7] On January 30, 2020, the World Health Organization declared a public health emergency of international concern. 8 Although the government of Wuhan banned nonessential vehicles in the urban area, hospitals were still densely populated and became the most critical places to control the spread of COVID-19.
Unlike severe acute respiratory syndrome (SARS) or Middle East respiratory syndrome, COVID-19 was less virulent, with a lower mortality rate. [9][10][11] Nevertheless, low virulence and longer incubation periods resulted in a significant number of asymptomatic carriers. 12 These patients might not take adequate precautions and thus could become a source of transmission. 5 Secondgeneration cases, spread by patients in the incubation period and asymptomatic carriers, have already been reported, and these cases appear to have included health care workers (HCWs). 13 Asymptomatic transmission could further increase the risk of superspreading in hospitals. 14 To date, research on transmission within hospitals has remained scarce.
Tongji Hospital is a large comprehensive tertiary hospital in Wuhan with more than 7000 beds and 9648 staff members. It was designated for the treatment of patients with COVID-19 during the epidemic outbreak. A total of 3110 of 9648 HCWs (32.2%) were transferred to fever clinics or wards to treat patients with the virus. By February 9, Tongji Hospital had received a total of 10 830 outpatients in fever clinics, with many later diagnosed with COVID-19. Frontline HCWs could be at high risk of infection because of close contact with these patients. Moreover, HCWs with infection could cause secondary transmission among patients, family members, and the community.

Study Design and Participants
We retrospectively recruited 110 HCWs with COVID-19 at Tongji Hospital from January 1 to February 9, 2020. Exposure, epidemiologic, demographic information was retrospectively collected by a structured questionnaire, and the clinical, laboratory, and radiologic information was collected from electronic medical records. First-line HCWs were defined as those who worked in fever clinics or wards and provided direct care to patients with confirmed or suspected COVID-19. Non-first-line HCWs were defined as those who attended patients in general (ie, patients without COVID-19).
To detect the prevalence of subclinical infection of asymptomatic HCWs, we actively screened 335 HCWs at Tongji Hospital. The screened HCWs comprised 135 staff members (40.3%) from fever clinics or wards and 200 staff (59.7%) from other departments. Participants were randomly selected according to their staff identification numbers. The study was approved by the Tongji Hospital research ethics committee. Written informed consent was obtained from all participants. All collected data were securely stored in a database. This study followed the Strengthening the

Personal Protective Equipment and Environmental Cleansing Protocols
The personal protective equipment (PPE) used in low-contagion areas included surgical masks (equivalent to ASTM level 2), latex gloves and gowns (equivalent to AAMI level 2), and disposable round caps. The PPE used in the high-contagion areas included fit-tested particulate respirators (equivalent to an N95 mask), long-sleeved gowns (equivalent to AAMI level 4), goggles, disposable round caps, latex gloves, and shoe covers. The detailed environmental cleaning protocols were as follows: (1) a chlorine dioxide air disinfection machine was used 4 times a day for 2 hours at a time for air disinfection in wards with patients; (2) empty wards were irradiated with UV light once a day for 1 hour; (3) chlorine dioxide (500 mg/L) was sprayed with an ultra-low volume sprayer for air disinfection in public areas, with a dose of 20 to 30 mL/m 3 ; and (4) surfaces of environmental objects were wrapped with chlorine-containing disinfection solution (1000 mg/L) twice a day. The environmental samples were collected after disinfection.

Sampling Process
SARS-CoV-2 laboratory tests followed the World Health Organization recommendations. 15 Nasopharyngeal swabs were obtained by nurses using a standard technique of wiping a flocculated swab across the posterior oropharynx from 1 tonsillar area to the other. Swabs were immediately placed in a transport medium, placed in a portable cooler, and delivered to our central laboratory.
Standard procedures 16 were followed to collect environmental surface samples from fever clinics (n = 30), other departments (n = 30), and administration offices (n = 30). Sterile, cottontipped swabs prewetted with phosphate-buffer saline were drawn back and forth once across a 100-cm surface. Circular sweeps were used to swab objects with which individuals with infection would have come in contact, including diagnostic tables, door handles, bed bars, elevator buttons, computer keyboards and mouses, and registration machines, among others. After sampling, cotton rods were directly immersed in a phosphate-buffered saline solution and delivered to our central laboratory. Laboratory confirmation of COVID-19 was carried out by real-time reverse transcriptionpolymerase chain reaction using methods described previously. 17

Statistical Analysis
Continuous variables were described with medians and interquartile ranges (IQRs). Categorical variables were described as frequency and percentages. The Mann-Whitney U test, χ 2 test, and Fisher exact test were used according to variable types as appropriate. The Poisson regression model was used to calculate the incident rate ratio (IRR) and 95% CIs for HCWs with COVID-19. A 2-sided P < .05 was considered statistically significant. All analyses were performed using SPSS statistical software version 20.0 (IBM Corp).

Development of the Epidemic in HCWs
The Figure

Exposure Information
According to reports by 110 HCWs with COVID-19, 70 (63.6%) were presumably infected in general clinics or wards, 7 (6.4%) in fever clinics or wards, and 14 (12.7%) through community-acquired infection. A total of 66 (60.0%) reported disease onset on or before January 20 and 25 (22.7%) after January 20; 65 (59.1%) attributed infection to contact with patients who were later diagnosed with COVID-19, 12 (10.9%) to contact with colleagues, and 14 (12.7%) to contact with family or friends. The other 19 HCWs (17.3%) could not recall their exposure history. None had been to Huanan seafood market, but 13 (11.8%) had been to other wet markets. Regarding the type of onset, 31 (28.2%) were

Clinical Characteristics of HCWs With COVID-19
Clinical characteristics of 110 confirmed HCWs with COVID-19 are shown in Table 3. The rate of comorbidities in affected HCWs was 12.7% (14 of 110). The 4 most common comorbidities among all   (3)(4)(5)(6)(7)(8) days, and the median (IQR) time from onset of symptom to treatment was 1 (0-2) days. There was no difference between first-line and non-first-line HCWs in the subgroups of comorbidity and common symptoms. Table 4 shows the laboratory findings for HCWs with COVID-19 on admission to hospital. The      .68

Discussion
Our study was based in a large comprehensive tertiary hospital in Wuhan, China. As a large number of outpatients were treated in fever clinics every day, HCWs were at high infection risk.
Superspreading events had been reported in other hospitals. 14  may not be as severe as SARS. 2 Many patients who were infected had no or very subtle symptoms, and some exhibited atypical symptoms. 19 The existence of such patients could greatly endanger the health of staff even though clinical areas caring for patients with and without COVID-19 were separated from each other. Third, because of lack of disease knowledge, it was difficult to identify patients with COVID-19 at the beginning of this epidemic. A total of 0.9% of HCWs with COVID-19 were asymptomatic. Until now, little was known about the risk of transmission from asymptomatic carriers. One reason for the rapid spread worldwide could be asymptomatic patients in the early stage. 5 The viral load detected in asymptomatic patients was similar to that detected in symptomatic patients, indicating the transmission potential of asymptomatic carriers of SARS-CoV-2. 12 These asymptomatic HCWs might become a risk factor for patients, colleagues, and the community. Therefore, identification of asymptomatic carriers among In our study, most infections in HCWs occurred at the early stage of the epidemic, before protective measures were taken. This may imply that the rigorous prevention measures taken in Tongji Hospital were effective to prevent or limit transmission in a health care setting. We stressed the importance of appropriate use and especially disposal of PPE for HCWs later in the outbreak to ensure that PPE was effective and to avoid any increase in transmission. Moreover, we strictly divided the highly contagious areas (ie, fever clinics and wards) in 3 parts, as clean areas, potentially contaminated areas, and contaminated areas. Furthermore, we separated medical staff and patient access to avoid possible cross-infection. No surface specimen tested positive. A possible explanation is that virus contamination in the health care setting might not be a source of transmission to patients or of nosocomial outbreaks for COVID-19. Moreover, cleaning and disinfection procedures, which were ensured consistently and correctly in the hospital, could largely reduce the spread of many pathogens in the health care setting. 20,21 Cleaning surfaces with water and detergent and applying additional hospital disinfectants (such as chlorine dioxide disinfectant) could be an effective and sufficient procedure to prevent transmission of COVID-19 through environmental contamination.
In this study, 84.5% of affected HCWs had mild or moderate disease. There are several possible reasons for this. First, most affected HCWs in our study were young adults. Patients with severe and critical COVID-19 are usually older. Second, early symptoms were more easily noticed by HCWs, which could also explain the lower frequency of fever reported in our study. Fever was much more common in other studies, including among patients with severe COVID-19. 13 Third, the time between symptom onset and treatment was 1 day, which was much shorter than in other studies. 19,22 All these may indicate that early diagnosis and treatment favored a better outcome for patients with COVID-19. Half the HCWs with infection were treated outside the hospital. This might indicate that treating mild patients outside a hospital setting with appropriate guidance from qualified medical professionals could be a feasible method when hospital capacity is limited.

Limitations
This study has limitations. The recall bias of this survey could be a concern, but information collection took place recently, and the possibility of recall bias was small. Furthermore, the information collected was about concrete behaviors, especially when the surveyed subjects were HCWs.

Conclusions
In this study, non-first-line HCWs were at a high risk of infection during the early stage of the COVID-19 outbreak, and interventions targeting this group should be evaluated. Most HCWs with infection had mild symptoms; however, special attention needs to be paid to protect HCWs from cross-infection from other HCWs.