Shanghai Public Health Clinical Center is the designated hospital to treat adult patients with COVID-19 in Shanghai. From January 20, 2020 to March 10, 2020, a total of 334 clinic- and laboratory-diagnosed patients have been hospitalized and treated in AIIRs with negative differential pressure in three independent buildings, denoted 1, 2 and 3. Relevant information on the AIIRs, patients and HCWs in each building is provided in Table 1. The 82 AIIRs in building 1 and 2 were non-ICU AIIRs dedicated to patients with mild symptoms. There were 58 HCWs (12 doctors and 46 nurses) in building 1 who were responsible for 111–113 patients, and 41 HCWs (10 doctors and 31 nurses) in building 2 responsible for 74–77 patients at the time of surveillance. The 33 AIIRs in building 3 were intensive care unit (ICU) AIIRs for patients in severe or critical condition. A total of 191 HCWs (30 doctors and 161 nurses) were responsible for 33 patients in building 3. All the surgery including intubation, tracheotomy and ECMO were performed in the AIIRs in building 3.
Parameter Building 1 Building 2 Building 3 AIIR information AIIR numbers 41 41 33 Beds in each AIIR 3 3 1 or 2 Air pressure (Pa) -20 -20 -20 Air change rate (per hour) 15 15 15 Operation daysa 17 11 24 Hospitalized patients Number of patients at first sampling 111 74 40 Number of patients at second sampling 113 77 32 Patient condition Mild Mild Severe, critical Surgery No No Intubation, tracheotomy, ECMO Healthcare workers Number of doctors 12 10 30 Number of nurses 46 31 161 AIIR airborne infectious isolation room, ECMO extracorporeal membrane oxygenation.
aFrom the date that the first patient was hospitalized to when the first sample was collected.
Table 1. Information on airborne infectious isolation rooms (AIIRs) at the Shanghai Public Health Clinic Center.
A diagram of the floor layout in the inpatient area of the Shanghai Public Health Clinic Center is shown in Fig. 1. For each floor, the space was divided into a clean area (including offices, living and changing rooms for HCWs), a semi-contaminated area (including nurse station and connective corridors) and a contaminated area (including corridor, AIIRs and dedicated bathrooms). Access to the contaminated area was restricted along a unidirectional route. Supplies were unidirectionally transferred from the clean area to the contaminated area through pass-through chambers.
All the AIIRs have independent air supply and exhaust systems, with a ventilation of 15 air changes per hour. Air supply was located at the ceiling above beds and the exhaust was placed on the wall near the floor, creating a directional airflow from top-to-bottom in individual AIIRs (Fig. 1). Exhaust air was cleaned by passing through HEPA filters before emission. The AIIR maintained a negative air pressure of 20 Pa differential to the corridor to prevent potential pathogen leakage into the clean area. All the AIIRs had self-closing doors equipped with hands-free foot-operated openers.
Before access to the semi-contaminated area and contaminated area, all healthcare workers were required to wear personal protective equipment (PPE), including hooded disposable coveralls, N95 respiratory masks, goggles, face shield, double-layers gloves, and disposable boots (Fig. 1). They were also required to wear powered air-purifying respirators when performing surgery in the ICU-AIIR of building 3.
The hygiene procedure was performed as follows. The floor was mopped with 2000 mg/L sodium hypochlorite solution once per day and the surfaces of furniture, instruments and other objects were disinfected with 0.22%–0.88% quaternary ammonium salt solution twice per day. Personal hygiene care of the healthcare workers was performed by spraying 75% alcohol solution or disinfection gel composed of 65% alcohol and 11% propanol after they performed surgery or medical care services.
Viral transmission and the risk of infection may be altered due to the unique environment and hygiene procedure in AIIRs. Under natural conditions SARS-CoV-2 is largely transmitted through respiratory droplets (Chan et al. 2020). To evaluate the risk of airborne transmission inside AIIRs, we collected air samples from 15 AIIRs, including 7 ICU-AIIRs in building 3 and 8 non-ICU AIIRs in buildings 1 and 2. Two of the samples were collected in the ICU-AIIR of building 3 when tracheotomy surgery was performed. Importantly, none of the air samples tested positive for the presence of SARS-CoV-2 virus (Supplementary Table S2). We also collected surface samples from air exhaust and HEPEA filters and failed to detect any viral RNA. Similarly, air samples collected in the corridor or the changing rooms of the semi-contaminated area did not show any presence of virus (Supplementary Table S2). The absence of virus in air samples indicates that the risk of airborne transmission inside AIIRs is low.
Two studies have identified surface contamination with SARS-CoV-2 in isolated wards before environmental hygiene measures were imposed (Ong et al. 2020; Cheng et al. 2020). To evaluate the transmission risk of surface contamination, we collected a total of 1138 surface samples and tested the presence of viral RNA at different locations inside AIIRs, including floors, walls, furniture, bathrooms, medical equipment and personal equipment such as cell phones (Fig. 1; Table 2). Samples were collected twice before environmental hygiene procedures. Critically, we did not detect any viral RNA in most of the surface samples inside AIIRs, including floors, walls, furniture, medical equipment or patients' cell phones, indicating that environment hygiene was effective in eliminating the virus (Table 2). However, viral RNA was detected in samples collected from the foot-operated openers and the bathroom sinks (Table 2). The amounts of viral RNA were low but detectable (Fig. 2). Notably, these positive samples were found in both mild (1 AIIRs in building 1) and severe (3 AIIRs in building 3) patient rooms, although positive samples seemed to be more frequent in AIIRs with severe patients, especially those containing surgical patients. Patients living in the AIIR in building 1 had mild disease and could get around freely, while those living in the 3 AIIRS in building 3 exhibited severe symptoms and were undergoing mechanical ventilation.
Sampling sites Building 1 Building 2 Building 3 Total 1sta 2nd 1st 2nd 1st 2nd Patient's room 7/537 (1.30%) 1. Air outlet 0/5b 0/5 0/5 0/5 0/2 NA 0/22 2. Floor 0/11 0/5 0/16 0/5 0/10 0/2 0/49 3. Wall 0/5 0/5 0/7 0/5 0/5 0/3 0/30 4. Door handle 0/10 0/13 0/12 0/5 0/5 0/14 0/59 5. Foot operated opener 1/2 0/13 0/5 NA 0/3 3/14 4/37 6. Chair 0/5 0/5 0/6 0/5 0/4 0/3 0/28 7. Medical equipment 0/1 0/5 0/1 0/5 0/22 0/11 0/45 8. Personal equipment (mobile phone) 0/6 0/7 0/6 NA 0/1 NA 0/20 9. Bed edge 0/9 0/10 0/11 0/10 0/10 0/6 0/56 10. Bathroom floor 0/2 0/5 0/3 0/5 0/3 0/3 0/21 11. Shower set 0/4 0/5 0/6 0/5 0/5 0/3 0/28 12. Sink 1/5 0/9 0/7 0/5 0/5 2/13 3/44 13. Table including handle 0/5 0/5 0/8 0/5 0/6 0/3 0/32 14. Toilet surface 0/4 0/6 0/6 0/5 0/4 0/3 0/28 15. Pass-through box including handle 0/5 0/5 NA NA 0/2 NA 0/12 16. Air sample 0/4 0/1 0/9 NA 0/5 0/7 0/26 Corridor 13/310 (4.19%) 17. Floor 0/9 0/14 0/3 0/6 3/12 1/18 4/62 18. Wall 0/6 0/6 0/6 0/6 0/12 0/6 0/42 19. Door handle 2/6 NA 0/4 NA 1/12 NA 3/22 20. Foot operated opener 1/6 NA 0/6 0/6 3/6 NA 4/24 21. Medical equipment 1/6 0/17 0/16 0/9 0/13 0/18 1/79 22. Sink 0/6 0/15 0/4 0/6 0/12 0/18 0/61 23. Table including handle NA NA 0/8 NA 1/2 NA 1/10 24. Air sample 0/1 0/2 NA NA 0/1 0/4 0/10 Elevator 2/69 (2.90%) 25. Floor 0/8 0/3 0/2 0/3 0/6 0/3 0/25 26. Wall 0/1 0/2 0/1 0/3 0/1 0/1 0/9 27. Elevator button 0/4 1/10 0/3 0/3 0/4 1/11 2/35 Healthcare workers 3/258 (1.16%) 28. Face shield 0/10 0/5 0/6 0/3 0/10 0/8 0/42 29. Front of protective clothing 0/10 0/5 0/6 0/3 0/11 0/8 0/43 30. Back of protective clothing 0/1 NA 0/6 NA NA NA 0/7 31. Hand (with gloves) 0/11 1/13 0/6 0/3 0/10 0/20 1/63 32. Sleeves 0/9 0/5 0/6 0/3 0/10 0/8 0/41 33. Foot 0/10 0/13 0/6 1/3 1/10 0/20 2/62 a Different numbers refer to different sampling times. b It stands for the number of positive samples/the total number of samples. NA, not available
Table 2. Detection of SARS-CoV-2 in environmental samples collected from the contaminated area of the hospital.
Figure 2. Viral loads in all the positive samples. The horizontal box lines represent the first quartile, the median, and the third quartile of viral loads. Each dot represents a positive sample and circles represent outliers.
The presence of viral RNA on foot-operated openers and the bathroom sinks may act as a source of contamination outside AIIRs. Accordingly, we collected and tested 61 samples in the corridors outside of AIIRs. As with testing inside AIIRs, viral RNA was also detected on the foot-operated openers in the corridors. Overall, 1 of 15 foot-operated opener samples in building 1, and 3 of 17 samples in building 3 were positive for SARS-CoV-2 RNA. Viral RNA was also detected in the samples collected on the corridor floor in building 3, but not in building 1 or 2. Furthermore, viral RNA was also detected on hand-touching objects, including the surfaces of door handles, medical equipment, furniture and elevator buttons in both buildings 1 and 3.
The presence of viral RNA on floors, foot-operator openers and hand-touching objects indicated that there was potential contamination of the gloves and boots of HCWs. We therefore tested the presence of viral RNA on the surface of the HCWs' PPE. Samples were collected from face shields or goggles, gloves, coverall sleeves, the front side of coveralls and bottom of disposable boots from 63 HCWs. Notably, samples were all collected just after HCWs provided medical care to patients and before disinfection (Fig. 1; Table 2). We did not detect any viral RNA on face shields, goggles, or on the front side of the HCW's coveralls. However, viral RNA was detected on the gloves of one nurse from building 1 (1/63) and two nurse's disposable boots in buildings 2 and 3 (2/62). The amounts of RNA were low, but detectable.
Although viral RNA was detected on the gloves and boots from some HCWs, all were required to remove PPEs and complete hand and boot hygiene before leaving the contaminated area. The chance of viral contamination of other areas was therefore very low. Indeed, no viral RNA was detected in 370 samples collected from semi-contaminated and clean areas, including floors, wall and other hand-touching surfaces (Supplementary Table S1).
According to the results of the environment surveillance, the environmental hygiene procedure was upgraded to more frequent floor-mopping, disinfecting the foot-operated openers and bathroom sinks, as well as more powerful personal hygiene of HCWs' gloves and boots with 75% alcohol with 0.10%–0.14% hydrogen peroxide solution. No viral RNA was detected in the samples collected following the application of the new infection control procedures.
At the time of writing, a total of 334 patients of COVID-19 have been hospitalized and treated at the center. Of these, 307 patients have been cured and discharged. All the off-duty HCWs received two throat swab tests for SARS-CoV-2 and they were isolated for medical observation for two weeks. None reported symptoms of COVID-19 infection or were positive for the presence of virus in throat swab tests.