key: cord-0933971-ishtl2os
authors: Wong, Shuk-Ching; Yuen, Lithia Lai-Ha; Chan, Veronica Wing-Man; Chen, Jonathan Hon-Kwan; To, Kelvin Kai-Wang; Yuen, Kwok-Yung; Cheng, Vincent Chi-Chung
title: Airborne transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2): What is the implication of hospital infection control?
date: 2021-07-12
journal: Infect Control Hosp Epidemiol
DOI: 10.1017/ice.2021.318
sha: 820c74af11d70eeee44c9c9891271c38c7bb7d7c
doc_id: 933971
cord_uid: ishtl2os

nan

To the Editor-Airborne transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the causative agent of coronavirus disease 2019 (COVID-19), has been increasingly recognized in the indoor air environment, 1 especially in poorly ventilated premises. 2 In the recent update of a scientific brief by Centers for Disease Control and Prevention, the modes of SARS-CoV-2 transmission include inhalation of very fine respiratory droplets and aerosol particles, deposition of virus on exposed mucous membranes, and touching mucous membranes with soiled hands contaminated with virus. 3 A nosocomial outbreak of COVID-19 was possibly attributed to airborne transmission in an old-fashioned general ward with low ceiling height, despite 6 air changes per hour (ACH). 4 To establish the role of airborne transmission of SARS-CoV-2 in the healthcare setting, it is important to demonstrate the presence of SARS-CoV-2 RNA and (preferably) viable virus in the air sample. However, this requires a challenging experiment. In the previous reports of air sampling in the clinical areas, findings have been inconsistent. 5 This inconsistency is not unexpected because air samplers with different mechanisms of sample collection (eg, solid impactors, liquid impactors, filters, and other sampling methods) were used. In addition, the testing protocols were different in terms of the relative position between patients and air samplers, number of patients in the room or ward, volume of air collected per sample, and the ACH in the patient care areas. Patient factors of transmission include the severity of clinical symptoms, the presence of aerosolgenerating procedure (AGP), viral load of clinical specimens, and whether the patient wore a surgical mask during sample collection. Current literature reporting the detection of SARS-CoV-2 RNA in the air in the healthcare setting is summarized in Supplementary Table 1 (online). Most of these studies do not mention the patient's viral load or whether the patient wore a surgical mask during sample collection.

To demonstrate the SARS-CoV-2 RNA viral load correlation between air and clinical samples, we performed air sampling in the airborne infection isolation room (AIIR; 16 m 2 and 12 ACH) where a single asymptomatic COVID-19 patient was cared for from June 11 to June 17, 2021. This patient was transferred to this hospital and had SARS-CoV-2 (PANGO lineage B.1.525). No AGP was performed during air sample collection. We collected the air sample using the AerosolSense Sampler (Thermo Fisher Scientific, Waltham, MA), 6 which is ∼35.5 cm in 3 dimensions and weighs 11.8 kg. It was placed 1 m from the patient's head. A single-use sampling cartridge containing 2.5 cm collection substrates was installed into the sampler. The air sample was collected through an omnidirectional inlet and was directed toward the collection substrate through an accelerating slit impactor at a flow rate of 200 L per minute. Particles were trapped on the collection substrate as the air moved around the collection area. After the sampling cycles of 2, 4, and 8 hours with patient with and without surgical masks, the sample cartridges were removed and sent to microbiology laboratory within 30 minutes. The collection substrates were then immersed into 1.5 mL viral transport medium and 250 μL medium for total nucleic acid extraction using the eMAG extraction system (bioMérieux, Marcy-l'Etoile, France) following the manufacturer's instructions. Quantification of SARS-CoV-2 RNA in the air samples was performed using the ultra-sensitive reverse-transcriptase droplet digital polymerase chain reaction (RT-ddPCR) with the QX200 Droplet Digital PCR System (Bio-Rad Life Science, Hercules, CA) as previously described. 7 The nasopharyngeal swabs were subjected to the same laboratory processing protocol. The viral loads of the air and clinical samples are summarized in Table 1 .

Our findings have implications for hospital infection control. In contrast to our previous report of undetectable SARS-CoV-2 RNA in 1,000 L air samples, 8 the SARS-CoV-2 RNA was detected at a concentration of 0.009 copies/L in the room of a COVID-19 patient who was not wearing surgical mask, with a moderate level of viral load (6,828,801 copies/mL) in the nasopharyngeal swab sample when 96,000 L air was collected over 8 hours. SARS-CoV-2 RNA was also detected (0.005 copies/L) in another 8-hour air sample from the room of this COVID-19 patient who was wearing a surgical mask. It appears that a low quantity of SARS-CoV-2 RNA can be detected in air, even in an AIIR with 12 ACH, when a large volume of air is collected for a prolonged period. If the experiment is performed in a general ward with 6 ACH, a higher quantity of SARS-CoV-2 RNA may be detected in the air. Therefore, inhalation of SARS-CoV-2 by patients may be possible if there is an unrecognized COVID-19 case in the same cubicle. 4 In such a case, a portable high-efficiency particulate filter may be installed, especially in an old-fashioned ward with suboptimal ventilation. In addition to the recommendation that healthcare workers (HCWs) wear surgical respirators during AGPs, we also suggest universal masking of patients and HCWs to reduce the risk of nosocomial transmission of SARS-CoV-2 in the healthcare setting. 9 These measures should be followed until herd immunity of COVID-19 through mass vaccination has been achieved.

Similar to the healthcare system in other developed areas, in Hong Kong we manage COVID-19 patients in hospital AIIRs with 12 ACH or in community treatment facilities with air ventilation of 80 L per second per person. 10 Full personal protective equipment, including surgical respirator, cap, face shield, gown, and gloves, is mandated when caring for COVID-19 patients. The risk of inhalation of SARS-CoV-2 by HCWs in hospital AIIRs or community treatment facilities is extremely low. However, transmission of SARS-CoV-2 is not only limited to the airborne route. Infection control professionals should update HCWs with new scientific evidence while enforcing hand hygiene, standard precautions, contact precautions, and droplet precautions to prevent nosocomial outbreaks of COVID-19. 

A systematic review of possible airborne transmission of the COVID-19 virus (SARS-CoV-2) in the indoor air environment

Probable airborne transmission of SARS-CoV-2 in a poorly ventilated restaurant

Scientific Brief: SARS-CoV-2 transmission

Nosocomial outbreak of COVID-19 by possible airborne transmission leading to a superspreading event

SARS-CoV-2: a systematic review of indoor air sampling for virus detection

Thermo Fisher Scientific launches in-air SARS-CoV-2 surveillance solution. Thermo Fisher Scientific website

Infection control challenges in handling recurrent blockage of sewage pipes in isolation facility designated for patients with COVID-19

Air and environmental sampling for SARS-CoV-2 around hospitalized patients with coronavirus disease 2019 (COVID-19)

Absence of nosocomial influenza and respiratory syncytial virus infection in the coronavirus disease 2019 (COVID-19) era: implication of universal masking in hospitals

Infection control challenges in setting up community isolation and treatment facilities for patients with coronavirus disease 2019 (COVID-19): Implementation of directly observed environmental disinfection

Acknowledgment. We thank our frontline staff of airborne infection isolation ward of Queen Mary Hospital for facilitating this study. Conflicts of interest. All authors report no conflicts of interest relevant to this article.