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Transmission of Severe Acute Respiratory Syndrome Coronavirus 1 and Severe Acute Respiratory Syndrome Coronavirus 2 During Aerosol-Generating Procedures in Critical Care: A Systematic Review and Meta-Analysis of Observational Studies*

Chan, Vinson Wai-Shun1*; Ng, Helen Hoi-Lam1*; Rahman, Laiba1; Tang, Audrey BSc (Hons)1; Tang, Kwan Pui2; Mok, Alex2; Liu, Jeremy Ho Pak2; Ho, Kenny Shiu Cheong2; Chan, Shannon Melissa FRCSEd (Gen)3; Wong, Sunny DPhil (Oxon), FRCP (Edin), FRCPath, FHKCP, FHKAM (Medicine)4; Teoh, Anthony Yuen-Bun MD, FRCSEd (Gen), FACS, FASGE, FJGES3; Chan, Albert FHKCA, FHKAM, FANZCA5; Wong, Martin MD, FHKCFP, FRACGP(Aust), FRSPH(UK), FHKAM(Fam Med)6; Yuan, Yuhong MD, PhD7; Teoh, Jeremy Yuen-Chun FRCSEd (Urol), FCSHK, FHKAM (Surgery)8

Author Information
doi: 10.1097/CCM.0000000000004965


The World Health Organization reported that 22,073 healthcare workers (HCWs) from 52 countries are diagnosed with coronavirus disease 2019 (COVID-19) as of April 8, 2020 (1). Previous experiences during the 2003 severe acute respiratory syndrome (SARS) outbreak suggested a huge risk of nosocomial infection through bioaerosolization of the virus (2) via aerosol-generating procedures (AGPs) such as endotracheal intubation (ETI) and extubation (3). Other AGPs considered by the Centers for Disease Control and Prevention include open suctioning of airways, sputum induction, cardiopulmonary resuscitation (CPR), noninvasive ventilation (NIV), bronchoscopy, manual ventilation, nebulizer administration, and high-flow oxygen delivery (3–5).

The stability of SAR-CoV-2 and SAR-CoV-1 in aerosols was found to be similar under laboratory conditions (6). In real-life environments, the transmissibility of SARS coronavirus (SARS-CoV)–1 and SARS-CoV-2 was also found to be comparable, as evident by the basic reproduction number (R0) (7–10). This study aims to review the odds of SARS-CoV-1, SARS-CoV-2, and Middle East respiratory syndrome coronavirus (MERS-CoV) transmission from patients to HCWs performing AGPs in the field of anesthetics and critical care (ACC) and the benefits of personal protective equipment (PPE) when performing AGPs.


This systematic review investigated the risks of SARS-CoV-1, MERS-CoV, and SARS-CoV-2 transmissions during common AGPs and the potential benefits of PPE. This review was performed according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement (11) and was registered on International prospective register of systematic reviews (Registration number: CRD42020182298).

Literature Search

A comprehensive literature search was conducted using a combination of keywords (MeSH terms and free text words) including “COVID-19”/“SARS-CoV*”/“SARS”/“MERS,” “Aerosol,” “Operation/procedure,” and “Healthcare workers” (Appendix 1, Supplemental Digital Content 1, MEDLINE, EMBASE, Cochrane Database of Systematic Reviews, and Cochrane CENTRAL were searched up to October 28, 2020. The search was limited to studies from the year of 2003, in line with the SARS outbreak. Only articles or abstracts written in English were included. Additional articles were sought from the reference lists of the included studies.

Selection Criteria

Observational studies including cohort studies and case controls on aerosol transmission of SARS-CoV-2, SARS-CoV-1, and MERS-CoV during common ACC procedures to HCWs were included for quantitative and qualitative analyses. Letter to editors, editorials, commentaries, and expert opinions were excluded. Animal, laboratory, and nonclinical studies were excluded. Table 1 summarizes the Population, Intervention, Control, Outcome and Study design of the study.

TABLE 1. - Population, Intervention, Control, and Outcome of the Review
Population HCWs exposed to SARS-CoV-1, Middle East respiratory syndrome coronavirus, and SARS-CoV-2 in a clinical environment.
Intervention (exposure) Performing AGPs including intubation, noninvasive ventilation, sputum suction, oxygen therapy, bronchoscopy, chest compressions, administering nebulized medications, and tracheostomy, with or without personal protective equipment.
Control (comparator) Not performing AGPs.
Outcomes Number of infections among HCWs, defined by any positive tests including real-time PCR, PCR, serology, and antibody tests.
AGP = aerosol-generating procedure, HCW = healthcare worker, PCR = polymerase chain reaction, SARS-CoV = severe acute respiratory syndrome coronavirus.

Screening and Data Extraction

All articles identified were initially screened by seven independent reviewers (H.H.L.N., L.R., A.T., K.P.T., A.M., J.P.H.L., K.S.C.H), and conflicts were settled by the senior authors (V.W.-S.C., J.Y.-C.T.). Full texts were then retrieved for further independent screening. Finally, a standardized form for data collection was devised to collect data on the transmission of SARS-CoV-1, SARS-CoV-2, or MERS-CoV to HCWs via AGPs in ACC. The baseline characteristics and data on the consistent use of PPE during clinical for each study were also collected.

Data Synthesis and Statistical Analysis

The primary outcome of our study is the odds of SARS-CoV-1, SARS-CoV-2, or MERS-CoV transmission from patients to HCWs via AGPs. Transmission of coronavirus is defined by a laboratory-confirmed diagnosis (via polymerase chain reaction or antibody detection) of coronavirus infection in an HCW after performing an AGP on a patient with confirmed SARS-CoV-1, SARS-CoV-2, or MERS-CoV infection. The secondary outcome of the study aims to explore the use of PPE to mitigate the risk of patient to HCW transmission; this is measured by the odds of SARS-CoV-1, SARS-CoV-2, or MERS-CoV transmission from patients to HCWs when providing general patient care with or without PPE.

Meta-analyses were performed when two or more studies reported the identically defined outcomes. Data were analyzed via Review Manager 5.3 (Cochrane Collaboration, Copenhagen, 2014) and reported as odds ratios (OR), 95% CIs and p values; the random effects model were used. Subgroup differences, defined as a chi-square p value of less than 0.10, were tested between cohort studies and case control studies. As some cohort studies have reported the numbers of infected HCWs (case) and the numbers of uninfected HCWs (control) of each exposure (AGPs or PPE), these studies were analyzed under the case control subgroup. Subgroup analyses were also performed for studies investigating SARS-CoV-1 and SARS-CoV-2 to ensure the two viruses behave similarly during AGPs. Substantial heterogeneity is defined as an I2 value greater than 50% or a chi-square p value of less than 0.10. The Risk of Bias in Nonrandomized Study—of Interventions tool was used to assess the risk of bias in studies included for quantitative analysis (12,13). Robvis software (University of Bristol, Bristol, United Kingdom) was used to produce a risk of bias summary (14).


The PRISMA checklist and flowchart are presented in Appendix 1 (Supplemental Digital Content 1, and Figure 1, respectively. A total of 2,676 records were identified upon literature search. Twenty-three records were sought additionally from the reference lists of the included literature. Two-thousand five-hundred seventy records remained after removing duplicates. Among them, 2,384 were excluded upon initial screening, and 168 were further excluded during full text review. Seventeen of these were included for meta-analysis in which seven reported transmission of SARS-CoV-2, and 10 reported transmission of SARS-CoV-1 to HCWs; no studies reported transmission of MERS-CoV to HCWs (Fig. 1). Supplementary Table 1 (Supplemental Digital Content 1, summarizes the study characteristics of the 17 included studies (15–31). Meta-analyses were performed incorporating both viruses, followed by subgroup analyses by virus type. The risk of bias summary is presented in Appendix 1 (Supplemental Digital Content 1, (Supplementary Fig. 1, Supplemental Digital Content 1,

Figure 1.:
Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow diagram.

EIT and Mechanical Ventilation

A total of 15 studies were identified, eight were reported as cohort studies, and seven as case controls. A total of 4,092 HCWs from a wide range of settings were included. Our meta-analysis suggested a significant increase in odds of HCWs contracting SARS-CoV-1 or SARS-CoV-2 during ETI (OR, 6.69; 95% CI, 3.81–11.72; p < 0.001) when compared with their those not involved in ETI (Fig. 2). In particular, although insignificant, Fowler et al (18) noted that nurses involved in intubation conferred a higher risk compared with physicians.

Figure 2.:
Endotracheal intubation. df = degrees of freedom, M-H = Mantel-Haenszel method.


Six studies involving 1,178 various HCWs administering NIV were identified. The setting and personnel involved in NIV were not reported in most studies. The types of NIV in these studies comprised of noninvasive positive-pressure ventilation: bilevel positive airway pressure (BiPAP) and continuous positive airway pressure (CPAP). In the four cohort studies and two case controls, an increased odd of infection in HCWs administering NIV was found (OR, 3.65; 95% CI, 1.86–7.19; p < 0.001) (Fig. 3).

Figure 3.:
Noninvasive ventilation. BiPAP = bilevel positive airway pressure, df = degrees of freedom, M-H = Mantel-Haenszel method.

Oxygen Therapy

Our meta-analysis of four studies (one reported as cohort study and three as case controls) involving 779 HCWs found that involvement in oxygen therapies did not increase the odds of HCWs contracting SARS-CoV-1 or SARS-CoV-2 (OR, 2.20; 95% CI, 0.44–11.11; p = 0.34) (Supplementary Fig. 2, Supplemental Digital Content 1, Substantial heterogeneity was observed in overall analysis and subgroup analysis for case controls, which might be a result of small sample sizes of included studies.


Four cohort studies and two case control studies had 1,137 HCWs. No significant increase in odds of HCWs contracting SARS-CoV-1 and/or SARS-CoV-2 was found when performing bronchoscopy (OR, 2.04; 95% CI, 0.58–7.15; p = 0.2778) (Supplementary Fig. 3, Supplemental Digital Content 1,

Sputum Suction

Seven studies were identified, with three studies reported as cohorts and four as case controls. Of the 1,145 HCW from varied backgrounds, an overall OR of 1.05 (95% CI, 0.54–2.04; p = 0.89) (Supplementary Fig. 4, Supplemental Digital Content 1, was found, with substantial heterogeneity between included studies. The definitions and systems used for sputum suction were varied: Loeb et al (22) defined sputum suction as suction before and after intubation, Liu et al (21) defined sputum suction by any contact with sputum, Teleman et al (31) investigated suctioning of body fluids, and Chatterjee et al (17) and Heinzerling et al (19) defined sputum suction as any respiratory tract or airway suctioning. Having removed the first three studies from the meta-analysis, heterogeneity no longer existed (p = 0.47), with overall results remaining insignificant (OR, 0.61; 95% CI, 0.33–1.14). Nevertheless, our meta-analysis found no significantly increased odds when performing sputum suction.


One-thousand two-hundred four HCWs from two cohort studies and two case control studies were included. No increased odd was found for HCWs contracting SARS-CoV-1 or SARS-CoV-2 while performing CPR (OR, 2.33; 95% CI, 0.80–6.76; p = 0.12) (Supplementary Fig. 5, Supplemental Digital Content 1, The studies did not state the clinical scenario in which CPR was performed.

Administering Nebulized Medications

Three cohort studies and one case control study cohorts within with a total of 591 HCWs, showed that administering nebulized medications significantly increased the odds of HCWs contracting SARS-CoV-1 or SARS-CoV-2 (OR, 10.03; 95% CI, 1.98–50.69; p = 0.005) (Fig. 4). Notably, Liu et al (20) reported no transmission during this procedure when HCWs are provided with full PPE.

Figure 4.:
Nebulized medications. df = degrees of freedom.

PPE and Infection Control

The meta-analysis of three cohorts and four case controls involving 1,473 HCWs detected a significantly reduced odds of coronavirus infections when N95 masks were used consistently (OR, 0.11; 95% CI, 0.03–0.39; p < 0.01) (Supplementary Fig. 6a, Supplemental Digital Content 1, Although substantial heterogeneity is noted, there are no subgroup differences between cohort studies and case controls, and the direction of effect is consistent. Gowns were reported in nine studies, three were cohort studies and six were case controls. When data from all 3,258 HCWs were pooled, gowning reduces the odds of coronavirus infection amongst HCWs significantly (OR, 0.59; 95% CI, 0.48–0.73; p < 0.01) (Supplementary Fig. 6b, Supplemental Digital Content 1, Similarly, in the nine studies with a total of 2,922 HCWs, a significantly reduced odds of coronavirus infections to HCWs who wore gloves when caring for patients with confirmed SARS-CoV-1 or SARS-CoV-2 infection (OR, 0.39; 95% CI, 0.29–0.53; p < 0.001) (Supplementary Fig. 6c, Supplemental Digital Content 1, Notably, in a study of 420 HCWs in Wuhan, when complete PPE (including N95, medical suit, isolation gown, apron, gloves, eye protection, and hair cover) was used, no HCWs were infected with SARS-CoV-2 despite being involved in AGPs (20). Collectively, the importance of appropriate PPE use is confirmed to reduce transmission of SARS-CoV-1 or SARS-CoV-2 from patients to HCWs.

Results of Sensitivity Analyses Between Studies Performed During SARS-CoV-1 and SARS-CoV-2

Sensitivity analyses were performed on all outcomes to account for potential differences between transmissibility of SARS-CoV-1 and SARS-CoV-2 to HCWs during AGPs. In all outcomes but sputum suction, no significant differences were found between the two group of studies. The potential reason for subgroup differences in sputum suction alone could be a result of the heterogeneity in studies performed during the SARS-CoV-1 epidemic (21,22,31). No included studies described confirmed cases whilst using N95 during AGPs in the current pandemic; hence, subgroup analysis was not possible. All performed subgroup analyses are presented in Supplementary Figures 7–14 (Supplemental Digital Content 1,


Mechanisms of airborne viral particle formation are hypothesized to require surface tension disruption of the respiratory tract lining (32), with shearing forces due to high velocity gas flow and open-closing of terminal bronchiole airways creating viral particles smaller than 5 μm (32). van Doremalen et al (6) investigated the sustainability of SARS-CoV-2 in aerosols and concluded that SARS-CoV-2 have a possible aerosol transmissible nature as with SARS-CoV-1. Our meta-analysis showed that AGPs significantly increase the odds of HCWs contracting SARS-CoV-1/SARS-CoV-2 during involvement in ETI, NIV, and nebulized medications administration; hence, AGPs should only be performed when clinically indicated, and adequate PPE must be worn when performing AGPs.

Brown et al (33) did not support ETI and extubation as AGP as they produce less aerosols than a volitional cough. Our positive results, however, contradicts this, highlighting differences in results between a controlled versus clinical environment. Consensus guidelines suggested early and planned intubation to prevent crash intubation (34); however, the risk of ventilation-induced lung injuries might be increased in these patients (35). Patients should be carefully selected for awake or anaesthetized ETI depending on intubation difficulty (36,37); where necessitated, rapid sequence induction is preferred (36,38). Video laryngoscopy should be used to increase rates of first past successes (37,39).

NIV has not been well established as an AGP (40) but may still pose a risk as exhaled droplets are released into the air when oxygen is delivered through NIV (39,41). Performing NIV has been shown in our meta-analysis to significantly increased odds of HCWs contracting SARS-CoV-1/SARS-CoV-2. The use of entrainment or venturi masks encourages dispersal of contaminated droplets and aerosols (42); hence, the choice of masks must be carefully considered. Expert have suggested a first choice of full-face nonvented mask, with an expiratory viral filter (43). Our meta-analysis found no heterogeneity between aerosol generation of BiPAP or CPAP. When administering NIV, the use of high efficiency particulate air filters and exhalation ports generating round-the-tube airflow are advocated (36).

Our meta-analysis found nebulizing medications administration to increase the odds of HCWs contracting SARS-CoV-1/SARS-CoV-2. The types of nebulizers and the types of patients were not clarified in included studies, but it is still of concern as nebulizing medications are often indicated in COVID-19 patients. Although generated aerosols from nebulized medications are sterile from nonpatient sources (44,45), a recent study by Tang et al (46) showed that significant generation of viral aerosol was possible during simulation. This reemphasizes the need to reconsider nebulizing medications as a potential AGP.

Although we did not detect any increased odds of coronaviruses transmission to HCWs upon sputum suction, bronchoscopy, CPR, and oxygen therapy, these results must be interpreted with care. Some recommendations on performing these procedures include using closed systems during sputum suction (47), using bronchoscopy as last resort for lung collapse (48), and diagnosing with bronchoscopies only if multiple swabs have failed to confirm infection status (48). The clinical scenarios where CPR was performed were unclear from the included studies; hence, chest compression as part of CPR should only be started with full PPE, with defibrillation as a priority (49). When delivering oxygen therapy, nonrebreather masks are the preferred type of masks due to the shortest aerosol dispersing distance (50).

Consistent PPE use was proved to confer HCWs protection against contracting coronavirus; thus, all AGPs should be performed under full PPE and in a negatively pressured room where possible. Liu et al (20) suggested full PPE to include a N95 respirator, medical suit, isolation gown, apron, gloves, eye protection, and hair cover (23). When doffing PPE, it is crucial that the appropriate order of removal is adopted to reduce risk of contamination (51). Double gloving and good hand hygiene in clinical practice have also been proven to reduce the risk of contamination (51–53).

This systematic review is the first to summarize the risk of coronavirus transmission to HCWs via AGPs since the COVID-19 pandemic. A comprehensive analysis of cohort studies, case controls has been covered. There are three further limitations to our study. First, although early in the COVID-19 pandemic, high-quality studies on AGPs and PPE were lacking. As the pandemic has progressed, the steep learning curve allowed HCWs to protect themselves, especially using PPE; this is evident by the studies published well into the pandemic in June by Liu et al (20) and in September by Lentz et al (54). When full PPE was worn, no HCWs performing AGPs contracted SARS-CoV-2 (20). This suggests that the results of our study may not be entirely generalizable as precautions developed overtime. It is difficult to perform high-quality studies during the SARS/COVID-19 pandemic; hence, this review is heavily based on retrospective observational studies. Furthermore, the studies from the SARS epidemic may not be entirely generalizable to the current COVID-19 pandemic clinically. Nonetheless, given the limited data, we hope this review will be informative to future pandemics and epidemics in viruses of similar transmissibility. Finally, coronavirus cases may be underreported due to the lack of testing. This may affect the accuracy of our results. Nonetheless, this review has provided evidence for AGPs and relevance of PPE usage during this critical period. We hope this study provides durable and transferable results helpful in clinical practice.


AGPs such as ETI, NIV, and nebulized medications administration significantly increased the odds of coronavirus infection. From a small number of studies, other AGPs did not show increased risk of coronavirus infection. Despite this, vigilance is demanded when performing these procedures. In order to reduce the odds of COVID-19 infection in HCWs, the use of full PPE must be always encouraged even when there is only a small risk of aerosol COVID-19 exposure.


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    aerosols; coronavirus; critical care; infectious disease transmission; patient-to-professional; intratracheal; intubation; noninvasive ventilation

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