Introduction
Given that severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) is capable of airborne transmission, Reference Van Doremalen, Bushmaker and Morris1–Reference Adeniran, Mohammed and Muniru4 adequate respiratory protective measures for health care workers are paramount. The clinical area in the back of an ambulance represents a unique environment for health care workers where ambulance staff may spend a prolonged period in this relatively small (∼25 m3), enclosed area with patients. The United Kingdom Health Security Agency (UKHSA; London, UK), formerly known as Public Health England (PHE), have recommended that ambulance personnel should carry out a “dynamic risk assessment” when attending suspected or confirmed coronavirus disease-19 (COVID-19) patients. 5 Additionally, in September 2021, the concept of applying a “hierarchy of controls” to guide personal protective equipment choice was introduced, 6 an approach ordinarily used to manage exposure to occupational hazards. Whilst the classification of respiratory protective equipment (RPE) to be worn in environments involving aerosol generating procedures (AGPs) has been outlined by UKHSA as a Level 3 filtering facepiece (FFP3) mask or a respirator/hood, 6 the general guidance related to mask use for health care workers in non-AGP settings has remained as a Level 2 fluid-resistant surgical mask only (FRSM Type IIR).
There is a perceived importance of events labelled as AGPs in the transmission of viruses and other infectious agents in clinical settings, but the quantitative evidence to support this is lacking. Reference Judson and Munster7–Reference Dhand9 Guidelines relating to AGPs 10 are based on a systematic review Reference Tran, Cimon, Severn, Pessoa-Silva and Conly11 with conclusions drawn from retrospective cohort studies that were all deemed to be of very low-quality. Reference Wilson, Norton, Young and Collins12 It is this evidence, where crucially aerosols were not measured, that has afforded AGPs their special status of an event considered to increase the risk of transmission of an airborne contagion. Reference Wilson, Marks and Eckhardt13
Studies have consistently found that traditional AGPs pose no greater risk than talking or breathing, Reference Hamilton, Arnold and Bzdek14 whilst energetic respiratory events, such as coughing, can generate vastly increased numbers of droplets and aerosols. Reference Bourouiba15 Significantly, recent studies have shown that a cough produces considerably more aerosol particles than numerous defined AGPs Reference Hamilton, Gregson and Arnold2 and yet cough is not classified as being aerosol generating by public health organizations. The UKHSA released updated guidance in January 2022 recommending that health care workers wear FFP3 masks when “caring for patients with a suspected or confirmed infection spread by the airborne route,” 16 but with asymptomatic spread of SARS-CoV-2 widely accepted, Reference Williams, Pan and Decker17–Reference Wölfel, Corman and Guggemos19 this guidance does not go far enough to protect health care workers and reduce disease spread. Therefore, establishing whether a cough from an infected individual within the prehospital environment poses a significant risk to ambulance personnel will alleviate anxiety amongst this staff group and potentially shape future public health guidelines.
This report will outline themes within existing research that will contribute to a better understanding of the risks to health care workers from aerosol emissions produced by a coughing event within the ambulance setting.
Methodology
The research question posed was “Is there a risk to the health care worker, via aerosol transmission, of an acute respiratory infection (ARI) during a coughing event whilst providing care for a patient with an ARI in an ambulance?” The following bibliographic databases were searched: CINAHL Plus (EBSCO Information Services; Ipswich, Massachusetts USA); SCOPUS (Elsevier; Amsterdam, Netherlands); PubMed (National Center for Biotechnology Information, National Institutes of Health; Bethesda, Maryland USA); and CENTRAL (The Cochrane Collaboration; London, United Kingdom). Grey literature was sought by searching specialist databases (OpenGrey [INIST-CNRS – Institut de l’Information Scientifique et Technique; Paris, France] and GreyNet [GreyNet International; Amsterdam, The Netherlands]) as well as key organizations’ websites: World Health Organization (WHO; Geneva, Switzerland), UKHSA, PHE, Resuscitation Council UK (London, UK), European Resuscitation Council (Niel, Belgium), Association of Ambulance Chief Executives (London, UK), International Liaison Committee on Resuscitation, and New and Emerging Respiratory Virus Threats Advisory Group. Methodological filters were not applied. Papers without an English language abstract were excluded from the review (n = 3). This initial search identified 2,405 articles with the breakdown per database detailed via a PRISMA flow diagram in Figure 1. One-hundred sixty-two duplicate publications were removed prior to screening. A total of 2,240 articles were initially screened by title with 2,104 articles removed, and then by abstract seeing 111 articles removed. The 25 remaining articles were assessed for eligibility via full-text review and consequently 20 papers were deemed eligible to be included in the scoping review. Forward and backward citation of key papers identified a further 16 articles that were appropriate for inclusion. The shortlist of 36 papers included in this review form a mixture of simulation studies (n = 16), modelling studies (10), case-control studies (2), literature reviews (2), general reviews (4), and commentary/discussion pieces (2).
Figure 1. PRISMA 2020 Flow Diagram Outlining Search Results and Screening Process of Records Identified by the Literature Search.
Discussion
Cough in Simulated Clinical Settings
Simulation studies have tended to utilize either human volunteers or artificial simulators as the source of cough during experiments. The most applicable study identified from the literature search was performed in a chamber (to model a medical examination room) with a cough simulator used to generate an aerosol-laden cough and aerosol particle counters located at different positions within the room. Reference Lindsley, King and Thewlis20 With the study specifically focused on the aspect of infectious bioaerosols dispersed by patients in a health care environment and the risk to health care workers, aerosol particles with diameters of 0.3µm to 7.5µm were evaluated with results showing that cough-generated aerosol particles became rapidly dispersed throughout the room after just five minutes. As with any cough-simulator, a limitation of using machinery as the cough source is the inability to replicate the impact of buoyancy. Reference Lindsley, King and Thewlis20 The naturally heated human cough plume is usually warmer than the ambient air, hence its buoyancy, and although this may not have a significant impact on larger particles, it is likely to have a significant effect on smaller particle sizes. Reference Lindsley, Reynolds, Szalajda, Noti and Beezhold21 Additionally, cough simulators are unable to replicate the same real-world mechanisms of aerosol generation – primarily being shear stress as airflow meets the mucous membrane, vibration between structures in close proximity, and bronchial fluid burst on terminal airway reopening. Reference Dhand, Jie and Li22
A methodologically similar study to Lindsley, et al Reference Lindsley, King and Thewlis20 investigating the spread of the influenza pathogen during coughing concluded that aerosol transmission likely plays a role in the spread of influenza. Reference Noti, Lindsley and Blachere23 Whether the results of studies looking at a specific pathogen can be generically applied to the airborne transmission of other infections is debatable, but Noti, et al’s Reference Noti, Lindsley and Blachere23 study attempts to quantify infectivity from a coughing event which is relevant to other ARIs. Studies attempting to provide clarity regarding infectivity report the presence of airborne ribonucleic acid when reviewing both influenza and coronaviruses, but they rarely found viable viruses in the air. Reference Shiu, Leung and Cowling24 The SARS-CoV-2 virus has been detected in the air with a half-life of just over one hour, Reference Van Doremalen, Bushmaker and Morris1 and this has numerous citations within the evidence base as proof of “viable” virus. However, Van Doremalen, et al’s Reference Van Doremalen, Bushmaker and Morris1 study was laboratory based with an aerosolized environment created in a Goldberg drum, so it has a significant limitation of not being representative of real-world data. Following initial ambiguity, the UK government now recognizes that SARS-CoV-2 is transmitted via the airborne route, 25 and the research broadly supports this concept. Reference Wilson, Norton, Young and Collins12
Surgical Mask as a Source Control Device during Cough
Face mask efficacy is the primary focus of the human volunteer studies. Air flow leakage is an aspect that is often also reported during these studies where face masks are used as a source control device (ie, being worn by the source of the cough). Of the studies using human volunteers, a significant proportion used the Schlieren technique – a well-established method to visualize the flows of gases and liquids by use of differences in light refraction. Reference Settles26 However, this technique does not provide data on aerosol size, concentration, or mass distribution, so it is limited in inferring risk relating to aerosol transmission. The evidence shows considerable lateral air leakage around a surgical mask, Reference Tang, Liebner, Craven and Settles27–Reference Lindsley, Blachere, Law, Beezhold and Noti30 with differing assertions on whether this effect redirects the jet-stream to a less harmful direction Reference Tang, Liebner, Craven and Settles27 or should be considered as a major hazard for those in the vicinity of the cough. Reference Viola, Peterson and Pisetta28 Researchers agree that a surgical mask is effective as a source control device but there is discrepancy in the degree of effect with a surgical mask recorded as blocking anywhere between 59% Reference Lindsley, Blachere, Law, Beezhold and Noti30 and ∼90% Reference Hamilton, Gregson and Arnold2,Reference Cappa, Asadi, Barreda, Wexler, Bouvier and Ristenpart31 of aerosols produced by coughing. It is noteworthy that the study reporting poorer efficiency used a manikin head and cough simulator to test mask performance. With the UK guidance relating to the COVID-19 pandemic encouraging patients to wear a face mask during transportation in an ambulance, 6 the element of face mask leakage is pertinent when weighing up risk to health care workers in a confined clinical setting such as an ambulance. Significantly, the evidence shows that loose-fitting face masks do not effectively prevent aerosol emissions contaminating the surrounding environment. Reference Leung, Chu and Shiu32
Cough Variation Amongst Individuals
Mathematical modelling studies are increasingly viewed as useful tools in clinical research, with the tendency being to use modelling when systematic reviews fail to adequately answer research questions. The results of modelling studies can be considered indicative with findings often determined by the validity of the primary data applied. The key parameter applied to modelling studies, and that which differs amongst the evidence, is the exhaled microdroplet/aerosol particle distribution and estimated viral copies produced during a cough. Variation amongst individuals has resulted in a “low” and “high” emitter range often being adopted with one modelling study finding that coughing emissions ranged between 0.000277 copies/cm3 (low emitter) to 36,030 copies/cm³ (high emitter) with the PM10 (particle size below 10µm) accounting for approximately one-half of these values. Reference Riediker and Tsai33 The aerosol number produced by a single cough has a range of between 900 to 300,000 particles when measuring aerosols between 0.35-10µm. Reference Lindsley, Pearce and Hudnall34 The SARS-CoV-2 virus is thought to be 60-140nm in size Reference Zhu, Zhang and Wang35 and the virion particles have an affinity to attach to larger particles in the 0.3-10µm range, Reference Ganann, Kitila, Patel, Brook and Pisegna36,Reference Leung and Sun37 so it is entirely plausible that the virus could be contained within particles of the size range associated with aerosols. Riediker and Tsai’s Reference Riediker and Tsai33 study used research based on healthy individuals Reference Yang, Lee, Chen, Wu and Yu38 to form their modelling of microdroplet dispersal and application of previous research in this way highlights a significant flaw that can be directed towards modelling studies as infected individuals are thought to produce a higher concentration of aerosol. Reference Hamilton, Gregson and Arnold2,Reference Lindsley, Pearce and Hudnall34
Aerosol Emissions from Coughing whilst Infected
A case-control study found that particles per cough in infected (influenza) versus non-infected participants were reported as 75,400 and 52,200, respectively. Reference Lindsley, Pearce and Hudnall34 The study reported particle size distribution for one participant considered to be a high emitter, displaying a generic increase in all size ranges when infected. This type of analysis would be particularly useful for the SARS-CoV-2 pathogen due to the inhibitory impact the virus has on surfactant production caused by the virion binding to ACE2 receptor sites and subsequently infecting and damaging Type II alveolar cells. Reference Piva, Diblasi and Slee39 Surfactant acts to reduce alveolar surface tension and is known to increase aqueous elasticity. Reference Johnson and Morawska40 In application to the SARS-CoV-2 infection, bronchiole fluid film burst may occur more frequently and at smaller diameters generating a larger volume of aerosols in the lower particle size range.
Although noting some significant limitations relating to reporting bias, Hamilton, et al Reference Hamilton, Arnold and Bzdek14 cites a similar theme regarding aerosol particle number concentration from coughing when infected with SARS-CoV-2 as to that highlighted for influenza by Lindsley, et al. Reference Lindsley, Pearce and Hudnall34 Hamilton, et al Reference Hamilton, Arnold and Bzdek14 recruited hospitalized COVID-19 patients as a case cohort (n = 8) alongside a control cohort (n = 25) of healthy volunteers. Using optical and aerodynamic particle sizers, the volunteers underwent protocolized procedures, including coughing. The environment in which the research was carried out also represented a significant limitation, differing between the groups due to logistical constraints with an ultra-clean laminar flow operating theatre used for healthy volunteers and a negative pressure ventilated room used for hospitalized volunteers. Nevertheless, the study concluded that aerosol number concentration was higher during cough for the infected volunteers.
Limitations
The literature search has failed to identify research that answers the initial research question posed. Whilst this is not a limitation in itself, the report discusses themes identified only within research that underwent full-text review as part of a screening process related to the posed research question.
Conclusion
There is no unequivocal evidence to determine if public health guidelines are adequate in reducing the risk of exposure to SARS-CoV-2 for ambulance staff in the presence of infected patients. A limited number of studies have attempted to model the risk of transmission of airborne viruses to health care workers during a coughing event, but not within the confines of an ambulance. On balance, current information suggests that face masks may reduce the risk of infection, but there remains uncertainty due to mask leakage and lateral jet flows created by loose fitting surgical masks. It is clear that further research to establish quantitative risks to health care workers from aerosol emissions during a coughing event in an ambulance setting is required. Future research should aim to provide an evidence base from which appropriate RPE levels for health care workers exposed to a coughing patient can be determined.
Conflicts of interest
The authors report there are no competing interests to declare.
Acknowledgments
Thank you to Sarah Jardine for her feedback and subsequent direction of the initial literature search.
Open access
