A quantitative evaluation of aerosol generation during supraglottic airway insertion and removal

Many guidelines consider supraglottic airway use to be an aerosol‐generating procedure. This status requires increased levels of personal protective equipment, fallow time between cases and results in reduced operating theatre efficiency. Aerosol generation has never been quantitated during supraglottic airway use. To address this evidence gap, we conducted real‐time aerosol monitoring (0.3–10‐µm diameter) in ultraclean operating theatres during supraglottic airway insertion and removal. This showed very low background particle concentrations (median (IQR [range]) 1.6 (0–3.1 [0–4.0]) particles.l−1) against which the patient’s tidal breathing produced a higher concentration of aerosol (4.0 (1.3–11.0 [0–44]) particles.l−1, p = 0.048). The average aerosol concentration detected during supraglottic airway insertion (1.3 (1.0–4.2 [0–6.2]) particles.l−1, n = 11), and removal (2.1 (0–17.5 [0–26.2]) particles.l−1, n = 12) was no different to tidal breathing (p = 0.31 and p = 0.84, respectively). Comparison of supraglottic airway insertion and removal with a volitional cough (104 (66–169 [33–326]), n = 27), demonstrated that supraglottic airway insertion/removal sequences produced <4% of the aerosol compared with a single cough (p < 0.001). A transient aerosol increase was recorded during one complicated supraglottic airway insertion (which initially failed to provide a patent airway). Detailed analysis of this event showed an atypical particle size distribution and we subsequently identified multiple sources of non‐respiratory aerosols that may be produced during airway management and can be considered as artefacts. These findings demonstrate supraglottic airway insertion/removal generates no more bio‐aerosol than breathing and far less than a cough. This should inform the design of infection prevention strategies for anaesthetists and operating theatre staff caring for patients managed with supraglottic airways.


Introduction
The COVID-19 pandemic caused by SARS-CoV-2 continues to have a huge global impact. Direct droplet and indirect contact transmission are still regarded as important modes of SARS-CoV-2 spread. However, airborne transmission by aerosol particles of respirable size is of great concern [1][2][3][4][5].
Aerosol-generating procedures are specific patient care activities designated as carrying a higher risk of viral transmission via the airborne route [10], and are presumed to generate aerosols from the respiratory tract. The evidence on which current aerosol-generating procedures are defined has been mostly epidemiological, from retrospective cohort and case-controlled studies of transmission during the SARS pandemic in 2003 [11,12].
These studies identified an association between certain medical procedures and the likelihood of healthcare workers involved contracting SARS. Increased risk of transmission was identified for tracheal intubation, noninvasive ventilation, tracheostomy and facemask ventilation (OR 6.6, 4.2, 3.1 and 2.8, respectively) [12].
The WHO has developed a list of aerosol-generating procedures [13] that healthcare organisations throughout the world have used as a framework for development of their guidelines [14,15]. To date, few published data reported the amount of aerosol produced by any of the currently defined anaesthetic aerosol-generating procedures. This has now been rectified with the introduction of aerosol measurements within operating theatres during putative aerosol-generating procedures.
Two groups have quantitated the degree of aerosol generated during tracheal intubation and extubation [16,17]. Our group identified that intubation and extubation generate considerably less aerosol than a single voluntary cough and has, therefore, questioned whether these airway management interventions should still be classified as highrisk aerosol-generating procedures [16,18]. As such, the risks from aerosol generated during airway management, and the optimum methods of preventing transmission, remain under debate.
Supraglottic airways are used in the majority of the approximately 2.7 million general anaesthetics performed in the UK each year [19]. In a UK survey in October 2020, 40% of responding hospitals reported that supraglottic airway removal, even in low COVID-19 risk pathways, is restricted exclusively to the operating theatre (rather than being performed in a recovery area), indicating the presence of policies that assume it is an aerosol-generating procedure [20]. Designation of a procedure as aerosolgenerating not only alters personal protective equipment worn by staff but also impacts operating theatre efficiency, as a fallow period is required to allow aerosol clearance after the procedure is conducted [21]. These precautionary measures have led to reduced operating theatre efficiency, with many operating at <75% of normal activity levels. The UK National Health Service (NHS) surgical waiting lists have grown substantially with over 385,000 patients currently waiting more than a year for planned surgery and a backlog in excess of 5 million surgical cases [22]. The designation of anaesthetic airway procedures as aerosol-generating has, therefore, an important impact on hospital operational efficiency, cost and the challenge of reducing surgical waiting lists.
Uncertainty remains as to whether insertion or removal of a supraglottic airway generates aerosols [23]. A recent consensus statement (based on expert opinion) suggested straightforward insertion of a supraglottic airway was unlikely to generate an increase in aerosol but noted a lack of evidence to support this conclusion. However, the statement also recommended supraglottic airway use be classified as an aerosol-generating procedure if airway suctioning, facemask ventilation, multiple attempts or conversion to tracheal intubation were required [24]. This statement needs to be reassessed in light of recent evidence indicating that tracheal intubation and associated facemask ventilation do not generate increased levels of aerosols [16]. Given the uncertain balance of potential risks and benefits associated with the protective strategies put in place to limit airborne viral transmission, we aimed to directly assess airborne particle emission during insertion and removal of supraglottic airways. We used real-time measures of aerosol generation with an optical particle sizer in a working operating theatre environment and compared the measured levels with reference to those generated by a volitional cough and the patient's own breathing. Aerosol particles were sampled with an optical particle sizer (TSI Incorporated, model 3330, Shoreview, NM, USA).

Methods
This reports the particle number concentration and optical size distribution within the diameter range 300 nm to 10 µm   0.001, Fig. 2c). The four supraglottic airway removals with the highest detected aerosol particle counts (ranging from 19 to 51 particles) each produced < 50% of the particle count sampled during an average volitional cough. Only one cough was noted during the removal sequences, this occurred with the anaesthetic facemask tightly applied to the patient by the anaesthetist and no increase in aerosol was detected.
In one patient, the first attempt at supraglottic airway insertion failed to produce a patent airway, the supraglottic airway was removed and a different size device inserted.
This insertion sequence was associated with increased particle generation: a total of 114 particles were detected.
No coughing was noted but after the first insertion attempt there was a period of unsuccessful ventilation (due to a large leak); the anaesthetic trainee removed the supraglottic airway and moved position to allow the senior anaesthetist to insert a larger supraglottic airway. The increase in aerosol occurred after the initial failed insertion during the process of removal, not during manual ventilation (Fig. 1d). This spike of aerosol had a similar time-course to a cough, but the aerosol produced had a different size profile with substantially fewer small particles (<1 µm) (Fig. 1d). Of note, contemporaneous with these events, the patient's head was  being of respiratory origin. These size distributions also resembled the aerosol particle spike associated with the failed supraglottic airway insertion and subsequent removal (Fig. 1d). The three supraglottic airway removal sequences with these unattributed aerosol events were those with the highest levels of aerosol generation and these singular events accounted for most of the increase above background.
In trying to identify the source of the unattributed aerosol events, we discovered several potential nonrespiratory sources of airborne particles including tying ribbon gauze to secure the airway device ('tube-tie'); opening different types of woven gauze; opening a throat pack; manipulation of a pillow; and the scrunching of scrub tops. These materials generated particle size distributions that were strikingly different to coughs but were similar to the five unattributed aerosol events (Fig. 3) with a clear predominance of particles of a larger size (> 1 µm).

Discussion
This study demonstrates that uneventful insertion and removal of a supraglottic airway generates no more aerosol than tidal breathing in the same patient and far less aerosol than a single volitional cough. As such, the routine, uncomplicated use of supraglottic airways does not appear to carry an increased risk of generating aerosol and, on this basis, does not meet the criterion to be classified as an 'aerosol-generating procedure' [14,15]. This is in keeping with other studies undertaken by our group investigating the amount of aerosol generated from currently defined aerosol-generating procedures. These medical procedures, including tracheal intubation and extubation, non-invasive ventilation, tracheostomy and use of high-flow nasal oxygen, do not generate aerosol levels greater than natural patient respiratory events [16,18]. These findings support existing guidance that the choice of airway and management strategy should not be made on the basis of perceived aerosol risk but rather should be informed by quantitative data [24].
Previous work has identified that bio-aerosols (of particle size <20 µm) originating from natural respiratory events, such as breathing, speaking, coughing or singing, display two overlapping size distributions [26]. This has been postulated to reflect their site of origin arising from either the lower respiratory tract or vibrations in the larynx [27]. The overall respiratory particle size distribution consistently reports the highest concentration of particles in the sub-micron range [16,26,[28][29][30], which is in agreement with the size distribution of the respiratory aerosols recorded in this study. procedures (or events) and respiratory particle emissions.
These study features provide confidence that nonrespiratory aerosol sources (artefacts) are identified and excluded as confounds in analysis.
Our study is the result of an ongoing collaboration between aerosol scientists and clinicians using an established methodology [16]. All recordings were undertaken in an ultraclean operating theatre, with a very low background particle count, essential for the resolution of respiratory events. Additionally, subject paired measurements of supraglottic airway insertion and removals along with baseline tidal breathing, used as a reference, minimised the effect of inter-person variability which is typically a challenge for studies of bio-aerosols. This has enabled meaningful comparisons to be made with recordings from a relatively small sample of patients.
Detailed patient level information was not collected, reflecting the specific consent given for the project which did not include collection of patient characteristics. A further, larger study would be required to extend our results to assess the influence of specific type of supraglottic airway, anaesthetic technique (e.g. spontaneous vs. mechanical ventilation) or surgical indication.
We carried out sampling using a funnel placed 50 cm in front of the patient's face in order not to interfere with anaesthetic care and to enable our results to be compared with a previous intubation study [16]. It is possible that sampling at this distance missed small quantities of aerosol generated during supraglottic airway insertion or removal but, to place this limitation in context, we were able to reliably detect bio-aerosols from breathing at this distance.
We used a volitional cough from one of the investigators (a healthy volunteer with no respiratory disease) to provide a reference standard. We acknowledge there may be advantages to using the patient's own cough as a reference, in the same way we have for tidal breathing, as this will also take account of inter-subject variation in aerosol production. It is worth noting that analysis of the particle concentrations for the coughs used in this study shows that they fall well within the distribution of the large database of coughs from multiple individuals we have acquired as part of the AERATOR study. It is likely that a healthy volunteer will generate less aerosol than an individual with an acute respiratory illness, therefore using a volunteer cough as a reference is likely to represent a more stringent threshold against which a procedure can be identified as having a low risk of aerosol generation.
Our study suggests uneventful supraglottic airway insertion and removal is not associated with increased levels of bio-aerosol and, to place this in a relative risk context, is no different to the aerosol generated by a patient's tidal breathing and is considerably lower than a volitional cough.
On this basis, we believe supraglottic airway insertion and removal should not be considered an aerosol-generating procedure.