Bioaerosol generation and spread critically governs transmission of several respiratory viruses.1 Bioaerosols are variable-sized infectious fluid particles suspended in air and contain a dose of pathogens. The World Health Organization uses a particle diameter of 5 μm to delineate aerosols into droplet nuclei (≤5 μm) and droplets (>5 μm).2 This distinction is important because the smaller aerosols (<10 μm) are exponentially more likely to stay airborne and infectious.3 Furthermore, bioaerosol size and, thus, transmissibility is also influenced by environmental conditions such as temperature, humidity and air flow. Aerosols containing SARS-CoV-2 (<5 μm) have been found to be stable in an experimental environment for up to 3 hours, with approximated half-life estimates of 1.1 to 1.2 hours.2–5 In addition, the aerodynamic nature of SARS-CoV-2 along with its viral RNA has been reported and detected in air samples of infected individuals through respiration, toileting, and fomite contact.6 These environmental characteristics have also been observed with other respiratory viruses, such as influenza, where up to 89% of virus-carrying particles were less than 4.7 μm.7
There are assumptions being made on whether phacoemulsification should be considered as an aerosol-generating procedure (AGP) or not; however, there is a lack of robust evidence to support or dismiss the concern.8 There have been some experimental reports and videos on visible droplet spray and splatter with phacoemulsification that show the use of a 2.2 mm phacoemulsification tip and hydroxypropyl methylcellulose (HPMC) reduces visible aerosol production.9–12 Once elective services begin to resume at reduced capacity, there will be significant rise in demand for cataract surgery. The challenges will be to address the safety aspects of elective cataract surgery, streamline the services to minimize risk for patients and healthcare workers alike, and eventually reach a stage where capacity is able to meet demand. There have been significant concerns about shortage of personal protective equipment (PPE) across the globe, so it becomes even more important to address the issue of phacoemulsification being an AGP or not and to demonstrate this in a quantitative method.13
It is already known that torsional phacoemulsification produces less cumulative dissipated energy than longitudinal phacoemulsification.14 This experiment was conducted in 2 parts: first to standardize the aerosol measurement processes and second to look at the difference in aerosol production with different phacoemulsification scenarios: with continuous power in longitudinal, torsional, and longitudinal with HPMC settings.
An ex vivo study of phacoemulsification on porcine eyes was conducted at the ophthalmic theater at Sussex Eye Hospital, Brighton & Sussex University Hospitals National Health Service Trust, Brighton, United Kingdom. The hospital research and development department gave formal approval, and the Brighton & Sussex University Hospitals National Health Service Trust Charity (Charity no. 1050864) funded the project. For the consistency of the study, fresh porcine eyes retrieved from local butchers were used within 24 hours of supply. The study was conducted in 2 parts. The first part of the experiment was to assess the efficacy of the particle counter in real-life theater settings with and without using a fit-testing hood (closed environment). The second part of the experiment was to assess the aerosol generation during phacoemulsification with predetermined torsional, longitudinal, and longitudinal settings with HPMC.
Measurement Standardization with the Particle Counter
The TROTEC PC200 (Trotec GmbH) optical particle counter was used because it counts particles measuring less than 10 μm; it was calibrated as per manufacturer instructions before use. Particle counts were recorded at a rate of 2.83 L/min. The time limit for sampling was set at 21 seconds that sampled 0.99 L of air. Particle counts were stored cumulatively in 6 channels with the following nominal diameters: 0.3 μm, 0.5 μm, 1 μm, 2.5 μm, 5 μm, and 10 μm. The values displayed against each channel number depict the number of particles with sizes of 0.3 µm or less, more than 0.3 to 0.5 µm, more than 0.5 to 1 µm, more than 1 to 2.5 µm, more than 2.5 to 5 µm, and more than 5 to 10 μm, respectively. Optical counters have in-built detectors that use light-scattering principles to provide real-time physical information pertaining to particles in the environment. Particle number is determined by the amount of scattered light pulses, whereas the particle size is deduced using the intensity of scattered light.15 Three separate baseline experiments were conducted for calibration and assessment of the particle counter apparatus. Each experiment was performed only after the theater had been empty for a minimum of 20 minutes.
To determine the mean difference between the baseline and after aerosol spray in a closed environment in theater conditions, 5 particle measurements were taken in theater within a qualitative fit-test hood as baseline (Figure 1). After this, 10 puffs of saccharin solution (3 M FT-11 Sodium Saccharin Sensitivity Test Solution), which is a standardized aerosol spray for fit-testing the respirator masks, were sprayed within the fit-testing hood, and another 5 particle measurements were recorded.
To determine the placement of the particle counter for capturing the maximum amount of aerosols, 5 particle measurements were taken in theater with the standard setup as baseline. After this, 5 puffs of nebulized saccharin solution were sprayed from the side 10 cm away from the particle counter, and another 5 particle measurements were taken sequentially and immediately after the spray. The spray was directed to the front of the particle counter from 10 cm distance once, and this was followed by 1 measurement. This exercise was repeated 5 times.
Once the appropriate position of the particle counter was established by the above-described experiment, the layout was finalized as shown in Figure 2A. A simulation head-mold (Philips Studio) was placed at the head end of the patient bed. The particle counter was setup on the body of the bed with its measurement probe pointing toward the head end, 10 cm away from the lateral canthus of the simulation head (Figure 2B). Our theater has a built-in positive pressure ventilation system. In principle, a positive pressure operating theater with adequate air changes could quickly eliminate the virus from the environment, and it has been shown that the risk of cross-contamination from airborne infection is low if staff are adequately protected with appropriate PPE.16
All personnel who were present in theater for the various parts of the study wore a valveless fit-tested FFP3 mask (3M 1863 series) to limit the spread of respiratory aerosols from respiration throughout the experiment. Participating personnel were also instructed to limit movement to a minimum during the experiment and communicate minimally and preferably using sign language rather than talking to reduce aerosol generation.
All particle count measurements were conducted by a designated operator (H.N.). Phacoemulsification was performed by a single surgeon (H.L.) accompanied by a theater nurse, particle counter operator (H.N.), and supervisor (M.A.N.).
The study used the Centurion (Alcon Laboratories, Inc.) phacoemulsification machine. Two sets of parameters were set to find the difference between the aerosol generation with continuous and torsional phacoemulsification (Figure 3A and B): (1) continuous setting using just 80% longitudinal power (no additional torsional power) on panel mode and (2) continuous setting using just 100% torsional power (no additional longitudinal power) on panel mode (Figure 3A and B).
Three separate phacoemulsification experiments were conducted on 15 porcine eyes embedded in the orbit socket of a head mold (Philips Studio). There were 5 preprocedure sequential particle measurements and another 5 acquired during phacoemulsification for each porcine eye. Therefore, a total of 75 measurements were recorded for 15 porcine eyes. The 3 experiments included 5 porcine eyes that underwent phacoemulsification using 80% longitudinal setting only (no torsional) on continuous power mode and 5 porcine eyes that underwent phacoemulsification using 100% torsional setting only (no longitudinal) on continuous power mode (Figure 3A and B). In addition, 5 porcine eyes underwent phacoemulsification using 80% longitudinal setting only (no torsional) on continuous power mode with copious application of HPMC (OcuCoat, Bausch & Lomb, Inc.) on the ocular surface at the start of phacoemulsification.
There was a 20-minute break between the aforementioned 3 experiments. All these experiments (baseline and phacoemulsification) were conducted on a single day to reduce the impact of environmental factors on the theater. The surgeries were performed by a single surgeon (H.L.) using a 2.8 mm standard 2-plane superior incision. The anterior chamber was filled with ophthalmic viscosurgical device, and a paracentesis was created for the second instrument. A phacoemulsification probe with 45-degree Kelman, 0.9 mm TurboSonics, mini-flared ABS tip (Alcon Laboratories, Inc.) was used for all the cases. The phacoemulsification probe was inserted into the anterior chamber and viscoelastic was aspirated. On the signal from the designated operator (H.N.), the surgeon (H.L.) pressed the footswitch to foot position 3 for maximum power. The observer pressed the recording button on the particle counter as soon as the ultrasound probe made the sound of energy dissipation. The surgeon was asked to stop pressing the footswitch once the recording was completed in 21 seconds. For the third experiment, copious amounts of HPMC were applied by the supervisor (M.A.N.) immediately after the start of the ultrasound and the particle counter recording. This process was repeated 5 times for every eye. The recording was saved as a JPEG photograph on a mobile device for future data entry.
Data Analysis and Sample Size
To determine the standard deviation of aerosol on the day of experiment, 30 particle measurements were serially taken by 1 designated operator (H.N.) with a fit-tested FFP3 mask in the theater with a standard setup and positive pressure ventilation without any additional personnel present. The mean and standard deviation (95% CI) for particle sizes of 0.3 µm or less, more than 0.3 to 0.5 µm, more than 0.5 to 1 µm, more than 1 to 2.5 µm, more than 2.5 to 5 µm, and more than 5 to 10 μm were 5654.74 ± 831.50 (5552.35; 5757.14), 1064.29 ± 242.91 (1034.38; 1094.20), 103.77 ± 38.68 (99.01; 108.54), 11.94 ± 6.02 (11.19; 12.68), 1.26 ± 1.09 (1.12; 1.39), and 0.97 ± 0.84 (0.86; 1.07), respectively. As the number of particles for smaller aerosol size was large with potential to induce noise in the data from outliers, any difference ±2 SD was considered to be outside the normal fluctuations.17 These outliers mainly occurred due to theater conditions, including humidity and temperature, dynamically changing throughout the experiment time and, therefore, were excluded.
Because this is the first experiment using the TROTEC PC 200 particle counter, sample-size calculation was planned based on the first part of the study. The aerosol counts 5 µm or less obtained with the saccharin spray directed to the front of the particle counter from 10 cm distance as described earlier were selected for calculating the sample size of porcine eyes required in each phacoemulsification setting groups. The aerosol particle size of 5 µm or less was chosen as per World Health Organization definition of aerosols characterization.2 The cumulative number of particles 5 µm or less after saccharin spray directed to the front of the particle counter increased to 12120 ± 995.5 from 9527.4 ± 171.4. Table 1 describes the breakdown of aerosol counts for various sizes in detail. Based on this difference in means of 2592.6, α of 0.05, and β of 0.05 with power of 95%, the sample size required was 4 eyes in each group. To err on the side of safety and account for any discarded measurements owing to erroneous readings from the particle counter or complications during the surgical procedure, it was decided to have 5 eyes in each group. To make the experiment more robust, 5 measurements were performed for each step for each porcine eye.
All data were entered into an Excel spreadsheet (Microsoft, Corp.), from which the mean and standard deviation were calculated for each measurement. Because the data were normally distributed, a t test was used to compare 2 groups, and a 1-way analysis of variance test was used to compare more than 2 groups of measurements. Finally, all the data from 3 phacoemulsification settings were combined (75 vs 75 measurements) to compare prephacoemulsification and during phacoemulsification aerosol generation for 5 µm or less, more than 5 to 10 μm, and 10 µm or less. A P value less than 0.05 was considered statistically significant.
Measurement Standardization with the Particle Counter
To ascertain the mean difference between the baseline and after aerosol spray in a closed environment in theater conditions, experiments were performed in the contained environment under the fit-testing hood, and significant increase in aerosols after 10 sprays of saccharin solution was found (Table 2). The mean difference noted was 333 292 ± 235 673; 291 742 ± 206 292; 66 661 ± 47 137; 10 073 ± 7122; 1193 ± 843; 316 ± 223 for 0.3 µm or less, more than 0.3 to 0.5 µm, more than 0.5 to 1 µm, more than 1 to 2.5 µm, more than 2.5 to 5 µm, and more than 5 to 10 μm (P < .01), respectively, after aerosol spray (Table 2).
To ascertain the placement of the particle counter for capturing maximum amount of aerosol, experiments were performed in the standard theater environment with normal positive pressure ventilation (without the fit-testing hood), and significant increase was found only in 0.3 µm or less particles (P < .01) with saccharin solution sprayed from the side (Table 3). In the open theater environment with normal positive pressure ventilation (without the fit-testing hood), significant increase in aerosols after 1 spray from the front for particle sizes up to 1.0 µm was found (P ≤ .01) because the saccharin solution is only meant to generate nonvisible aerosol (Table 1).
There was no significant difference between the aerosol counts during phacoemulsification between the 3 groups (P > .01, analysis of variance test) (Table 4). There was no significant difference in aerosol generation of all sizes during each phacoemulsification setting with torsional, longitudinal, and longitudinal with HPMC settings (P > .09, t test) (Table 4). Combining data of all 3 phacoemulsification settings (150 measurements from 15 eyes), there was no significant difference comparing prephacoemulsification and during phacoemulsification for aerosols 5 µm or less (1455 vs 1363.85, P = .60), 5 to 10 μm (1.5 vs 1.03, P = .43), and 10 µm or less (1209 vs 1131.55, P = .60).
Our study had 2 parts. The first part was to assess the efficacy of the TROTEC PC200 particle counter in the dynamic theater environment and its temperature and humidity along with the best position to measure the aerosols during phacoemulsification. The second part was to assess aerosol generation through phacoemulsification. Various commercial systems are available that use the optical principle for particle measurements. To the authors’ knowledge, there are no previous studies measuring theater aerosol counts in ophthalmology using a particle counter such as the TROTEC PC200. Because the theater aerosol environment is constantly changing and is dependent on several factors, we first tested the efficacy of the TROTEC PC200 particle counter in a closed system (within the hood) where the positive pressure ventilation of the theater was less likely to influence the results (Table 2).4,18 Once the efficacy of the particle counter was established, it was important to assess the best position for measuring the aerosol counts with the TROTEC PC200. In the theater environment with positive pressure ventilation, it was expected and evident that the particle counter captured more aerosols when the source of aerosol was facing toward the particle counter (Table 1). The optical particle counter in this experiment showed good efficacy in measuring the aerosols, and there was no significant aerosol generation of 10 μm or less with continuous setting of phacoemulsification in torsional, longitudinal, and longitudinal with the application of HPMC on the surface (Table 4). Furthermore, it is unknown to what extent the SARS-CoV2 viral load is present intraocularly. In addition to this, during phacoemulsification, 0.2 mL of aqueous is exchanged with ophthalmic viscosurgical device, which is then irrigated out before phacoemulsification even commences. Then, there is continuous irrigation with a balanced salt solution. Therefore, any aerosolization that does occur with ultrasound would be of a balanced salt solution infusion rather than of intraocular fluid.
Our study quantifies generation of aerosols measuring 10 μm and less during phacoemulsification. Smaller aerosols that measure less than 10 μm are of special interest because they can stay airborne for longer duration and can reach the lower pulmonary alveoli.18 For example, particles of sizes 0.5 μm and 1 μm will remain airborne for an average of 41 hours and 12 hours, respectively.3 This propensity to stay in air, coupled with extended survival times, can transmit the infective pathogen to secondary hosts directly and indirectly through fomites.3 It is also important to note that relative humidity and temperature of the environment also affect size of these emitted infectious particles.18 Furthermore, it is known that standard surgical masks are only protective for droplets that are more than 5μm, so quantifying small-particle generation during phacoemulsification is paramount because it will have significant implications on the use of respiratory PPE in an ophthalmic theater.19 The latest recommendations by the American Academy of Ophthalmology state that risk of aerosol generation during phacoemulsification and vitrectomy would be low and that standard surgical PPE would suffice.20 Our study findings support this recommendation. Most infectious particles generated from human respiratory sources occur primarily as droplet nuclei, with a diameter of 0.5 to 5.0 μm, and studies have demonstrated the increased risk of SARS transmission with AGP, particularly with intubation.21,22 All these aforementioned factors prompted us to particularly observe generation of smaller size aerosols, those less than 10 μm.
In the literature, AGPs are defined as “any medical procedure that can induce the production of aerosols of various sizes” and include intubation, extubation, suction, nebulizers and noninvasive ventilation, CO2 laser ablation, and high-speed rotating devices.1,2 Other patient-related activities such as toilet flushing, movement of people, and even bed making in a hospital environment have been associated with production of particles of 3 μm or greater.23,24 One cadaveric study, using fluorescein dye, found aerosol generation from routine rhinology procedures with the smallest particle observed to be less than 1 mm in size and found that this could be mitigated with the use of concurrent suction.25 In ophthalmology, some experiments have shown visible droplet aerosol production during phacoemulsification.9,11,12 The smallest particles that are visible are usually around 50 μm.2,26 These visible droplets are not considered as high risk (for transmitting respiratory infections) when compared with droplet nuclei with diameters ranging from 0.5 to 5.0 μm because they are likely to settle in the vicinity of the surgical field because of gravity and are less likely to circulate rapidly with the positive pressure ventilation in the theater.21 Therefore, standard surgical hygiene practices (fluid resistant surgical gowns, surgical masks, draping of patients, and wiping down of the surfaces and potential fomites) and good surgical technique to avoid undue splatter and spray outside the eye during phacoemulsification should mitigate production of the visible droplet production as seen in other experimental models.9–12
The findings of our ex vivo study might suggest that precautionary use of full PPE and microscope drapes might not be necessary for routine phacoemulsification procedure in all patients.27,28 However, we realize that this is the first study of its kind where a particle counter is used to measure the aerosols during phacoemulsification and further in vivo and ex vivo studies using different aerosol counting methods are needed. Currently, because the PPE supply is a challenge in many countries the findings of our study might be welcomed. So, similar to Shih et al.29 we propose slowly resuming cataract surgery at reduced capacity in areas where community transmission is low.
There is a possibility of transmitting the virus from the ocular surface during surgery, which is mitigated with the use of povidone–iodine as it was shown to be effective against SARS-CoV in reducing virus infectivity.30 A previous experimental model suggested frequent use of HPMC to reduce visible aerosol, but our study did not show any difference in nonvisible aerosol even when copious amounts of HPMC was used (Table 4).9
One of the limitations of this study is the use of porcine eyes; however, the results can be extrapolated to human eyes. In addition, we did not measure aerosols larger than than 10 μm because the particle counter used in the study measures cumulative values and gives number of particles up to 10 μm. Similar research is required for other intraocular procedures such as vitrectomy in future. However, as a first quantitative study investigating aerosol production during phacoemulsification, we believe that this study shows that the phacoemulsification procedure does not generate aerosols measuring less than 10 μm.
WHAT WAS KNOWN
- Many nonophthalmic procedures are proven to be aerosol-generating procedures. However, there is a limited amount of evidence or quantification of aerosol generation in phacoemulsification.
WHAT THIS PAPER ADDS
- Optical particle counters can be used for measuring aerosols less than 10 μm.
- Phacoemulsification was not found to be a small-particle aerosol-generating procedure.
- The use of hydroxypropyl methylcellulose did not have an effect on aerosol generation.
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