As more cases of COVID-19 present in healthcare facilities worldwide, there seems to be some confusion as to what constitutes an aerosol-generating procedure. Turning up to work is not without risk, with a large number of healthcare workers in Italy and Ireland diagnosed with COVID-19. There is a case report of asymptomatic carriage lasting up to 16 days, so we need to be careful whether the child in front of us has been diagnosed with COVID-19 or not.
Much of our data comes from the 2003 SARS epidemic and the H5N1 influenza outbreaks. There are always going to be a number of confounding variables when looking at these reports—whether the HCW was wearing appropriate PPE (or had access to it), how good their hand-washing was, and how close together patients are—but nosocomial infections do occur.
First, we will examine what an aerosol is and how aerosols and droplets relate to some common and uncommon things we do in paediatrics.
Aerosol or droplet?
Let’s define some terms before we get started—it turns out it’s not as easy as it sounds.
A respiratory droplet is a fluid bundle of infectious particles that travels from the infected individual’s respiratory tract onto another’s mucosal surface rather than floating down the respiratory tract. Small droplets are between 5-20μm and tend to hang up around the glottis. Large droplets are > 20μm and are probably too big to follow airflow. They tend to obey the laws of gravity and so settle on nearby surfaces when you sneeze.
You can transmit the infection if you inadvertently touch the same surface and then touch your face. This is why we wash our hands. In healthcare, droplet precautions include a surgical mask, eyewear, disposable gown, and gloves. The surgical mask is a physical barrier to droplets too large to be inhaled.
A droplet nucleus is what is left once the liquid rapidly evaporates from a droplet. They are in the order of 10μm in diameter and are in the respirable range. This is generally defined as any particle less than 10μm. The inspirable range is defined as anything between 10 – 100μm in size
An aerosol is a liquid (or solid) suspended in the air – think mist and fog. These small particles are less than 5μm and are in the respirable range (rather than the inspirable range like droplets) and can enter the lower respiratory tract. They are affected by diffusion rather than gravity, so they hang around for a while. Measles is one such airborne disease. A recent letter in the NEJM suggests that SARS-CoV-2 can remain viable in aerosols for at least 3 hours. However, the WHO’s guidance is clear that it should be managed with droplet and contact precautions UNLESS you are performing an aerosolising procedure.
Consider them on the continuum of aerosol -> small droplets -> large droplets -> puddles. Aerosols and small droplets can travel fair distances, especially if powered by a blast of oxygen or expired air. Larger droplets tend to obey the laws of gravity and settle on surfaces.
Just breathing, coughing and sneezing
However, even putting an oxygen mask on the patient may not protect you. Hui et al. (2006) used fancy laser beams and smoke to detect how far a single breath might travel.Â
With a standard oxygen mask on the patient, a flow rate of 4l/min, a tidal volume of 500mls, and 12 breaths a minute, the smoke plume travelled approximately 0.45m. In most experiments, scientists use smoke as a stand-in for the more nebulous breath of air. Non-biological aerosols will behave differently depending on the airflow and ventilation in the room and have a constant density. Mathematical modelling would suggest that the further from the source a sample is taken, the lower the potential infectivity until a state of equilibrium is reached. Fortunately, the air is exchanged in most hospital rooms regularly.
A patient coughing and sneezing can produce large, short-range droplets and small, long-range aerosols. The aerosols produced by coughing are heavier than the smoke used in experiments, so hopefully, they will not be able to travel as far. Experimental data will tend to overestimate the spread of droplets.
Thompson et al (2013) took 99 air samples around presumptive AGPs. 26.1% of them contained viral RNA. But the baseline level of contamination, when no AGPs (as defined by WHO 2009) were performed was 10.5%. Just because a procedure might generate an aerosol, it does not hold that the aerosol can cause an infection.
Most of our data comes from the fast SARS-CoV epidemic in 2002-2003. Tran et al. searched for all papers on HCW infection and aerosol-generating procedures. They found 10 – 5 non-randomized cohort studies and five retrospective cohort studies. They then created pooled estimates of odds ratios.
Judson and Munster usefully categorized AGPs into those that mechanically create and disperse aerosols and those that make the patient wriggle and cough. Or you could think of them, as suggested by Brewster et al. (2020), as those procedures that require gas flow and those that require no extrinsic gas flow.
Bag-valve-mask ventilation and CPR
High risk
A paediatric cardiac arrest is uncommon. When it occurs, your first move* should be to open the airway and provide rescue breaths. During COVID-19, I doubt anyone will be doing mouth-to-mouth/nose ventilation. They are going to reach for an appropriately sized bag-valve mask. Just like when placing a standard oxygen mask, there is a transverse movement of droplets even with a reasonable seal. The addition of an HME filter appears to attenuate some of this, as Chan et al.(2018) demonstrated.
Adult CPR guidelines are advocating for chest compression-only CPR in the community and rapid intubation pre-compressions if circumstances allow. There has been little guidance on paediatric CPR from the ALSG, but several enterprising teams are looking at it.
Possible cases of SARS transmission by CPR have been reported (Christian et al. 2004), but BVM ventilation took place during the cases, and this may be the most important factor for possible viral transmission.
Intubation
High risk
Anything where the clinician is inches away from the patient’s respiratory tract is going to be a high-risk procedure. There have been huge collaborative efforts worldwide to create COVID-19 intubation algorithms, which share many similarities.
- The most experienced operator performs the procedure – this is not a time for learning.
- No bag-valve-mask ventilation before intubation
- Use of videolaryngoscopy to maximize the distance between the intubator and the patient
- Minimum number of staff present
This is my favourite paediatric intubation resource from Queensland Children’s Hospital.
Nebulizing a medication
High risk / Unclear evidence
There are few indications for nebulizing medication. Bronchodilators are best delivered by MDI and spacer when possible, but in cases of severe asthma or, more commonly, in croup, a nebulizer chamber may be the way to go. The UK guidelines do not consider the delivery of nebulized medications as an AGP. The rationale is that the aerosol is derived from a non-patient source. Even if they have the disease, the medication sticks to the mucus membranes and will not get released into the general environment. There seems to be a lack of global consensus on this.
Nebulizers generate small particles, between 1 and 5 microns in diameter, to get down into the bronchioles and not just be deposited in the oropharynx. Viable COVID-19 viral RNA has been detected in aerosol form 3 hours after delivery by nebulizer in experimental conditions, but this does not prove infectivity, just infectious potential.
In 2009, O’Neill et al. performed air sampling studies for common patient activities, including making the bed and providing nebulized therapy, as well as some more invasive treatments (bronchoscopy and suctioning). Although in small numbers, they found an increase in influenza particle numbers (from baseline) of up to 70,000/cm³.
High Flow Nasal Cannula
High risk
In adult practice, high-flow oxygen delivery is anything over 6l/min. In paediatrics, it is 2l/kg/min up to the adult maximum of 60l/min. In one of my favourite studies to date (and certainly in keeping with the DFTB ethos), five anaesthetists gargled 10mls of red food dye, inhaled to their vital capacity and then coughed. They then repeated the experiment using blue food dye and HFNC at 60l/min and compared the distance travelled. They showed a baseline cough distance of 2.48m, increasing to 2.91m with high flow. Of course, children have a much smaller vital capacity.
This contradicts the data from Hui et al. (2019). They used a human-patient-simulator (as opposed to humans in the above study), smoke and lasers. With a properly fitted mask, forward flow was increased to ~26 cm with 5cm of CPAP and to around 33cm with 20cm of CPAP. With HFNC, the exhalation distance increased from 6.5cm (10l/min) to ~17cm (60l/min). When the mask became loose or disconnected, smoke was detected up to ~62cm laterally. So why is there a big difference in the studies? It is the cough that causes the problem.
This Sick Kids in Toronto video says more than any words ever could.
Whether you believe in the benefits of high-flow or not, pushing oxygen through the nose at 2l/kg/min and out through the mouth can create an aerosol spread of snot and virus. We would advise that it only be used when low-flow oxygen therapy fails. It also makes sense, then, that it should only be started where the patient will end up. It would not be wise to start a patient on HFNCO2 and then wheel them through the hospital, leaving a cloud of viral particles in their wake like some overactive Bisto Kid. If you are going to do it with a coughing patient, then it would be sensible to put a standard face mask on first.
Non-invasive ventilation (CPAP or BiPAP)
High risk
In many cases, high-flow nasal cannula seems to have superseded non-invasive ventilation, though CPAP is regularly used in neonatal practice. There is very little evidence for maternal transmission of COVID-19, and one might suppose that full PPE is then not warranted. However, you need to consider where the baby has come from.
Open suctioning and chest physiotherapy
High risk
Removal of nasal foreign body
Medium to high risk
There are many ways to remove a nasal foreign body, but all of them will generate snot. The old standby—the mother’s kiss—is, realistically, no more dangerous for the parent than living in close proximity. If your pre-encounter probability of infection with SARS-CoV-2 is low, i.e., there is little community transmission, then the risk to the provider is probably low.
Nitrous oxide
Medium to high risk
Respiratory illness is a contra-indication to nitrous sedation, but given that there is a degree of asymptomatic carriage, we might need to use it. With children not going to school and being told to stay away from their friends, there will be a spike in trampoline and bunk-bed-related injuries. Again, consideration should be made regarding the possibility of community transmission. Logically, holding a continuous flow mask on an uncooperative toddler would expose an HCW to higher risk than being a room Sith a cooperative patient using a demand system with appropriately attached to suction.
Examining the throat
Medium to high risk
In normal times, no paediatric examination is complete without looking in the ears, nose, and throat, no matter how hard it might be. You can argue that looking at tonsils might not be overly helpful, given that the inter-rate variability is pretty high, but there are other things to look for, too – emerging teeth, Koplik spots, ulcers. But does a look in the throat put us at risk?
The Royal College of Paediatric and Child Health concurs and, in a statement released on March 24th, suggests that we only look in the throat if it is essential. If we have to do it, we should be wearing appropriate protection (glove, gown, surgical face mask). If a child is at particularly high risk, they recommend empiric antibiotics.
Even ENT experts, like Eric Levi, recognize the unique risks that fiddling around near the upper respiratory tract hold.
Inserting a nasogastric tube
Medium to high risk
The combined Colleges of Surgeons of Great Britain and Ireland suggest that inserting a nasogastric tube in an adult is an AGP, probably as it may induce coughing.
Taking a nasopharyngeal swab
Low to moderate risk
The CDC states that collecting a nasopharyngeal swab doesn’t need to take place in an isolation room but should at least be performed in a single room with a closed door. The health care practitioner should wear an N95 mask or equivalent, coupled with eye protection, gloves, and a gown. Given how far the swab has to travel up the nasopharynx, nobody should be surprised that it might make someone sneeze.
The current Australian guidance contains slightly different advice.
 We can also add IV access, suprapubic aspiration and performance of a lumbar puncture to this list of LOW-risk procedures.
And let’s not forget our surgical and dental colleagues
Surgical procedures
Some surgical procedures are more dangerous than others. Eric Levi advocates for a risk assessment before any procedure takes place, starting with ‘Does it need to be done now?’ Take a look at his post on how he is modifying his operative technique to reduce risk to himself and his colleagues.
On March 25th, the combined Colleges of Surgeons of Great Britain and Ireland recommended against laparoscopic surgery due to the potential for aerosol formation. Endoscopy, at either end, also has the potential for the creation of fomites and aerosolizing droplets and so should be carried out with extreme caution.
Dental procedures
Very few dental procedures need to be performed as an emergency, but given that high-speed drills can lead to aerosolization, we must care for our dental colleagues who may also be exposed in the course of duty.
The guidance for these procedures is common sense. Don’t perform them if you don’t have to. This is not the time for some minor dental procedures. If they have to be carried out, they should happen in the appropriate space with the appropriate staff. This means in a single room (ideally) with the minimum number of staff wearing appropriate PPE.
These are our thoughts based on the current evidence, and we’d love you to persuade us otherwise in the comments below.
*Clearly the first step of the algorithm is D for Danger. That means putting on your PPE.
Selected references
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Brewster DJ, Chrimes NC, Do TB, Fraser K, Groombridge CJ, Higgs A, Humar MJ, Leeuwenburg TJ, McGloughlin S, Newman FG, Nickson CP. Consensus statement: Safe Airway Society principles of airway management and tracheal intubation specific to the COVID-19 adult patient group.
Brown JS, Gordon T, Price O, Asgharian B. Thoracic and respirable particle definitions for human health risk assessment. Particle and fibre toxicology. 2013 Dec 1;10(1):12.
Davies A, Thompson G, Walker J, Bennett A. A review of the risks and disease transmission associated with aerosol generating medical procedures. J Infect Prev 2009; 10:122–6.
van Doremalen N, Bushmaker T, Morris D, Holbrook M, Gamble A, Williamson B, Tamin A, Harcourt J, Thornburg N, Gerber S, Lloyd-Smith J. Aerosol and surface stability of HCoV-19 (SARS-CoV-2) compared to SARS-CoV-1. medRxiv. 2020 Jan 1.
Hui DS, Ng SS. Recommended hospital preparations for future cases and outbreaks of novel influenza viruses. Expert Review of Respiratory Medicine. 2020 Jan 2;14(1):41-50.
Hui DS, Ip M, Tang JW, Wong AL, Chan MT, Hall SD, Chan PK, Sung JJ. Airflows around oxygen masks: A potential source of infection. Chest. 2006 Sep 1;130(3):822-6.
Kam KQ, Yung CF, Cui L, Lin Tzer Pin R, Mak TM, Maiwald M, Li J, Chong CY, Nadua K, Tan NW, Thoon KC. A well infant with coronavirus disease 2019 (COVID-19) with high viral load. Clinical Infectious Diseases. 2020 Feb 28.
Liu Y, Ning Z, Chen Y, Guo M, Liu Y, Gali NK, Sun L, Duan Y, Cai J, Westerdahl D, Liu X. Aerodynamic Characteristics and RNA Concentration of SARS-CoV-2 Aerosol in Wuhan Hospitals during COVID-19 Outbreak. bioRxiv. 2020 Jan 1
Macintyre CR, Seale H, Yang P, Zhang Y, Shi W, Almatroudi A, Moa A, Wang X, Li X, Pang X, Wang Q. Quantifying the risk of respiratory infection in healthcare workers performing high-risk procedures. Epidemiology & Infection. 2014 Sep;142(9):1802-8.
Noti JD, Lindsley WG, Blachere FM, Cao G, Kashon ML, Thewlis RE, McMillen CM, King WP, Szalajda JV, Beezhold DH. Detection of infectious influenza virus in cough aerosols generated in a simulated patient examination room. Clinical Infectious Diseases. 2012 Jun 1;54(11):1569-77.
Seto WH. Airborne transmission and precautions: facts and myths. Journal of Hospital Infection. 2015 Apr 1;89(4):225-8.
Shiu EY, Leung NH, Cowling BJ. Controversy around airborne versus droplet transmission of respiratory viruses: implication for infection prevention. Current opinion in infectious diseases. 2019 Aug 1;32(4):372-9.
Somogyi R, Vesely AE, Azami T, Preiss D, Fisher J, Correia J, Fowler RA. Dispersal of respiratory droplets with open vs closed oxygen delivery masks: implications for the transmission of severe acute respiratory syndrome. Chest. 2004 Mar 1;125(3):1155-7.
Tang JW, Li Y, Eames I, Chan PKS, Ridgway GL. Factors involved in the aerosol transmission of infection and control of ventilation in healthcare premises. J Hosp Infect 2006;64:100-14.
Tellier, R., Li, Y., Cowling, B.J. et al. Recognition of aerosol transmission of infectious agents: a commentary. BMC Infect Dis 19, 101 (2019). https://doi.org/10.1186/s12879-019-3707-y
Thompson KA, Pappachan JV, Bennett AM, et al. EASE study consortium. Influenza aerosols in UK hospitals during the H1N1 (2009) pandemic–the risk of aerosol generation during medical procedures. PLoS One. 2013;8:e56278.
World Health Organization. Infection prevention and control during health care when novel coronavirus (‎‎‎ nCoV)‎‎‎ infection is suspected: interim guidance, January 2020. World Health Organization; 2020
Intubation
Cheung JC, Ho LT, Cheng JV, Cham EY, Lam KN. Staff safety during emergency airway management for COVID-19 in Hong Kong. The Lancet Respiratory Medicine. 2020 Feb 24.
Nebulizing a medication
O’Neil CA, Li J, Leavey A, Wang Y, Hink M, Wallace M, Biswas P, Burnham CA, Babcock HM. Characterization of aerosols generated during patient care activities. Clinical Infectious Diseases. 2017 Oct 1.
Amirav I, Newhouse MT. RE: Transmission of Corona Virus by Nebulizer-a serious, underappreciated risk!.
High Flow Nasal Cannula
Hui DS, Chow BK, Lo T, Tsang OT, Ko FW, Ng SS, Gin T, Chan MT. Exhaled air dispersion during high-flow nasal cannula therapy versus CPAP via different masks. European Respiratory Journal. 2019 Apr 1;53(4):1802339.
Leung CC, Joynt GM, Gomersall CD, et al. Comparison of high-flow nasal cannula versus oxygen face mask for environmental bacterial contamination in critically ill pneumonia patients: a randomized controlled crossover trial. J Hosp Infect. 2019;101(1):84–87.
Loh NH, Tan Y, Taculod J, Gorospe B, Teope AS, Somani J, Tan AY. The impact of high-flow nasal cannula (HFNC) on coughing distance: implications on its use during the novel coronavirus disease outbreak. Canadian Journal of Anesthesia/Journal canadien d’anesthésie. 2020 Mar 18:1-2.
Non-invasive ventilation
Singh A, Sterk PJ. Noninvasive ventilation and the potential risk of transmission of infection. European Respiratory Journal. 2008 Sep 1;32(3):816-.
Bag-Valve-Mask Ventilation
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Suctioning
Inserting a nasogastric tube
Nitrous oxide
Taking a naso-pharyngeal swab
Examining the throat
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Removal of foreign bodies
Surgical spread
Ong J, Cross GB, Dan YY. The prevention of nosocomial SARS-CoV2 transmission in endoscopy: a systematic review of recommendations within gastroenterology to identify best practice. medRxiv. 2020 Jan 1.
Dental spread
Divya R, Senthilnathan KP, Kumar MP, Murugan PS. Evaluation of aerosol and splatter contamination during minor oral surgical procedures. Drug Invention Today. 2019 Sep 1;12(9).
Sabino-Silva R, Jardim AC, Siqueira WL. Coronavirus COVID-19 impacts to dentistry and potential salivary diagnosis. Clinical Oral Investigations. 2020 Feb 20:1-3.
Would you consider breathing through masks, such as low grade surgical masks or course weave fabric, to be a potential generator of aerosols? Particularly after a fabric has reached saturation, it makes sense that droplets initially obstructed by fabric fibers are eventually pushed through a fabric weave, under pressure, and emerge as aerosols. In some situations, with the goal of reducing transmission of a virus to others, larger droplets may be preferable to aerosols. What are you thoughts on this?
I was hoping if you cover dental procedures more
Thanks for mentioning about nitrous oxide as a separate category here. I think what should differentiate nitrous oxide from other oxygen mask therapies is the lower flow rate of gases being delivered and the negative pressure in the breathing circuit for scavenging purpose.
In my opinion, for its use in dentistry, using in a cooperative child patient with lower flow rate, with adequate scavenging pressure should not be contributing to generation of aerosols. Will the exhaled air in this scenario be in any way different from a normal exhaled air except for the fact that it is mixed with nitrous oxide gas.
COVID-19 is not an airborne disease but transmitted by respiratory droplets. With certain considerations such as low flow rate and proper scavenging I don’t think we’ll be producing respiratory droplets unless a child sneezes or coughs which anyways can happen in any normal situation. Hence nitrous oxide use for a cooperative child should be categorized as a low risk procedure.
Thank you Andrew – I would concur with that classification
Had a look up RA there – (Relative Analgesia for those following at home). I’d classify it as low
Hi Andrew, yes, it is a difficult debate with no real clinical evidence to determine one way or the other unfortunately. the main AGP items being ultrasonic scalers and high-speed instruments which obviously produce more airborne contamination that any other instrumentation in dentistry. would you venture an opinion as to whether RA could be classified as low or moderate AGP?
Hi Janet, this is something we have been debating at work. I agree that the set up is completely unlike high flow where I imagine a hurricane being forced into a small childs oropharynx, picking up viral particles like so much Kansas tumbleweed, then pushing it out in the faces of those nearby. The demand valves of most nitrous delivery devices really prevent this from happening.
The bigger challenge is in the potentially uncooperative child.
As with a lot of paediatric procedures we need to take into account the baseline rate of disease in your community (here in Oz it is incredibly low) coupled with the need to do the procedure or the risks/benefits of an alternative? We use a lot of nitrous and IN ketamine for fracture reduction, for example. I would imagine the risk to the HCW would be much higher if we insisted these patients went to theatre for intubation and reduction (though, personally I’d go for IV procedural sedation.
What I haven’t looked at either (and I am not going to) is the potential for aerosolisation of viral particles in the context of an actively vomiting child.
Interesting editorial. Would it be possible to have a comment re nitrous oxide sedation and its classification as a AGP? This is administered only using dedicated nitrous oxide flowmeters with a usual flow rate of 6 l/min into a dental sedation scavenger breathing system with nasal mask scavenged at a flow rate of 40 – 45 L/min maximum.
I agree, Eimear.
Anecdotally I have been seeing a lot more adults with dental abscesses and pericorinitis but I think that i because a lot of practices are closed.
I’ve not seen any case reports of dentists or staff being infected in the workplace (but am happy to be corrected).
~Andy
Hi there, I am a dentist working in primary care and we have always used high levels of PPE and use rigorous cross-infection control measures, given this and the fact that our drilling is on teeth and we use high volume evacuation with treated water being sprayed on the teeth do you think the risk from aerosol is as high as frontline staff dealing with sick patients. Most patients avoid us when they can but especially if they aren’t feeling well. Given that you discuss the exposure time to sick patients with high viral loads surely this means the risk from dentistry is extremely low. If we analyse how many dental staff get sick during flu season or more recently through this pandemic many countries have continued to carry out dentistry with little evidence of widespread infection amongst my colleagues?
Thank you Eimear O’Connell
In view of the following realities I would think.that the sentiments should lean towards a.higher.level.of.protection for paediatric HCW for ALL procedutes in young children. Adult data cannot be extrapolated.to.paediatric.patients.as the situations.are vastly different . The following factors need to be taken into consideration:
1. Smaller size of the patient and the subseqyent proximity of HCW to the patient’s airways.
2. The presence of an assistant and a caregiver (optionsl but often helpful) in the room.
3. The ancious behaviour of a young child in distress (kicking, crying with mouth wide open, fighting, screaming, vomiting) as well as their lack.of cough amd.sneeze eriquette .
4. The duration.of.the exposure (ofrlten much longer than with adults) and even more so when procedures amd administrwtion of drugs and fluids are combined with the procedure in order to conserve PPE
5. Size of the room – for some.bizarre reason small patients always seem.to get smaller spaces allocated,despite the inevitable presence of more than one HCW and/or caregiver
7. Recommendations not to use masks in children under.2 years.
8. Children.may be less affecred.clinically and should not.pose a considerable or compa able threat to the PPE supply.
9. Chdren are however often asymptomatic but highly infectious carriers.
10. Paediatric orientsted amd trained HCW are not easy to.replace. The use of non pediatric traoned HCW in the pediatric setting increase risk as specific skills are.required.to.assist with pediatroc.procedures. These skills.are acquired.with time and experience and cannot be iinstantly taught or acquired.
Comments will be appreciated.
Is chest tube insertion considered to be AGMP (trauma patient with a pneumothorax or tension pneumothorax)?
I’ve not found any formal data so I think common-sense and plausibility would suggest that it could well be.
Thank you Andrew
Hi
Is a cystoscopy or a Transurethral Resection of a blandear cancer considered an aerosol generating procedure?
Thank you
Jose, I’m afraid I only looked through the paediatric literature.
Thankyou Dr Tagg keep safe
Thank you for posting this article. Has anyone come across the level of risk with administering intranasal medications?
Hi Erin, I had a really good look but couldn’t find anything. To me, the risk would be in making a child sneeze a load of goobers in my face but it doesn’t seem to happen that often. ~Andy
Question: what are your thoughts about ventilation via uncuffed ETT? Risk of AGMPs?
Many procedures as considered AGPs are due to the cough they stimulate, should we not take the same precautions with a coughing patient who is generating an aerosol? The term aerosol generating event AGE seems to make more sense – could include procedures and the coughing patient.
Any thoughts on HCW protection with N95 versus surgical mask for coughing patient not necessarily having and AGP? CDC advocate N95, Australian guidelines surgical mask.
Excellent article just what we needed