key: cord-0729366-hjzlj8k3 authors: Mick, Paul; Murphy, Russell title: Aerosol-generating otolaryngology procedures and the need for enhanced PPE during the COVID-19 pandemic: a literature review date: 2020-05-11 journal: J Otolaryngol Head Neck Surg DOI: 10.1186/s40463-020-00424-7 sha: b9fd7732ffddfec3f71d98e6035b4d2b22275c8d doc_id: 729366 cord_uid: hjzlj8k3 BACKGROUND: Adequate personal protective equipment is needed to reduce the rate of transmission of COVID-19 to health care workers. Otolaryngology groups are recommending a higher level of personal protective equipment for aerosol-generating procedures than public health agencies. The objective of the review was to provide evidence that a.) demonstrates which otolaryngology procedures are aerosol-generating, and that b.) clarifies whether the higher level of PPE advocated by otolaryngology groups is justified. MAIN BODY: Health care workers in China who performed tracheotomy during the SARS-CoV-1 epidemic had 4.15 times greater odds of contracting the virus than controls who did not perform tracheotomy (95% CI 2.75–7.54). No other studies provide direct epidemiological evidence of increased aerosolized transmission of viruses during otolaryngology procedures. Experimental evidence has shown that electrocautery, advanced energy devices, open suctioning, and drilling can create aerosolized biological particles. The viral load of COVID-19 is highest in the upper aerodigestive tract, increasing the likelihood that aerosols generated during procedures of the upper aerodigestive tract of infected patients would carry viral material. Cough and normal breathing create aerosols which may increase the risk of transmission during outpatient procedures. A significant proportion of individuals infected with COVID-19 may not have symptoms, raising the likelihood of transmission of the disease to inadequately protected health care workers from patients who do not have probable or confirmed infection. Powered air purifying respirators, if used properly, provide a greater level of filtration than N95 masks and thus may reduce the risk of transmission. CONCLUSION: Direct and indirect evidence suggests that a large number of otolaryngology-head and neck surgery procedures are aerosol generating. Otolaryngologists are likely at high risk of contracting COVID-19 during aerosol generating procedures because they are likely exposed to high viral loads in patients infected with the virus. Based on the precautionary principle, even though the evidence is not definitive, adopting enhanced personal protective equipment protocols is reasonable based on the evidence. Further research is needed to clarify the risk associated with performing various procedures during the COVID-19 pandemic, and the degree to which various personal protective equipment reduces the risk. During the coronavirus disease 2019 (COVID-19) pandemic, personal protective equipment (PPE) worn by health care workers is critical for reducing transmission of the infection in health care settings, particularly when aerosol-generating medical procedures (AGMP) are being performed. An aerosol is a suspension of fine solid particles or liquid droplets in air or another gas. Within an aerosol, viral droplet nuclei can travel long distances and remain in the air for long periods of time. Aerosols are not as effectively filtered by surgical masks, and can be breathed directly into the lungs. For transmission to occur, it is not enough for viral material to exist in droplet nuclei; the virus must remain viable. Whether or not COVID-19 remains viable in aerosols (and for how long) is still being investigated, but the balance of evidence indicates that betacoronaviradae such as the 2003 SARS coronavirus (SARS-CoV-1) are viable in aerosols [1] . Many otolaryngology procedures are thought to be aerosolgenerating [2] . When healthcare workers are at risk of transmission of infection from aerosols, "airborne" (rather than droplet) precautions are required [3] . Otolaryngologists who are susceptible to being infected with COVID-19 and who are working in close proximity to infected tissues for lengthy periods may be exposed to large infectious doses. COVID-19 infects the upper aerodigestive tract with the highest viral loads occurring in the nasal cavities [4] . The surgeon's nose, throat, and conjunctiva (all potential routes of transmission) [1, 5] are typically within 30-60 cm of the patient's upper respiratory mucosa. During AGMP, as a surgeon gets closer to the source of the aerosol, particle density increases exponentially according to principles of diffusion [6] . The association between infectious dose and disease severity has not yet been determined. Analogous novel viral respiratory viruses, however, may provide a degree of evidence. The basic reproductive numbers (the expected number of cases directly generated by one individual in a population where all individuals are susceptible) for SARS-CoV-1 and COVID-19 appear to be similar and thus comparisons are reasonable [7, 8] . In animal studies, increasing the initial exposure to SARS-CoV-1 increased the risk that mice developed the infection [9] . Greater initial exposures to SARS-CoV-1 [10] , MERS coronavirus [11] and influenza [12] resulted in more severe disease. In at least one recent study, a higher concentration of COVID-19 in the nasal passages (i.e., higher viral load) was associated with increased risk of more severe disease and death [13] . Viral load, however, is measured after the onset of infection and thus is not a proxy for infective dose. During the pandemic, health care agencies such as the World Health Organization, U.S. Centers for Disease Control and the Public Health Agency of Canada [3, 14, 15] are responsible for defining AGMP and rationing PPE when demand is greater than supply. The lists of AGMP often do not specifically include otolaryngology procedures. National otolaryngology organizations and other ENT groups [16] have published otolaryngology-specific AGMP lists and PPE guidelines that call for a greater levels of protection than the public health agencies. For example, Givi et al and the Canadian Society of Otolaryngology-Head and Neck Surgery [2] call for airborne precautions when performing AGMP on patients for whom the index of suspicion for COVID-19 infection is not high, whereas the World Health Organization, the U.S. Centers for Disease Control, and the Public Health Agency of Canada do not [3, 14, 15] . Givi et al also suggest that health care workers use powered air purifying respirators (PAPRs) when available for AGMP performed on patients with probable or confirmed COVID-19, in contrast to public health agencies that are either silent on the issue or suggest PAPRs are not needed [17] . We are members of the Division of Otolaryngology in Saskatoon, Saskatchewan. We were invited by the local health authority to provide evidence that a.) demonstrates which otolaryngology procedures are aerosolgenerating, and that b.) clarifies whether the higher level of PPE advocated by otolaryngology groups is justified. The following serves as a summary of our submission. Part 1: aerosol-generating otolaryngology procedures Is COVID-19 transmitted via aerosols? Respiratory aerosols typically consist of droplet nuclei less than 5 μm in size [18] . Droplets fall to the ground at rates inversely proportional to their size. A 10 μm diameter particle settles in 8.2 min, compared to 1.5 h for a 3 μm diameter particle, and 12 h for a 1 μm particle [19] . Thus, unless rooms are well ventilated, aerosolized droplets can become more concentrated over time. For an infection to be transmitted via aerosol, the organism must be able to survive within the droplet nuclei until it is deposited onto the mucous membrane of a susceptible individual either via inhalation or direct contact. The World Health Organization has cautioned that more studies are needed to confirm if COVID-19 is transmitted via aerosols [20] , however an April 1, 2020 report from the U.S. National Academies of Science, Engineering and Medicine suggests it is likely [21] . The letter cites studies in which COVID-19 RNA was detected in air samples in hospital rooms of patients with COVID-19 [22] . A widely cited experimental study indicates that COVID-19 can remain viable in aerosols for hours [5] , but has been criticized since the methods used to aerosol the virus in the experiment are not reflective of AGMP or natural cough [20] . A case report of a trans-nasal pituitary adenoma excision performed in China before widespread introduction of strict PPE provides anecdotal evidence of aerosolized transmission of COVID-19. During the case, fourteen Chinese health care workers were reportedly infected by the patient (who was mildly symptomatic pre-operatively), who was later confirmed to have COVID-19. Transmission occurred to workers who were both inside and outside the operating room [23] . During the SARS-CoV-1 epidemic, the largest nosocomial outbreak in Hong Kong occurred with a clear spatial pattern of infection that matched ventilatory patterns of the hospital floor, suggesting aerosolized transmission was likely [24] . A similar study showed that the pattern of spread of a large community outbreak of SARS-CoV-1 matched the ventilatory pathways from the apartment of the index case [25] . Research about AGMP has arisen from and been motivated by the need to protect health care workers during previous pandemics. Cohort and case-control studies comparing the rates of transmission from patients to health care workers who perform certain procedures versus health care workers who do not provide direct evidence of the risk conferred by the procedures. Experiments demonstrating that various procedures generate aerosols provide more limited evidence since they do not prove that transmission occurs via the airborne route. After the AIDS epidemic of the 1980s there was concern regarding the transmission of blood-borne viral illnesses during surgery. Experiments showed that electrocautery, bone drilling, ultrasonically activated (Harmonic) devices, and suction irrigation create aerosolized blood droplets and tissue particles [26] [27] [28] [29] . There is no epidemiological evidence, however, that the human immunodeficiency virus can be transmitted via aerosolized blood droplet nuclei [30] . Experiments have also shown that intranasal and temporal bone drilling aerosolizes bone, blood and mucosa [26, 28, 31] . Workman et al applied fluorescein inside the nasal cavity of cadaveric specimens, performed various surgical procedures, and measured aerosol spread outside of the nostrils using a blue-light filter and digital image processing. Intranasal drilling but not cold instrumentation or microdebriding produced fluorescein aerosols that could be detected up to 60 cm from the nostrils [31] . During temporal bone drilling the spread of particles might be greater since the walls of the nasal cavity likely prevent the spread of some material. It is not known if the respiratory mucosa lining the middle ear and mastoid air cell system is involved in COVID-19, but because the rest of the airway is involved, it appears likely that the lining of the eustachian tube, middle ear, and mastoid air cell system are also contaminated [32, 33] . .For these reasons, the use of use of high speed drills during mastoidectomy should be considered an AGMP during COVID-19. During the SARS-CoV-1 epidemic, it was initially thought that transmission occurred primarily via contact or large respiratory droplets. It was observed, however, that transmission to health care workers occurred despite the use of contact and droplet precautions, particularly during procedures suspected to be aerosolgenerating such as endotracheal intubation [34, 35] . A meta-analysis of observational studies evaluating the risk of transmission of SARS-CoV-1 during the epidemic showed that health care workers performing endotracheal intubation, non-invasive ventilation, tracheotomy and manual ventilation before intubation were significantly more likely than health care workers not involved in these procedures to contract the disease [36] . Only one case-control study of front-line health care workers caring for SARS-CoV-1 patients in China contributed to the "meta-analysis" of tracheotomy [37] . In the univariate analysis, 6/85 cases (who had IgG against SARS-CoV-1) versus 11/646 controls (who did not have IgG against SARS-CoV-1) had performed tracheotomies during the epidemic (Odds ratio 4.15, 95% CI 2.75, 7.54). The odds ratio for bronchoscopy, on the other hand, did not reach significance (pooled OR 1.3, 95% CI 0.5, 14.2). Many public health agencies and professional organizations [38] , however, list bronchoscopy as an aerosol generating procedure. The World Health Organization appears to classify bronchoscopy [39] as an AGMP based on a study comparing the rate of tuberculin skin test conversion among pulmonology and infectious diseases fellows graduating in 1983 during a resurgence of tuberculosis in the United States. Seven of 62 (11%) pulmonology fellows versus one of 42 (2.4%) infectious diseases fellows reported having converted tuberculin skin tests during their fellowships [40] . It was not clear that the pulmonology fellows were infected as a result of performing bronchoscopies. A 2009 study during the H1N1 influenza outbreak measured the amount of viral RNA in the air in the vicinity of H1N1 positive patients undergoing bronchoscopy and other procedures, compared to controls. The concentration of viral RNA was not significantly increased during bronchoscopy or any other procedure studied. The authors wrote that their study may have been underpowered to detect small differences in aerosol concentrations [41] . If bronchoscopy is aerosol-generating, it may be due to the suctioning usually involved with the procedure. Air currents moving across the surface of a film of liquid generate droplets at the air-liquid interface, with the size of the droplets inversely proportional to the velocity of the air [39] . It is for this reason that any procedure that involve open suctioning of the airway is usually classified as aerosol-generating. There do not appear to be any studies that directly assess whether diagnostic nasopharyngoscopy produces aerosols in patients infected with respiratory viruses, and/or if it is associated with increased risk of airborne transmission of respiratory viruses to healthcare workers. Workman et al performed an experiment in which they pushed an atomizer device from the cranium of a cadaver through the cribriform plate and into the nasal cavity, plunged the syringe "at maximal pressure" to inject aerosolized fluorescein into the nasal cavity, then performed intra-nasal endoscopy and measured the spread of fluorescein out the nostrils. Various masks that were modified to allow passage of the endoscope were placed on the cadaver head in front of the nostrils. It is not known whether their methods accurately mimic the situation in patients with COVID-19. They did find, however, that the masks reduced the spread of fluorescein outside the nostris [31] . Despite the lack of evidence, in the COVID-19 era diagnostic endoscopy of the upper airways is often listed as an AGMP by health care agencies, likely because of its perceived similarities to bronchoscopy and because the endoscope travels through tissues with high COVID-19 viral loads [2, 42] . In contrast to bronchoscopy, however, many endoscopic procedures of the upper aerodigestive tract do not require suctioning. Further evidence is needed to understand the degree to which endoscopy of the upper aerodigestive tract generates aerosols. Generation of aerosols during cough, pursed lip breathing and normal breathing: implications for outpatient procedures Most ENT outpatient procedures induce coughing due to deep instrumentation and/or excessive mucous or blood that triggers the cough reflex. The jet of droplets and aerosols expelled by a cough can hit nearby health care workers at high volume and velocity, and at close range. The frequency of cough is higher in a patient infected with COVID-19, since it is a symptom of the infection [43] . The World Health Organization considers cough to be aerosol-generating [44] , a position that is supported by a number of studies [45] [46] [47] [48] [49] [50] . The average distribution of droplet sizes expelled during cough ranges on average between 0.58-5.42 μm, with multimodal peaks at 1, 2 and 8 μm. Larger droplets may partially evaporate during the jet expulsion from the mouth to produce smaller droplet nuclei [45] . Aerosols are also generated by "pursed lip" breathing methods, often adopted by patients who have epistaxis to avoid aspirating blood trickling posteriorly and into the throat [51] . Aerosols can be produced by normal breathing as air passes over respiratory mucosa [52] [53] [54] , through the reopening of closed small airways to form small airborne droplets [55] , and/or through fluid film rupture in the bronchioles [56] . During normal breathing, the lungs filter out most larger droplets from being exhaled [53] . As might be expected, coughing produces more aerosolized droplets than normal breathing or talking [53] . Breathing rate and age are both positively correlated with breath aerosol concentration, but do not completely explain the variability observed between individuals [56] . Head and neck physical examinations and the collection of nasopharyngeal swab samples are not typically classified as AGMP [17] . The fact that aerosols are produced during normal breathing combined with the close proximity required to perform these procedures do, however, provide support for recommendations from otolaryngology groups that airborne precautions should be taken by health care workers performing head and neck examinations in patients who have suspected or known COVID-19 [16] . Part 2: evidence clarifying if enhanced PPE are needed for otolaryngology AGMP Givi et al and the Canadian Society of Otolaryngology-Head and Neck Surgery suggest adhering to airborne precautions when performing AGMP on patients whose COVID-19 status is unknown or who have low risk of infection during the pandemic [2, 16] . They also recommend PAPRs (if available) to perform AGMP on patients with probable or confirmed COVID-19 [2, 16] . The World Health Organization [57] , CDC [14] and Public Health Agency of Canada [15] do not make these recommendations. Occupational health professionals are often tasked with determining the type of PPE needed in novel circumstances arising in various industries. The CDC through the National Institute for Occupational Safety and Health (NIOSH) [58] and the Canadian Center for Occupational Safety and Health [59] recommend "control banding" as a qualitative or semi-qualitative technique used to guide the implementation of workplace control measures. In control banding assessments, the potential for harm is determined by 1.) the consequences of exposure; 2.) the concentration of toxin; and 3.) the risk of exposure. Operations that expose workers to a greater potential for harm demand more stringent control measures. The consequences of COVID-19 infection to individuals are well described elsewhere [43] but range from mild illness to death. If health care workers become sick they can pass the infection to others, propagating the pandemic, and are no longer available to assist on the front lines. The increased risk of exposure to high concentrations of aerosols during otolaryngology AGMP has already been discussed. Thus, the following section focuses on the third element, the risk of exposure to COVID-19, and the likelihood that the different PPE recommended by the different groups alters the risk. The risk of exposure to COVID-19 when a patient's COVID-19 status is unknown A significant proportion of individuals infected with COVID-19 are either pre-symptomatic (they have not developed symptoms yet) or asymptomatic (they never develop symptoms). The mean incubation of COVID-19 period is 5-6 days, with a range of 1-14 days [43] . A well-known study of 3063 passengers on the quarantined Diamond Princess cruise ship showed that 52% of 634 persons who tested positive for COVID-19 had no symptoms at the time of testing [60] . On March 31, 2020, the director of the U.S. Centers for Disease Control (CDC) stated that the percentage of people in the general population who have COVID-19 but do not have symptoms is 25% [61] . This estimate ranges from 12.6% in China [62] to 50% in Iceland, where a very high proportion of the population (5%) has been tested for COVID-19 and thus the results may be more reflective of reality [63] . Pre-symptomatic carriers can transmit disease. On April 1, the CDC reported the results of an investigation of all 243 cases of COVID-19 reported in Singapore between January 23 and March 16. Seven clusters of cases were identified in which pre-symptomatic transmission was the most likely cause of secondary cases [64] . It is estimated that 44% of transmission could occur before the first symptoms [65] . The true number of cases of COVID-19 in the population is unknown but is assuredly much higher than the number of cases confirmed by testing and reported to government agencies due to limitations in population sampling and test sensitivity [66] . It is therefore likely that a significant proportion of patients presenting to the health care system for various reasons but who do not complain of symptoms of COVID-19 will be infected with the virus and can transmit it to health care workers for many months to come. The sensitivity and specificity of commonly performed COVID-19 diagnostic tests has not been definitively determined in part because a safe "gold standard" comparator has yet to be developed. Variability in sampling due to technical difficulties swabbing the nasopharynx or because of changes in the viral load throughout the course of illness may affect the sensitivity of the test. A negative result thus does not necessarily rule out infection. If the test is positive, it is likely correct, although it is possible that though cross-contamination from other patients or lab workers could result in false positive results [66] . The positive-and negative-predictive values of the test depend in part on the local true prevalence of COVID-19. For the reasons stated above, recommendations for airborne precautions for AGMP performed on patients whose COVID-19 status is unknown during the pandemic appear to be reasonable according to the precautionary principle [67] . It is not clear when such precautions should be rescinded. Published epidemiological projections suggest that similar to previous pandemics, even after the current wave of new cases subsides, outbreaks will recur throughout the world over at least the next year until herd immunity and/or an effective vaccination program is established [68] . The risk of exposure of COVID-19 using powered airpurifying respirators, reusable elastomeric respirators and filtering facepiece respirators (N95 masks) Powered air-purifying respirators (PAPRs), reusable elastomeric respirators and filtering facepiece respirators (e.g., N95 masks) represent different methods of filtering out aerosols in the air. A PAPR, which costs about USD 1400, contains a battery-powered high-efficiency particulate air filter that delivers clean air into a hood or a full face mask, and blows off exhaled air. The hood is either hard and tight-fitting or loose. The risk of leakage with PAPRs is negligible and, unlike reusable elastomeric respirators and N95 masks, there is no need for a fit test or additional eye protection since the head is completely enclosed within the system [69] . This feature of the PAPR benefits individuals who fail fit tests and those whose religious beliefs prevent them from shaving. Decontamination protocols for PAPRs must be in place and adhered to meticulously before they are re-used [69] . Resuable elastomeric respirators, which typically cost