Coronavirus Disease 2019 and Airborne Transmission: Science Rejected, Lives Lost. Can Society Do Better?

This is an account that should be heard of an important struggle: the struggle of a large group of experts who came together at the beginning of the COVID-19 pandemic to warn the world about the risk of airborne transmission and the consequences of ignoring it. We alerted the World Health Organization about the potential significance of the airborne transmission of SARS-CoV-2 and the urgent need to control it, but our concerns were dismissed. Here we describe how this happened and the consequences. We hope that by reporting this story we can raise awareness of the importance of interdisciplinary collaboration and the need to be open to new evidence, and to prevent it from happening again. Acknowledgement of an issue, and the emergence of new evidence related to it, is the first necessary step towards finding effective mitigation solutions.

The size distribution of SARS-CoV-2 genetic material in airborne particles sampled in hospital and home care environments occupied by COVID-19 positive subjects.

Characterizing the size distribution of airborne particles carrying SARS-CoV-2 virus is essential for understanding and predicting airborne transmission and spreading of COVID-19 disease in hospitals as well as public and home indoor settings. Nonetheless, few data are currently available on virus-laden particle size distribution. Thus, the aim of this study is reporting the total concentrations and size distributions of SARS-CoV-2- genetic material in airborne particles sampled in hospital and home environments. A nanoMOUDI R122 cascade impactor (TSI, USA) was used to collect size-segregated aerosol down to the sub-micron range in home and in three different hospital environments in presence of infected patients in order to provide the concentration of airborne SARS-CoV-2 genetic material for each particle size range at different sampling locations. Providing one of the largest datasets of detailed size-fractionated airborne SARS-CoV-2 RNA to date, we found that 45.2 % of the total sub- and super-micrometric fractions were positive for SARS-CoV-2 with its genetic material being present in 17.7 % of sub-micrometric (0.18-1 µm) and 81.9 % of super-micrometric (>1 µm) fractions. The highest concentration of SARS-CoV-2 genetic material in total suspended particles (5.6 ± 3.4 RNA copies m-3) was detected in the room occupied with patients with more severe COVID-19 symptoms collected during the patients' high flow nasal oxygen therapy. The highest concentration at certain particle size fraction strongly depends on the sampling environment. However, the contribution of SARS-CoV-2 genetic material was in favour of super-micrometric compared to sub-micrometric particle size range. The evaluation of the individual risk of infection was carried out on the basis of the obtained data considering a hypothetical exposure scenario. The obtained results indicate the necessity of the protective masks in presence of infected subjects, especially while staying for longer period of time in the hospital environments.

Respiratory aerosol particle emission and simulated infection risk is greater during indoor endurance than resistance exercise.

Pathogens such as severe acute respiratory syndrome coronavirus type 2 (SARS-CoV-2), influenza, and rhinoviruses are transmitted by airborne aerosol respiratory particles that are exhaled by infectious subjects. We have previously reported that the emission of aerosol particles increases on average 132-fold from rest to maximal endurance exercise. The aims of this study are to first measure aerosol particle emission during an isokinetic resistance exercise at 80% of the maximal voluntary contraction until exhaustion, second to compare aerosol particle emission during a typical spinning class session versus a three-set resistance training session. Finally, we then used this data to calculate the risk of infection during endurance and resistance exercise sessions with different mitigation strategies. During a set of isokinetic resistance exercise, aerosol particle emission increased 10-fold from 5,400 ± 1,200 particles/min at rest to 59,000 ± 69,900 particles/min during a set of resistance exercise. We found that aerosol particle emission per minute is on average 4.9-times lower during a resistance training session than during a spinning class. Using this data, we determined that the simulated infection risk increase during an endurance exercise session was sixfold higher than during a resistance exercise session when assuming one infected participant in the class. Collectively, this data helps to select mitigation measures for indoor resistance and endurance exercise classes at times where the risk of aerosol-transmitted infectious disease with severe outcomes is high.

Increasing ventilation reduces SARS-CoV-2 airborne transmission in schools: A retrospective cohort study in Italy's Marche region.

Introduction: While increasing the ventilation rate is an important measure to remove inhalable virus-laden respiratory particles and lower the risk of infection, direct validation in schools with population-based studies is far from definitive. Methods: We investigated the strength of association between ventilation and SARS-CoV-2 transmission reported among the students of Italy's Marche region in more than 10,000 classrooms, of which 316 were equipped with mechanical ventilation. We used ordinary and logistic regression models to explore the relative risk associated with the exposure of students in classrooms. Results and discussion: For classrooms equipped with mechanical ventilation systems, the relative risk of infection of students decreased at least by 74% compared with a classroom with only natural ventilation, reaching values of at least 80% for ventilation rates >10 L s-1 student-1. From the regression analysis we obtained a relative risk reduction in the range 12%15% for each additional unit of ventilation rate per person. The results also allowed to validate a recently developed predictive theoretical approach able to estimate the SARS-CoV-2 risk of infection of susceptible individuals via the airborne transmission route. We need mechanical ventilation systems to protect students in classrooms from airborne transmission; the protection is greater if ventilation rates higher than the rate needed to ensure indoor air quality (>10 L s-1 student-1) are adopted. The excellent agreement between the results from the retrospective cohort study and the outcome of the predictive theoretical approach makes it possible to assess the risk of airborne transmission for any indoor environment.

What were the historical reasons for the resistance to recognizing airborne transmission during the COVID-19 pandemic?

The question of whether SARS-CoV-2 is mainly transmitted by droplets or aerosols has been highly controversial. We sought to explain this controversy through a historical analysis of transmission research in other diseases. For most of human history, the dominant paradigm was that many diseases were carried by the air, often over long distances and in a phantasmagorical way. This miasmatic paradigm was challenged in the mid to late 19th century with the rise of germ theory, and as diseases such as cholera, puerperal fever, and malaria were found to actually transmit in other ways. Motivated by his views on the importance of contact/droplet infection, and the resistance he encountered from the remaining influence of miasma theory, prominent public health official Charles Chapin in 1910 helped initiate a successful paradigm shift, deeming airborne transmission most unlikely. This new paradigm became dominant. However, the lack of understanding of aerosols led to systematic errors in the interpretation of research evidence on transmission pathways. For the next five decades, airborne transmission was considered of negligible or minor importance for all major respiratory diseases, until a demonstration of airborne transmission of tuberculosis (which had been mistakenly thought to be transmitted by droplets) in 1962. The contact/droplet paradigm remained dominant, and only a few diseases were widely accepted as airborne before COVID-19: those that were clearly transmitted to people not in the same room. The acceleration of interdisciplinary research inspired by the COVID-19 pandemic has shown that airborne transmission is a major mode of transmission for this disease, and is likely to be significant for many respiratory infectious diseases.

Risk of SARS-CoV-2 in a car cabin assessed through 3D CFD simulations.

In this study, the risk of infection from SARS-CoV-2 Delta variant of passengers sharing a car cabin with an infected subject for a 30-min journey is estimated through an integrated approach combining a recently developed predictive emission-to-risk approach and a validated CFD numerical model numerically solved using the open-source OpenFOAM software. Different scenarios were investigated to evaluate the effect of the infected subject position within the car cabin, the airflow rate of the HVAC system, the HVAC ventilation mode, and the expiratory activity (breathing vs. speaking). The numerical simulations here performed reveal that the risk of infection is strongly influenced by several key parameters: As an example, under the same ventilation mode and emitting scenario, the risk of infection ranges from zero to roughly 50% as a function of the HVAC flow rate. The results obtained also demonstrate that (i) simplified zero-dimensional approaches limit proper evaluation of the risk in such confined spaces, conversely, (ii) CFD approaches are needed to investigate the complex fluid dynamics in similar indoor environments, and, thus, (iii) the risk of infection in indoor environments characterized by fixed seats can be in principle controlled by properly designing the flow patterns of the environment.

Increased close proximity airborne transmission of the SARS-CoV-2 Delta variant.

The Delta variant of SARS-CoV-2 causes higher viral loads in infected hosts, increasing the risk of close proximity airborne transmission through breathing, speaking and coughing. We performed a Monte Carlo simulation using a social contact network and exponential dose-response model to quantify the close proximity reproduction number of both wild-type SARS-CoV-2 and the Delta variant. We estimate more than twice as many Delta variant cases will reproduce infection in their close proximity contacts (64%) versus the wild-type SARS-CoV-2 (29%). Occupational health guidelines must consider close proximity airborne transmission and recommend improved personal respiratory protection for high-risk workers.

The airborne contagiousness of respiratory viruses: A comparative analysis and implications for mitigation

The infectious emission rate is a fundamental input parameter for airborne transmission risk assessment, but data are limited due to reliance on estimates from chance superspreading events. This study assesses the strength of a predictive estimation approach developed by the authors for SARS-CoV-2 and uses novel estimates to compare the contagiousness of respiratory pathogens. We applied the approach to SARS-CoV-1, SARS-CoV-2, MERS, measles virus, adenovirus, rhinovirus, coxsackievirus, seasonal influenza virus and Mycobacterium tuberculosis (TB) and compared quanta emission rate (ERq) estimates to literature values. We calculated infection risk in a prototypical classroom and barracks to assess the relative ability of ventilation to mitigate airborne transmission. Our median standing and speaking ERq estimate for SARS-CoV-2 (2.7 quanta h–1) is similar to active, untreated TB (3.1 quanta h–1), higher than seasonal influenza (0.17 quanta h–1), and lower than measles virus (15 quanta h–1). We calculated event reproduction numbers above 1 for SARS-CoV-2, measles virus, and untreated TB in both the classroom and barracks for an activity level of standing and speaking at low, medium and high ventilation rates of 2.3, 6.6 and 14 liters per second per person (L s–1 p–1), respectively. Our predictive ERq estimates are consistent with the range of values reported over decades of research. In congregate settings, current ventilation standards are unlikely to control the spread of viruses with upper quartile ERq values above 10 quanta h–1, such as SARS-CoV-2, indicating the need for additional control measures.

Tracing surface and airborne SARS-CoV-2 RNA inside public buses and subway trains.

Given the widespread concern but general lack of information over the possibility of SARS-CoV-2 infection in public transport, key issues such as passenger personal hygiene, efficient air circulation systems, and the effective disinfection of frequently touched surfaces need to be evaluated to educate the public and diminish the risk of viral transmission as we learn to live with the ongoing pandemic. In this context we report on a study involving the collection of 99 samples taken from inside Barcelona buses and subway trains in May to July 2020. From this sample group 82 (58 surface swabs, 9 air conditioning (a/c) filters, 3 a/c dust, 12 ambient air) were selected to be analysed by RT-PCR for traces of the SARS-CoV-2 virus. Thirty of these selected samples showed evidence for one or more of 3 target RNA gene regions specific for this virus (IP2, IP4, E). Most (24) of these 30 samples showed positivity for only 1 of the 3 RNA targets, 4 samples yielded 2 targets, and 2 samples provided evidence for all 3 targets. RNA remnants were more common in surface swabs from support bars (23 out of 58) than in ambient air inside the vehicles (3 out of 12), with relatively higher concentrations of viral RNA fragments in buses rather than in trains. Whereas subway train a/c filters examined were all virus-free, 4 of the 9 bus a/c filter/dust samples yielded evidence for viral RNA. After nocturnal maintenance and cleaning most buses initially yielding positive results subsequently showed elimination of the RT-PCR signal, although signs of viral RNA remained in 4 of 13 initially positive samples. The presence of such remnant viral traces however does not demonstrate infectivity, which in the present study is considered unlikely given the fragmentary nature of the gene targets detected. Nevertheless, best practice demands that close attention to ventilation systems and regular vehicle disinfection in public transport worldwide need to be rigorously applied to be effective at eliminating traces of the virus throughout the vehicle, especially at times when COVID-19 cases are peaking. Additionally, infectivity tests should be implemented to evaluate the efficiency of disinfection procedures to complement the information resulting from RT-PCR analysis. Modelling the probability of infection whilst travelling in buses under different scenarios indicates that forced ventilation greatly reduces the risk.

Transmission of SARS-CoV-2 by inhalation of respiratory aerosol in the Skagit Valley Chorale superspreading event.

During the 2020 COVID-19 pandemic, an outbreak occurred following attendance of a symptomatic index case at a weekly rehearsal on 10 March of the Skagit Valley Chorale (SVC). After that rehearsal, 53 members of the SVC among 61 in attendance were confirmed or strongly suspected to have contracted COVID-19 and two died. Transmission by the aerosol route is likely; it appears unlikely that either fomite or ballistic droplet transmission could explain a substantial fraction of the cases. It is vital to identify features of cases such as this to better understand the factors that promote superspreading events. Based on a conditional assumption that transmission during this outbreak was dominated by inhalation of respiratory aerosol generated by one index case, we use the available evidence to infer the emission rate of aerosol infectious quanta. We explore how the risk of infection would vary with several influential factors: ventilation rate, duration of event, and deposition onto surfaces. The results indicate a best-estimate emission rate of 970 ± 390 quanta/h. Infection risk would be reduced by a factor of two by increasing the aerosol loss rate to 5 h-1 and shortening the event duration from 2.5 to 1 h.

How can airborne transmission of COVID-19 indoors be minimised?

During the rapid rise in COVID-19 illnesses and deaths globally, and notwithstanding recommended precautions, questions are voiced about routes of transmission for this pandemic disease. Inhaling small airborne droplets is probable as a third route of infection, in addition to more widely recognized transmission via larger respiratory droplets and direct contact with infected people or contaminated surfaces. While uncertainties remain regarding the relative contributions of the different transmission pathways, we argue that existing evidence is sufficiently strong to warrant engineering controls targeting airborne transmission as part of an overall strategy to limit infection risk indoors. Appropriate building engineering controls include sufficient and effective ventilation, possibly enhanced by particle filtration and air disinfection, avoiding air recirculation and avoiding overcrowding. Often, such measures can be easily implemented and without much cost, but if only they are recognised as significant in contributing to infection control goals. We believe that the use of engineering controls in public buildings, including hospitals, shops, offices, schools, kindergartens, libraries, restaurants, cruise ships, elevators, conference rooms or public transport, in parallel with effective application of other controls (including isolation and quarantine, social distancing and hand hygiene), would be an additional important measure globally to reduce the likelihood of transmission and thereby protect healthcare workers, patients and the general public.