This is a repository copy of A paradigm shift to combat indoor respiratory infection.
White Rose Research Online URL for this paper:
https://eprints.whiterose.ac.uk/177405/
Version: Accepted Version
Article:
Morawska, L, Allen, J, Bahnfleth, W et al. (36 more authors) (2021) A paradigm shift to
combat indoor respiratory infection. Science, 372 (6543). pp. 689-691. ISSN 0036-8075
https://doi.org/10.1126/science.abg2025
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A paradigm shift to combat indoor respiratory infection
Building ventilation systems must get much better
POLICY FORUM
Lidia Morawska, Joseph Allen, William Bahnfleth, Philomena M. Bluyssen, Atze Boerstra,
Giorgio Buonanno, Junji Cao, Stephanie J. Dancer, Andres Floto, Francesco Franchimon,
Trisha Greenhalgh, Charles Haworth, Jaap Hogeling, Christina Isaxon, Jose L. Jimenez,
Jarek Kurnitski, Yuguo Li, Marcel Loomans, Guy Marks, Linsey C. Marr, Livio Mazzarella,
Arsen Krikor Melikov, Shelly Miller, Donald K. Milton, William Nazaroff, Peter V. Nielsen,
Catherine Noakes, Jordan Peccia, Kim Prather, Xavier Querol, Chandra Sekhar, Olli
Seppänen, Shin-ichi Tanabe, Julian W. Tang, Raymond Tellier, Kwok Wai Tham, Pawel
Wargocki, Aneta Wierzbicka, Maosheng Yao
Email: l.morawska@qut.edu.au
There is great disparity in the way we think about and address different sources of
environmental infection. Governments have for decades promulgated a large amount
of legislation and invested heavily in food safety, sanitation, and drinking water for public
health purposes. By contrast, airborne pathogens and respiratory infections, whether
seasonal influenza or COVID-19, are addressed fairly weakly, if at all, in terms of
regulations, standards, and building design and operation, pertaining to the air we breathe.
We suggest that the rapid growth in our understanding of the mechanisms behind respiratory
infection transmission should drive a paradigm shift in how we view and address the
transmission of respiratory infections to protect against unnecessary suffering and
economic losses. It starts with a recognition that preventing respiratory infection, like
reducing waterborne or foodborne disease, is a tractable problem.
Two factors in particular may contribute to our relatively weak approach to fighting airborne
transmission of infectious diseases compared to waterborne and foodborne transmission.
First, it is much harder to trace airborne infections. Food and water contamination nearly
always come from an easily identifiable point source with a discrete reservoir, such as a
pipe, well, or package of food. Its impact on human health is early if not immediate in terms
of characteristic signs and symptoms, so that diligent epidemiology can track and identify the
source relatively easily. Over the years, this has led to the current public health structures in
well-resourced countries. Standards have been enacted for all aspects of food and water
processing, as well as wastewater and sewage. Public health officials, environmental health
officers, and local councils are trained in surveillance, sampling, and investigation of clusters
of potential food and waterborne outbreaks, often alerted by local microbiology laboratories.
There are published infection rates for a large range of pathogens, with morbidity and
mortality risks now well established. By contrast, airborne studies are much more difficult to
conduct because air as a contagion medium is nebulous, widespread, not owned by
anybody, and uncontained. Buildings and their airflows are complicated, and measurement
methods for such studies are complex and not generally standardized.
Second, a long-standing misunderstanding and lack of research into airborne transmission
of pathogens has negatively affected recognition of the importance of this route(1). Most
modern building construction has occurred subsequent to a decline in the belief that airborne
pathogens are important. Therefore, the design and construction of modern buildings make
few if any modifications for this airborne risk (other than for specialized medical, research, or
manufacturing facilities, for example). Respiratory outbreaks have been repeatedly
“explained away” by invoking droplet transmission or inadequate hand hygiene. For
decades, the focus of architects and building engineers was on thermal comfort, odor
control, perceived air quality, initial investment cost, energy use, and other performance
issues, whereas infection control was neglected. This could in part be based on the lack of
perceived risk or on the assumption that there are more important ways to control
infectious disease, despite ample evidence that healthy indoor environments with a
substantially reduced pathogen count are essential for public health.
It is now known that respiratory infections are caused by pathogens emitted through the
nose or mouth of an infected person and transported to a susceptible host. The pathogens
are enclosed in fluid based particles aerosolized from sites in the respiratory tract during
respiratory activities such as breathing, speaking, sneezing, and coughing. The particles
encompass a wide size range, with most in the range of submicrometers to a few
micrometers (1).
Although the highest exposure for an individual is when they are in close proximity,
community outbreaks for COVID-19 infection in particular most frequently occur at larger
distances through inhalation of airborne virus–laden particles in indoor
spaces shared with infected individuals (2). Such airborne transmission is potentially the
dominant mode of transmission of numerous respiratory infections. There is also strong
evidence on disease transmission— for example, in restaurants, ships, and schools
suggesting that the way buildings are designed, operated, and maintained influences
transmission.
Yet, before COVID-19, to the best of our knowledge, almost no engineering-based measures
to limit community respiratory infection transmission had been employed in public buildings
(excluding health care facilities) or transport infrastructure anywhere in the world, despite the
frequency of such infections and the large health burden and economic losses they cause
(3). The key engineering measure is ventilation, supported by air filtration and air disinfection
(4). In this context, ventilation includes a minimum amount of outdoor air combined with
recirculated air that is cleaned using effective filtration and disinfection.
VENTILATION OF THE FUTURE
There are ventilation guidelines, standards, and regulations to which architects and building
engineers must adhere. Their objectives are to address the issues of odor, and occupant
generated bioeffluents [indicated by the concentrations of occupant-generated carbon
dioxide (CO2)], by specifying minimum ventilation rates and other measures to provide an
acceptable indoor air quality (IAQ) for most occu-pants. Similarly, there are other guidelines
and regulations to ensure thermal comfort.To achieve this, the amount of outdoor air
delivered to indoor spaces is recommended or mandated in terms of set values of air change
rate per hour, or liters of air per person per second. Threshold values of CO2 and a range of
indoor air temperatures and relative humidity have also been prescribed.
There are also some health-based indoor air quality guidelines. The most important are the
World Health Organization (WHO) IAQ guidelines, providing values for benzene, carbon
monoxide, formaldehyde, and other chemicals, based on the duration of exposure (5). There
are, however, no ventilation guidelines or standards to specifically control the concentration
of these pollutants indoors. None of the documents provide recommendations or standards
for mitigating bacteria or viruses in indoor air, originating from human respiratory activities.
Therefore, it is necessary to reconsider the objective of ventilation to also address air
pollutants linked to health effects and airborne pathogens.
One challenge is that ventilation rates required to protect against infection transmission
cannot be derived in the same way as rates for other pollutants. First, infection focused
ventilation rates must be risk-based rather than absolute, considering pathogen emission
rates and the infectious dose [for which there exist data for a number of diseases, including
influenza (6), severe acute respiratory syndrome coronavirus (SARSCoV), Middle East
respiratory syndrome, tuberculosis, SARS-CoV-2, and measles]. There is often limited
knowledge of viral emission rates, and rates differ depending on the physiology of the
respiratory tract (which varies with age, for example), the stage of the disease, and the type
of respiratory activity (e.g., speaking, singing, or heavy breathing during exercise). The
infectious dose may differ depending on the mode of transmission. This is well established
for influenza A, for which the infectious dose is smaller with an aerosol inoculum than with
nasal instillation (7). Some infectious agents display “anisotropy,” in which the severity of
disease varies according to the mode of transmission (7).
Second, future ventilation systems with higher airflow rates and that distribute clean,
disinfected air so that it reaches the breathing zone of occupants must be demand controlled
and thus flexible (see the figure). The ventilation rate will differ for different venues according
to the activities conducted there (e.g., higher ventilation rates for exercising in gyms than for
resting in movie theaters). There are already models enabling assessments of ventilation
rates and their effective distribution in the occupant microenvironments (8), and in general
this is a rapidly expanding field.
Demand control and flexibility are necessary not only to control risk but also to address other
requirements, including the control of indoor air pollution originating from inside and outside
sources and, especially, to control energy use: Ventilation should be made adequate on
demand but not unreasonably high. Buildings consume over one-third of energy globally,
much of it expended on heating or cooling outdoor air as it is brought indoors. Therefore,
although building designs should optimize indoor environment quality in terms of health and
comfort, they should do so in an energy efficient way in the context of local climate and
outdoor air pollution.
Third, in some settings, it will not be possible to increase ventilation to the point of reducing
the risk to an acceptable level, regardless of the quality of the ventilation system. This refers
to individual risk of infection for each susceptible occupant, to the event reproduction number
(the expected number of new infections arising from a single infectious occupant at an
event), and to the reality that ventilation has less of an impact for near-field exposure.
Management of the event reproduction number is important for the control of an epidemic,
especially for indoor spaces with a high density of people, high emission rate (vocalization
or exercising), and long periods of shared time. Spaces like this will require air-cleaning
measures, including air filtration and disinfection. Air filtration can be achieved by
incorporating filters into the building heating, ventilation, and air conditioning system or by
portable air cleaners, and air disinfection can be achieved by using ultraviolet devices (4)
while avoiding unproven technologies. The necessity of such measures and their effective
per-person additional removal rate, and thus their efficacy in risk reduction, can be
incorporated into risk assessment and prospectively modeled.
None of this means that every indoor space should become a biosafety facility. It means that
a building should be designed and operated according to its purpose and the activities
conducted there, so that air-borne infection risk is maintained below an acceptable level.
Such measures cannot easily be taken during the current pandemic because most building
systems have not been designed for limiting respiratory infection, building owners and
operators were not trained to operate the systems during the pandemic, and ad hoc
measures are often not sufficient. Such training, and appropriate measures, should form a
part of national strategies to prevent the spread of airborne diseases and infections.
The only types of public buildings where airborne infection control exists are healthcare
facilities, where requirements for ventilation rates are typically much higher than
for other public buildings (9). However, although modern hospitals comply with relevant
standards set to control infection, this may not always be the case for some hospitals located
in very old buildings. Comparing health care ventilation requirements with those for non–
health care venues suggests that non–health care rates should be higher for effective
infection control or that more recirculation with better filtration should be used.
There needs to be a shift in the perception that we cannot afford the cost of control, because
economic costs of infections can be massive and may exceed initial infrastructure costs to
contain them. The global monthly harm from COVID-19 has been conservatively assessed
at $1 trillion (10), but there are massive costs of common respiratory infections as well. In
the United States alone, the yearly cost (direct and indirect) of influenza has been calculated
at $11.2 billion (11); for respiratory infections other than influenza, the yearly cost stood
at $40 billion (12).
It is not known exactly what fraction of infections could be prevented if all building and
transport ventilation systems on the planet were ideal (in terms of controlling airborne
infections), or the cost of design and retrofitting to make them ideal. However, the airborne
transmission route is potentially the dominant mode of transmission (1, 2, 13). Estimates
suggest that necessary investments in building systems to address airborne infections would
likely result in less than a 1% increase in the construction cost of a typical building (14). For
the vast inventory of existing buildings, although economic estimations are more complex,
there are numerous cost-effective, performance-enhancing solutions to minimize the risk of
infection transmission. Although detailed economic analyses remain to be done, the existing
evidence suggests that controlling airborne infections can cost society less than it would to
bear them.
The costs of infections are paid from different pockets than building and operating costs or
health care costs, and there is often resistance to higher initial expenditure. But ultimately,
society pays for all the costs, and costs and benefits are never evenly distributed.
Investment in one part of the system may generate savings in a different part of the system,
so cross-system reallocation of budgets must be facilitated. The benefits extend beyond
infectious disease transmission. An improvement in indoor air quality may reduce
absenteeism in the workplace from other, non infectious causes, such as sick building