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April 16, 2021

Indoor Air Changes and Potential Implications for SARS-CoV-2 Transmission

Author Affiliations
  • 1T.H. Chan School of Public Health at Harvard University, Boston, Massachusetts
  • 2Department of Surgery, Taubman College of Architecture & Urban Planning, University of Michigan, Ann Arbor
  • 3HOK Architects, Chicago, Illinois
JAMA. 2021;325(20):2112-2113. doi:10.1001/jama.2021.5053

Buildings have been associated with spread of infectious diseases, such as outbreaks of measles, influenza, and Legionella. With SARS-CoV-2, the majority of outbreaks involving 3 or more people have been linked with time spent indoors, and evidence confirms that far-field airborne transmission (defined as within-room but beyond 6 feet) of SARS-CoV-2 is occurring.1

Controlling concentrations of indoor respiratory aerosols to reduce airborne transmission of infectious agents is critical and can be achieved through source control (masking, physical distancing) and engineering controls (ventilation and filtration).2 With respect to engineering controls, an important flaw exists in how most buildings operate in that the current standards for ventilation and filtration for indoor spaces, except for hospitals, are set for bare minimums and not designed for infection control. Several organizations and groups have called for increasing outdoor air ventilation rates, but, to date, there has been limited guidance on specific ventilation and filtration targets. This article describes the rationale for limiting far-field airborne transmission of SARS-CoV-2 through increasing outdoor air ventilation and enhancing filtration, and provides suggested targets.

To reduce far-field airborne transmission of SARS-CoV-2 in small-volume indoor spaces (eg, classrooms, retail shops, homes if guests are visiting), the suggestions include targeting 4 to 6 air changes per hour, through any combination of the following: outdoor air ventilation; recirculated air that passes through a filter with at least a minimum efficiency rating value 13 (MERV 13) rating; or passage of air through portable air cleaners with HEPA (high-efficiency particulate air) filters.

Despite the dose-response for SARS-CoV-2 being unknown, and continued scientific debate about the dominant mode of transmission, evidence support these suggestions. First, SARS-CoV-2 is primarily transmitted from the exhaled respiratory aerosols of infected individuals. Larger droplets (>100 μm) can settle out of the air due to gravitational forces within 6 feet, but people emit 100 times more smaller aerosols (<5 μm) during talking, breathing, and coughing. Smaller aerosols can stay aloft for 30 minutes to hours and travel well beyond 6 feet.1 Second, high-profile and well-described SARS-CoV-2 outbreaks across multiple space types (eg, restaurants, gyms, choir practice, schools, buses) share the common features of time indoors and low levels of ventilation, even when people remained physically distanced.3

Third, these suggestions are grounded in the basics of exposure science and inhalation dose risk reduction. Higher ventilation and filtration rates more rapidly remove particles from indoor air, thereby reducing the intensity of exposure and duration that respiratory aerosols stay aloft inside a room. Fourth, this approach is consistent with what is used in hospitals to minimize risk of transmission (eTable in the Supplement). Fifth, reviews on the relationship between ventilation and infectious diseases found that the weight of evidence indicates ventilation plays a key role in infectious disease transmission, citing observational epidemiological studies showing low ventilation associated with transmission of measles, tuberculosis, rhinovirus, influenza, and SARS-CoV-1.4-6 All 3 reviews note the limited number of research papers on this topic and limitations of observational data. Sixth, more recently, the National Institute of Allergy and Infectious Diseases cited the importance of adequate ventilation in the suite of COVID-19 control measures,2 and the Centers for Disease Control and Prevention and the American Society of Heating, Refrigerating and Air-Conditioning Engineers (ASHRAE) support higher ventilation rates and enhanced filtration as components of holistic risk reduction strategies.

Current Indoor Air Ventilation Measures and Standards

Current ventilation standards for most indoor spaces are established by ASHRAE.7 These standards have been designed with the goal of diluting bioeffluents (such as odors from people) and achieving basic levels of acceptable indoor air quality, rather than infection control.8

While multiple conventions exist to describe ventilation rate (eg, total volumetric flow, volumetric flow per person and area, outdoor air ventilation rates), air exchange rate is frequently used in health care settings and commonly expressed in units of air changes per hour (ACH).

The existing minimum standards for ACH vary based on building type (eTable in the Supplement). For example, according to ASHRAE, the predominant standard-setting organization for ventilation rates, the minimum required total ACH that occur in most households is 0.35 ACH of outdoor air, and schools should be designed for approximately 10 times higher rates, although most schools do not meet this in practice.9 The suggestion for increasing the target to 4 to 6 ACH is more consistent with rates set in hospitals, where the higher ACH requirements underscore the potential role of air change rates as an infection control strategy.

Current Air Filtration Measures and Standards

In addition to air ventilation from outdoor air, respiratory aerosols can also be removed through air filtration. Filtered air can therefore be considered in terms of equivalent air changes per hour (ACHe) and added to the ACH from outdoor air.

Clean air delivery rate (CADR) is a term used to describe the amount of clean air delivered to a space as determined by filtration effectiveness and the amount of air moving through that filter. Portable air cleaners commonly use CADR to describe their effectiveness. For example, if a portable air cleaner has a high-efficiency particulate air (HEPA) filter, it will capture 99.97% of aerosols at 0.3 μm. Filter efficacy is commonly reported based on the aerosol size against which the filter performs most poorly (0.3 μm), although a HEPA filter will capture an even greater percentage of aerosols larger (and smaller) than 0.3 μm.

The CADR metric is valuable because it can be used to estimate the ACH of virus-free air being delivered to the room. The estimated ACHe is calculated as [CADR in ft3/min × 60 min] divided by the room volume in ft3. A device with a CADR of 300 in a 500-square-foot room with 8-foot ceilings will therefore deliver 4.5 ACH.

This same filtration concept can be applied to air that is recirculated through a central mechanical ventilation system or within-room ventilation system. However, most central mechanical systems were not designed for HEPA filters. Instead, these systems use filters on a different rating scale, minimum efficiency reporting value, or MERV, and typically use a low-grade filter (eg, MERV 8) that captures only approximately 15% of 0.3- to 1-μm particles, 50% of 1- to 3-μm particles, and 74% of 3- to 10μm particles.4 For infection control, buildings should upgrade to MERV 13 filters when possible, which could capture approximately 66%, 92%, and 98%, of these sized particles, respectively. These MERV values can be applied to the estimate of the overall clean air delivery rate for the room as with HEPA filters, but, instead of using near 100% capture efficiency for HEPA, the calculation has to be adjusted for the lower capture efficiencies of whichever MERV filter is used. Upgrading filters in mechanical systems is particularly important in buildings that use systems that recirculate air within the same room or same local ventilation zone.

Practical Design Considerations When Increasing Air Exchange and Filtration

Implementing changes to air ventilation and filtration to any building will have several important and practical design considerations.

First, increasing air exchange rates involves trade-offs including the added costs of moving more air as well as heating or cooling this larger volume of air. These added costs could be limited by using energy-efficient systems and “smart” systems that deliver air when the space is occupied. In addition, when appropriate, natural ventilation (eg, open windows) also could minimize the costs of achieving increased ventilation.

Second, improving indoor air ventilation and filtration only accounts for far-field (ie, beyond 6 feet) aerosol transmission and does not significantly influence close contact transmission. Wearing masks is still important indoors for source control and for close contact with individuals even when high air exchange rates are achieved.

Third, the utility of air changes per hour over a volumetric flow approach to ventilation is most useful in small rooms with ceiling heights generally less than 12 feet. In rooms with higher ceilings (eg, gymnasiums, atria), aerosols will dilute into the larger space and volumetric flow per area or per person would be a more appropriate measure that takes into account occupant density and activity level, which also influence aerosol emission rates.

Fourth, air exchange rates are useful under typical or low-occupant-density scenarios, as should be happening during a pandemic. In places with large occupancy limits, or if more people are added to a smaller space than it is designed for, ventilation needs to scale up accordingly.

Fifth, in locations where masks are not worn all of the time, like restaurants, additional strategies are needed including increasing to higher air change per hour targets, workers wearing high-efficiency masks, patrons wearing masks at all times other than while actively eating or drinking, and everyone inside physically distancing at least 6 feet.

Sixth, while these design considerations are important to reducing airborne transmission in the current context of the COVID-19 pandemic, improved air ventilation and filtration is a strategy that should be considered for continued use in buildings going forward because of associations with lower work and school absenteeism, better performance on cognitive function tests, and fewer sick building syndrome symptoms, such as headache and fatigue.10

Conclusions

Increasing air changes per hour and air filtration is a simplified but important concept that could be deployed to help reduce risk from within-room, far-field airborne transmission of SARS-CoV-2 and other respiratory infectious diseases. Healthy building controls like higher ventilation and enhanced filtration are a fundamental, but often overlooked, part of risk reduction strategies that could have benefit beyond the current pandemic.

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Article Information

Corresponding Author: Joseph G. Allen, DSc, MPH, Harvard T.H. Chan School of Public Health, 677 Huntington Ave, Boston, MA 02115 (jgallen@hsph.harvard.edu).

Published Online: April 16, 2021. doi:10.1001/jama.2021.5053

Conflict of Interest Disclosures: Dr Ibrahim reports receiving payments from HOK Architects in his role as a senior principal and chief medical officer. Dr Allen owns 9 Foundations Inc, which has provided consulting regarding COVID-19 risk reduction strategies across many sectors, including education, real estate, government, private entities, and faith-based organizations. Dr Allen has also received consulting fees from for-profit organizations, including serving as a scientific advisor for Carrier Corporation.

References
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National Academies of Sciences, Engineering, and Medicine. Airborne Transmission of SARS-CoV-2: Proceedings of a Workshop—in Brief. National Academy of Sciences; October 2020.
2.
Lerner  AM, Folkers  GK, Fauci  AS.  Preventing the spread of SARS-CoV-2 with masks and other “low-tech” interventions.   JAMA. 2020;324(19):1935-1936. doi:10.1001/jama.2020.21946PubMedGoogle ScholarCrossref
3.
The Lancet COVID-19 Commission Task Force on Safe Work, Safe School, and Safe Travel. Six priority areas. The Lancet COVID-19 Commission; 2021.
4.
Li  Y, Leung  GM, Tang  JW,  et al.  Role of ventilation in airborne transmission of infectious agents in the built environment: a multidisciplinary systematic review.   Indoor Air. 2007;17(1):2-18. doi:10.1111/j.1600-0668.2006.00445.xPubMedGoogle ScholarCrossref
5.
Sundell  J, Levin  H, Nazaroff  WW,  et al.  Ventilation rates and health: multidisciplinary review of the scientific literature.   Indoor Air. 2011;21(3):191-204. doi:10.1111/j.1600-0668.2010.00703.xPubMedGoogle ScholarCrossref
6.
Luongo  JC, Fennelly  KP, Keen  JA,  et al.  Role of mechanical ventilation in the airborne transmission of infectious agents in buildings.   Indoor Air. 2016;26(5):666-678. doi:10.1111/ina.12267PubMedGoogle ScholarCrossref
7.
American Society of Heating, Refrigerating and Air-Conditioning Engineers. ANSI/ASHRAE standards and guidelines to address COVID-19. Accessed April 9, 2021. https://www.ashrae.org/technical-resources/ashrae-standards-and-guidelines
8.
Persily  A.  Challenges in developing ventilation and indoor air quality standards: the story of ASHRAE Standard 62.   Build Environ. 2015;91:61-69. doi:10.1016/j.buildenv.2015.02.026PubMedGoogle ScholarCrossref
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Fisk  WJ.  The ventilation problem in schools: literature review.   Indoor Air. 2017;27(6):1039-1051. doi:10.1111/ina.12403PubMedGoogle ScholarCrossref
10.
Allen  J, Macomber  J.  Healthy Buildings: How Indoor Spaces Drive Performance and Productivity. Harvard University Press; 2020.
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    8 Comments for this article
    EXPAND ALL
    Importance of ACH and Out Flow in Determining Aerosol Contaminant Concentrations of Enclosed Spaces
    Bert Silich, M.D., M.S. | Henry Ford Hospital
    When dealing with problems of aerosol contaminant concentrations in enclosed spaces it is vital to realize out flow (Q m^3/hr) determines the steady state aerosol contaminant concentration of a room and ACH determines the time to reach steady state contaminant concentration. Any two different sized rooms with identical out flows will achieve the same steady state concentration. Any two different-sized rooms with identical ACH values will achieve their respective steady state contaminant concentrations in the same amount of time. This assumes the source of the contamination is identical in each case.

    The evidence comes from two articles (1,2). Within
    each article's appendix are derivations of the basic ventilation equations including recirculated, filtered air. Understanding these basic equations and how they affect the results of aerosol contaminant concentration is fundamental to solving problems of this nature. These articles assume ideal mixing of aerosol contaminants. When ideal mixing does not occur, adjustments can be made to compensate. The topic of compensation was not discussed in these articles.

    References

    1. Method to Reduce Aerosolized Contaminant Concentration Exposure to Healthcare Workers During the COVID-19 Pandemic when Temporary Isolation Systems Are Required https://doi.org/10.5811/westjem.2020.9.48170 

     2. A Model for Inhalation of Infectious Aerosol Contaminants in an Aircraft Passenger Cabin https://doi.org/10.15394/ijaaa.2021.1545
    CONFLICT OF INTEREST: Member of Vector Vantage LLC for consulting and software development.
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    Role of HVAC Systems
    Kenneth Elovitz, BS, JD | Energy Economics, Inc.
    It is worth emphasizing that this article addresses the spread of disease only by aerosol transmission in a well mixed room. The article (and HVAC systems in general) do not address close range transmission such as might occur when an infected person is talking to another person and infection occurs by large droplet transmission or because of locally higher concentration of infectious material.

    It might also be worth noting that clean air delivery rate (CADR) is only one element of disease transmission by aerosol contaminants. The well known Wells Riley equation recognizes the size of the space
    and time spent in the space as operative factors.

    For more information on HVAC systems and an application of the Wells Riley equation, see https://www.hpac.com/covid-19/article/21138820/assessing-the-role-of-hvac-systems-in-fighting-covid19.
    CONFLICT OF INTEREST: None Reported
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    Additional Airflow Concern Regarding SARS-CoV-2 in Churches, Schools, and Performance Venues
    Jim Toevs, PhD Experimental Physics | James W. Toevs Consulting; Los Alamos National Laboratory; First Presbyterian Church Santa Fe, NM
    Thank you for an excellent, well-written article that will be of considerable help to many people concerned with creating COVID-safe spaces in churches, schools, and other venues in which large audiences or classes will be present.

    In developing safe procedures for church classrooms and sanctuary I have found an additional concern regarding spread of SARS-CoV-2 to another person from a single COVID-emitting person, whether coughing, sneezing, or just exhaling. The concern is that even with an HVAC system 5 - 6 ACH, aerosols from the emitter may move very slowly past another person sitting a proper social distance
    away, slowly enough that the person with a poorly fitted mask or no mask may breathe a considerable quantity of virus particles in the mucosalivary aerosol droplet cloud from the emitter.

    For example, our church sanctuary is 70 feet long and the return path for air circulation is at the back of the chancel. With 6 ACH and no other air circulation, on average the air from the back of the sanctuary will have 10 minutes (600 seconds) to move the 70 feet, giving a speed of about 1.4 inches/second. If the aerosol cloud from a sneeze extends 20 feet and is not dispersed, the cloud will take about 170 seconds to pass the forward person, which is adequate time for that person to receive a significant dose of SARS-CoV-2.

    Additional air circulation from, for example, ceiling fans, oscillating fans, or vortex fans can disperse the cloud from the emitter's sneeze so that no other person is in the originally emitted dense cloud for a prolonged time.
    CONFLICT OF INTEREST: None Reported
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    Near vs. Far Field Exposure?
    John Murphy, PhD | University of Toronto
    A key point not addressed in Dr. Allen's and Dr. Ibrahim's paper is that that the patterns of COVID-19 transmission point to the likelihood that far-field exposures account for an exceedingly small fraction of transmissions as compared to near-field exposures. Ventilation upgrades do nothing to mitigate the latter, and consequently are unlikely to have material impacts on transmissions in spaces that are already ventilated in line with prevailing design standards. The authors' qualifiers are duly noted.
    CONFLICT OF INTEREST: None Reported
    Ventilation of Enclosed Space
    David Peters, D.O. | MSUCOM, Michigan
    Excellent article. It’s good to see an this analysis regarding the human species. This has been well known in large scale animal production for some time. Especially with swine production, percent air exchange per hour as well as temperature and humidity control, to be optimally managed, are species-specific when it comes to infection control.

    Large scale veterinary medicine is ahead of us on this one. However, quarantining an individual before introduction to herd has yet to be worked out in school or work place settings. Our schools and offices historically have been under ventilated with sub
    optimal temperature and humidity control. Perhaps in the past they didn’t have to be.
    CONFLICT OF INTEREST: None Reported
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    Don't Forget The Possibility of Vertical Air Flow For Extreme Situations
    Robert Blasdell, Ph.D. | Retired
    It is encouraging to see studies on improving the engineering of room air flow to minimize airborne virus transmission. One note of caution: Don't forget that it is possible in extreme situations to outfit a room for vertical airflow.

    Creating vertical room air flow is (or at least was) a common practice in mainframe computer rooms to manage the very high heat load from multiple separated devices. Floors are raised and ceilings lowered and and both are perforated to allow forced air to flow almost perfectly vertically upward at every point inside the occupied
    portion of the room. The goal is to not have adjacent computers "breathing" the hot air of their neighbors. It seems likely that the same thing could be done (perhaps in reverse with almost perfectly vertically descending air flow) in high medical risk environments to prevent adjacent patients and treatment providers from being exposed to each other's horizontally diffusing aerosol contaminants.
    CONFLICT OF INTEREST: None Reported
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    Misleading
    Bruce Davidson, MD MPH | Pulmonary Medicine, Providence Health System
    Both authors disclose working for/owning private companies. I have no such conflict. I'm an AMA member and JAMA reader for decades who served as a TB Control Program director when CDC taught us airborne transmission prevention in the 1990s. In 1991(1) the Massachusetts Dept of TB Control, after investigating a building outbreak, published the evidence and clinical reasoning showing the limitation of ventilation for preventing airborne infection transmission. Low-dose upper-room germicidal UVC 254nm GUV doesn't have that limitation and is much cheaper but these co-authors aren't selling and marketing GUV on either of their websites.

    The authors misquote ASHRAE
    guidance in their text and on-line Supplement as Air Changes per Hour, ACH, whereas ASHRAE guidance is in Cubic Feet per Minute, CFM, of outside air, per occupant. Classrooms require 10 CFM outside air per occupant so 300 CFM for 28 pupils + 2 teaching staff; for 60 minutes, 18,000 CF per hour. Their Supplement cites an ASHRAE default classroom, 1000 sq ft. With a 9' ceiling, 9000 CF requires 2 full ACH of 100% outside air for its 30 occupants. But although some aircraft achieve 50% outside air in their ventilation, buildings usually achieve <33%. EPA has written: "Because it is costly to heat cold winter air and to cool hot summer air, some building engineers reduce or eliminate the amount of outdoor air brought into the system during hot and cold spells…" Six ACH of 33% outside air in that classroom meets the ASHRAE standard, providing 10 CMF per occupant = 2 ACH of 100% outside air, but provides minimal disinfection—at a comfortable air speed of 0.34 mph. Tripling ventilation to 30 CFM outside air per occupant, 900 CFM for the room, would obtain 40% disinfection but requires 3 times more ACH, 18 ACH total, 162,000 CF per hour total air (33% outside air), at 30 mph air speed. Who will pay to condition all that air? Who will sit through that windstorm? So these authors require masking, "high-efficiency masking", and "low-occupant-density scenarios"—but what about children's schools? Houses of worship? Cafes?

    Since 1991, public health professionals have instead promoted GUV with ordinary fan circulation which disinfects in any weather, using the modest ASHRAE-recommended ventilation to remove CO2 and odors, at far less expense (2,3,4,5). $280 retail cost, including tax, shipping, and one hour of handyman time with a ladder gets that previously described classroom air safely GUV-disinfected with 70-80% efficacy (4,5), equivalent to 16-20 ACH. A replacement bulb one year later costs $12.

    It is a disservice to medicine, physician readers, AMA members, and JAMA's tradition of scholarship not to mention its previously peer-reviewed published limitations and not to mention GUV. A new endovascular device for coronary disease could not be discussed in these pages without at least mentioning other devices, medical therapy, and surgical options. 

    References

    1. Nardell EA et al. Am Rev Respir Dis 1991; 144:302-306
    2. Davidson BL. Photochem Photobiol 2021; https://doi.org/10.1111/php.1338
    3. Sliney D. Photochem Photobiol 2013, 89: 770–776
    4. Mphaphlele M et al. Am J Respir Crit Care Med 2015; 192: 477-484
    5. Escombe AR et al. PLoS Medicine 2009; 6: e1000043
    CONFLICT OF INTEREST: None Reported
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    "Building ID Card" Requirement for Building Ventilation
    Mehmet Soy, Professor | Istanbul Altinbas University, Faculty of Medicine. Turkey
    I congratulate the authors for writing this article. it has been seminal for me.

    I believe that one of the lessons to be learned from the COVID-19 pandemic is that "buildings should be built primarily to ventilate from the outside" even at the expense of increasing energy costs. In order to reduce the spread of infection, especially in hospitals, it is necessary that the windows of the rooms can be opened.

    A "Building ID Card" application should be initiated for each building where people enter and exit for various reasons. This card must be hung at the entrance
    of the building where everyone can see it. When people enter the building, they should know in advance what type of building they enter, and what ventilation standards they are entering. Ventilation standards should be specific for each building, taking into account factors such as the purpose of use of the building and the number of people entering and leaving per unit time. For example, the standards of a building with an average of 100 people entering and leaving a day and a building with 500 people entering and exiting should be different.

    In addition, ventilation standards should be redefined for hospitals and compliance with these standards should be more strictly controlled. At the entrance door of each hospital, a "Building Identity Card" should be hung which includes information such as which standards are complied with for ventilation, the type of filters used, when they are changed, how much outdoor air they take, and so on.
    CONFLICT OF INTEREST: None Reported
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