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June 7, 2022

Reducing SARS-CoV-2 in Shared Indoor Air

Author Affiliations
  • 1Centers for Disease Control and Prevention, Atlanta, Georgia
JAMA. 2022;328(2):141-142. doi:10.1001/jama.2022.9970

SARS-CoV-2 replicates in the respiratory tract and spreads through exhalation of infectious respiratory particles. The chances of transmission increase the longer an uninfected person stays in an enclosed space with an infected person. Infection can occur not only through short-range transmission of exhaled respiratory particles from an infectious person resulting in mucous membrane deposition or inhalation of exhaled respiratory particles by an uninfected person. Infection also can occur through long-range transmission from inhalation of infectious respiratory particles that remain suspended in air for longer periods (potentially after the infectious person is no longer present) and across longer distances (greater than a few meters).

Because no single approach is 100% effective in preventing COVID-19, prevention measures work best when layered, including vaccination and nonpharmacologic interventions that reduce inhalation of infectious particles. Community masking and physical distancing, both of which can reduce the likelihood of encountering and inhaling virus-containing particles, have received substantial attention. However, there is less public awareness about existing indoor air recommendations that can directly reduce the number of virus-containing particles in indoor air and thereby reduce the risk of inhaling these particles from shared air.

Methods to reduce the concentration of SARS-CoV-2 particles in indoor air include ventilation, filtration, and disinfection. Much remains to be learned about benefits of specific interventions and combinations under different circumstances. However, observational studies and modeling suggest substantial effectiveness for these strategies used alone, combined, and with other approaches. For example, in a 2020 study that included 169 Georgia elementary schools, COVID-19 incidence was 39% lower in 87 schools that improved ventilation compared with 37 schools that did not (35% lower in 39 schools that improved ventilation through dilution alone [incidence rates, 2.94 vs 4.19 per 500 students enrolled] and 48% lower in 31 schools that improved ventilation through dilution combined with filtration [incidence rates, 2.22 vs 4.19 per 500 students enrolled]).1 A simulation model found that filtration with 2 high-efficiency particulate air (HEPA) cleaners alone or combined with mask wearing could potentially reduce exposure to infectious particles by an estimated 65% or 90%, respectively.2

To date, there has been limited and uneven implementation of interventions to prevent SARS-CoV-2 transmission by reducing its concentration in the air. A report in Morbidity and Mortality Weekly Report highlights the considerable heterogeneity and inequity that schools report in the deployment of these measures.3 In this report based on a nationally representative sample of 420 schools in 2022, low-cost interventions (opening windows and doors) were widely used, but higher-cost and resource-intensive strategies such as upgrading heating, ventilation, and air conditioning (HVAC) systems were used much less frequently. Schools in rural areas or at mid-level poverty (with 26% to 75% of students eligible for free or reduced-priced meals) were least likely to implement several measures.3 It is likely that comparable disproportionalities exist in other indoor settings, from homes to businesses to large public spaces such as airports.

Reducing contaminants in shared air by improving air handling systems in buildings is an attractive, broadly effective structural measure that does not require repeated individual actions. An individual can wear a mask, open windows and doors, turn on fans and vents, and use portable air cleaners. Like fluoridation of drinking water to prevent tooth decay and road and vehicle design improvements to increase road safety,4 structural interventions that reduce the concentration of SARS-CoV-2 particles in the air can protect more people with less individual effort. Such strategies are increasingly valuable as society learns to coexist with COVID-19 and people return to sharing indoor spaces.

A growing list of options exists for structural interventions to prevent COVID-19 through dilution, filtration, and disinfection of shared indoor air. Air handling system upgrades, improvements, or setting changes can reduce viral particle concentrations by bringing in outdoor air to dilute potential contaminants. Using air filters with higher minimum efficiency reporting value (MERV) ratings in HVAC systems can more effectively filter respiratory particles from recirculated air. Portable and commercially available HEPA air cleaners can do the same for a single room without modifying the building’s existing air handling system. These devices can be especially useful in areas used by people at greater risk of having or acquiring COVID-19. Air disinfection methods such as upper room and in-duct UV germicidal irradiation are options for health care facilities and other settings (eg, school nurses’ offices, homeless shelter sleeping areas) where people with COVID-19 are likely to be present or where there is crowding and the health status of individuals is unknown.

Through the American Rescue Plan, Congress has appropriated nearly a half trillion dollars ($350 billion to state, local, and tribal governments and $122 billion to schools), roughly half of which remains available to support indoor air quality improvements in small businesses, industrial settings, commercial buildings, low-income housing, transportation hubs, and schools. To ensure that maximum benefit is realized from these resources and to protect the public from ineffective or potentially harmful technologies, the Environmental Protection Agency (EPA) recently issued guidance for building owners and operators as part of the agency’s Clean Air in Buildings challenge.5 Centers for Disease Control and Prevention (CDC) guidance likewise highlights proven interventions to improve ventilation and filtration in buildings.6 The CDC also provides interactive tools for home and schools to estimate the effects on indoor air quality of simple changes such as opening windows, upgrading HVAC filters, or using a HEPA air cleaner.7

Balancing effectiveness, equity, and feasibility means that the optimal set of interventions will vary by setting and situation. Many enhancements to ventilation and filtration can be made at no or low (<$100) cost, including opening windows, inspecting and maintaining HVAC systems, and using fans to increase the effectiveness of open windows. Portable HEPA air cleaners can be added for a few hundred dollars each.6 Environmental or safety considerations (eg, temperature extremes, fall risk, crime) might make low-cost interventions such as opening windows less feasible in some circumstances. In underresourced settings, there may be fewer resources to mitigate such concerns (eg, converting windows on high floors that cannot be opened to windows that can be opened with window guards). Although do-it-yourself options are not recommended as permanent solutions, they can be less costly and, when properly constructed, may be more practical in resource-constrained settings than commercial options.8

Most costly are large structural improvements, such as new or updated HVAC systems in public buildings; however, these structural changes most equitably improve indoor air quality for many people simultaneously and can also generate energy savings costs. The CDC, EPA, ASHRAE, and other organizations have voluntary recommendations and guidance for HVAC systems.5,6 Schools that take advantage of available funding to follow these recommendations can improve health and safety for all students and employees. Businesses that update HVAC systems not only benefit from energy efficiency and future cost savings but also make the environment safer for all workers and customers, especially essential workers who may need to interact with large numbers of people in the public.

Several methods are readily available to assess if improvements are working. Carbon dioxide monitors can provide insight on how well an occupied space is ventilated.6 Airflow measurement devices and tracer gas tests can directly examine ventilation rates. Aerosol sensors can determine the effectiveness of filtration systems.

Improving air quality has the potential to reduce not only infections with SARS-CoV-2 but also infections with other respiratory viruses and bacteria, reactive airway disease (eg, asthma) triggered by antigens,9 pulmonary and cardiovascular injury from inhalation of harmful respiratory particulates (eg, wildfires, smog), and toxicity from inhalation of volatile organic compounds. A once-in-decades opportunity now exists to make sustained improvements to public and private indoor air quality, reduce COVID-19 risk, and improve school, workplace, and consumer health and safety.

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Article Information

Corresponding Author: Deborah Dowell, MD, MPH, Division of Overdose Prevention, Centers for Disease Control and Prevention–National Center for Injury Prevention and Control, 4770 Buford Hwy NE, Atlanta, GA 30341 (ddowell@cdc.gov).

Published Online: June 7, 2022. doi:10.1001/jama.2022.9970

Conflict of Interest Disclosures: None reported.

Disclaimer: The views expressed in this article are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention.

References
1.
Gettings  J, Czarnik  M, Morris  E,  et al.  Mask use and ventilation improvements to reduce COVID-19 incidence in elementary schools—Georgia, November 16–December 11, 2020.   MMWR Morb Mortal Wkly Rep. 2021;70(21):779-784. doi:10.15585/mmwr.mm7021e1PubMedGoogle ScholarCrossref
2.
Lindsley  WG, Derk  RC, Coyle  JP,  et al.  Efficacy of portable air cleaners and masking for reducing indoor exposure to simulated exhaled SARS-CoV-2 aerosols—United States, 2021.   MMWR Morb Mortal Wkly Rep. 2021;70(27):972-976. doi:10.15585/mmwr.mm7027e1PubMedGoogle ScholarCrossref
3.
Pampati  S, Rasberry  CN, McConnell  L,  et al.  Ventilation improvement strategies among K-12 public schools—the National School COVID-19 Prevention Study, United States, February 14–March 27, 2022.   MMWR Morb Mortal Wkly Rep. Published online June 7, 2022. doi:10.15585/mmwr.mm7123e2Google ScholarCrossref
4.
Frieden  TR.  A framework for public health action: the health impact pyramid.   Am J Public Health. 2010;100(4):590-595. doi:10.2105/AJPH.2009.185652PubMedGoogle ScholarCrossref
5.
Environmental Protection Agency. Clean air in buildings challenge: guidance to help building owners and operators improve indoor air quality and protect public health. Accessed May 12, 2022. https://www.epa.gov/indoor-air-quality-iaq/clean-air-buildings-challenge
6.
Centers for Disease Control and Prevention. Ventilation in buildings. Accessed May 12, 2022. https://www.cdc.gov/coronavirus/2019-ncov/community/ventilation.html
7.
Centers for Disease Control and Prevention. Interactive home ventilation tool. Accessed May 26, 2022. https://www.cdc.gov/coronavirus/2019-ncov/prevent-getting-sick/interactive-ventilation-tool.html
8.
Environmental Protection Agency. Air cleaners, HVAC filters, and coronavirus (COVID-19). Accessed May 10, 2022. https://www.epa.gov/coronavirus/air-cleaners-hvac-filters-and-coronavirus-covid-19
9.
Brown  KW, Minegishi  T, Allen  JG, McCarthy  JF, Spengler  JD, MacIntosh  DL.  Reducing patients’ exposures to asthma and allergy triggers in their homes: an evaluation of effectiveness of grades of forced air ventilation filters.   J Asthma. 2014;51(6):585-594. doi:10.3109/02770903.2014.895011PubMedGoogle ScholarCrossref
6 Comments for this article
EXPAND ALL
Measuring CO2 to Reduce Covid-19 Exposure Risk
Jeoffry Gordon, MD, MPH | Retired
I recently bought a cheap ($90) CO2 meter online. It is not NEL or certified in any way. I recently attended 2 medical conventions, one in a high risk city (avg 270 cases/100,000 and test positivity 9.0%). Outside CO2 measured 400-600. Baseline indoor CO2 random was about 600; in a large well-ventilated auditorium it may be 900. In some small conference rooms it reached 1600 and 1900. Needless to say I was masked at all times, but I felt it would be optional when my meter read 600-800. If readings went over 2000 I would have left the room. The other conference auditorium was by the sea with open doors/windows and the reading never went over 900.

In addition to the formal use of CO2 meters to strictly measure HVAC efficiency, having a cheap CO2 meter is a good way to personally approximate otherwise unmeasurable personal exposure and risk when being up and about in the world.
CONFLICT OF INTEREST: None Reported
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Reducing SARS-CoV-2 Aerosol Transmission through Minimizing Talking Indoors
Alexander van Assendelft, M.D. | Kymenlaakso Central Hospital
Mechanical methods to reduce aerosols, the most important transmission route of the SARS-CoV-2 virus (1) do not address the origin of the airborne virus. Aerosol is produced by breathing, talking, shouting, singing, coughing and sneezing. Depending on volume, speaking spreads 5 -200 (on average 10) times more aerosols than breathing (2).

Currently used protective measures act like slices of Swiss cheese (3), through the holes of which aerosols pass, if not stopped by impermeable barriers, such as shut mouths. Minimizing talking indoors would boost the elimination of the virus. Since talking outdoors is much less dangerous than indoors,
verbal communication should preferably take place outdoors.

It would have been possible to eradicate the earlier SARS-CoV-2 variants in six to eight weeks by adding a strategy of minimizing talking indoors to the other tools of protection against SARS-CoV-2. The same result applies to complete lock downs, as recently has been seen in Shanghai/China (4).

This conclusion is also supported by an estimation using the Wells-Riley equation (2):

According to the used estimation model the R0 value diminishes from 3,4 to 0,9 and the infection risk from 2,1 to 0,5 per cent in a ventilated restaurant when talking is diminished by 75 per cent.

The parameters of the model are:

Room Volume m3 300
Infection Susceptible individuals 80
Exposure Time min. 90
Mechanical Air Exchange rate/h 9,2
Exhaled Quanta rate/h 147
Inhalation rate m3/h 0,54

(Peter Heldt, Ph.D. personal communication, 2021)

The Omicron variants are, however, much more transmissible than the earlier SARS-CoV-2 variants. They are as transmissible as measles (5). The possibility of eradicating the SARS-CoV-2 virus by minimizing
talking indoors is therefore lost. This method would, however, still be able to substantially diminish the cases of Covid-19. Also the World Health Organization (WHO) stresses on its web site in the answers to the question "COVID-19 how is it transmitted", that conversational distance is dangerous.

In any case it would be important for the population to be informed about the fact, that talking is the most infectious part of encounters between people. As the proverb says "speech is silver, silence is golden". During the pandemic this has a greater actuality than ever (6).

References

1. Alcami A, del Val M, Herman M, et al. I forme cientifico sobre vias de transmision SARS-CoV-2. Para el
Ministeri de Ciencia e Innovation de Espana. 29-Oct-2020 (actualization 10 Nov 2020).

2. Buonanno G, Stabile, Morawska L. Estimation of airborne viral emission: quanta emission rate of SARS-
Co-2 for infection risk assessment. Environ Int. 2020 Aug;141:105794. Doi: 10.1016/j.envint.2020.
105794

3. Larouzee J, Le Coze J-C. Good and bad reasons: The Swiss cheese model and its critics. Review. Safety
Science, June 2020; 126: 104660. doi: 10.1016/j.ssci.2020.104660

4. Bloomberg News, June 6, 2022. Beijing, Shanghai Reopening Speed up: China Lockdown Tracker.

5. UNMC. Nebraska Medicine. Omicron transmission: how contagious diseases spread. Dec. 21, 2021.

6. van Assendelft A, Rosendahl H, Groop, P-H, Kovanen P. Aerosolivälitteinen SARS-CoV-2-tartunta
- aliarvioitu vaara (Aerosol transmitted SARS-CoV-2 infection - a negleted danger). Suom Lääkäril
2020;75.1202-03. (in Finnish)

CONFLICT OF INTEREST: None Reported
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Reducing SARS-CoV-2 in Shared Indoor Air by UV-C
Stephen Strum, MD | Private Practice of Hematology & Oncology
Dowell et al. report on decreasing the SARS-CoV-2 air concentration by improved methods in ventilation/filtration with or without N95 masks (1). This is time-consuming and expensive. The use of UV-C exposure with the appropriate lamp inserted into a classroom for "x" amount of minutes pending the square footage of the classroom (or any room) is a more expedient and far cheaper approach to solve this problem. Peer-reviewed articles on this topic have been published in 2018 relating to H1N1 influenza (2) and in 2020 relating to SARS-CoV-2 (3-5). Now in 2022, reports on the use of UV-C to disinfect and reuse N95 masks (6) and to disinfect surfaces (7) have been reported. Confirmatory studies can easily be done to assess the efficacy of UV-C exposure in the decontamination of rooms in schools or anywhere by currently available light fixtures plugged into 120v receptacles.

References

1. Dowell D, Lindsley WG, Brooks JT. Reducing SARS-CoV-2 in Shared Indoor Air. JAMA. 2022.
2. Welch D, Buonanno M, Grilj V, et al. Far-UVC light: A new tool to control the spread of airborne-mediated microbial diseases. Sci Rep. 2018;8(1):2752.
3. Hessling M, Hones K, Vatter P, Lingenfelder C. Ultraviolet irradiation doses for coronavirus inactivation - review and analysis of coronavirus photoinactivation studies. GMS Hyg Infect Control. 2020;15:Doc08.
4. Heilingloh CS, Aufderhorst UW, Schipper L, et al. Susceptibility of SARS-CoV-2 to UV Irradiation. Am J Infect Control. 2020.
5. Buonanno M, Welch D, Shuryak I, Brenner DJ. Far-UVC light (222 nm) efficiently and safely inactivates airborne human coronaviruses. Sci Rep. 2020;10(1):10285.
6. Poster DL, Hardwick M, Miller CC, et al. Disinfection of Respirators with Ultraviolet Radiation. Journal of Research of the National Institute of Standards and Technology. 2021;126:1-29.
7. https://www.nist.gov/news-events/news/2022/06/seeking-covids-kryptonite

CONFLICT OF INTEREST: None Reported
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Reverse Fan Filter
Dr Mubarak M Khan, MBBS, DLO, DNB(ENT) | Sushrut ENT Hospital & Dr Khan’s Research Centre, Talegaön Dabhade, Pune India
We agree with the many points discussed in viewpoint regarding “ Reducing SARS-CoV-2 in Shared Indoor Air." The simplest solution we found is use of a reverse fan filter in closed indoor spaces. The reverse fan (exhaust fan) with its outlet covered by N95 mask material achieves possible filtration of air in closed indoor spaces. We are using this simplest available tool in our day-to-day practice in our crowded outpatient, inpatient, and even in OT units.

Depending upon the area of the closed indoor space, the fan's speed can be increased or multiple fans can be used. We change
the N95 mask material daily.

We have been using this simple technique in the last 2 years and have added a UVC tunnel in the reverse fan outlet for greater reduction of SARS-CoV-2 and other viruses and bacteria.

We think this can be a good alternative to costly HEPA air filters.

Sincere Regards
Dr Mubarak Khan
Dr Sapna Parab
Consultant & Directors
Sushrut ENT Hospital & Dr Khan’s Research Centre
Talegaön Dabhade
Pune
India

CONFLICT OF INTEREST: None Reported
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What About UV light?
Noel Eldridge, MS | Personal Opinion

This article does not mention ultraviolet light. Shouldn't it be pursued more strongly for Covid? Both the FDA and National Academies have websites on the topic.

CONFLICT OF INTEREST: None Reported
Electronic Filters
Harold Kornylak, DO | Private Practice
Electronic filters (plates with about 9000 volt across them) are actually more effective than HEPA filters at removing virus particles less than 1/4 the size of coronavirus, and simply need to periodic washing rather than expensive replacement. I am curious why everyone is ignoring them?
CONFLICT OF INTEREST: None Reported
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