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healthxwiki COVID-19 evidence review 
How Much Can Ventilation Help? 


Original post date: 28 May 2020; Updated 29 Sept 2020

Overview

The internal debates of whether or not COVID-19 is largely transmitted via aerosols or larger droplets continue even as the evidence now reflects successfully cultured live infectious virus from aerosol samples. But, why is this debate not semantics or an academic exercise? Simply put, effective COVID-19 prevention strategies requires prioritizing the right tools. In the case of COVID-19, this means ventilation as a first line of defense.  

Certain environments are particularly implicated in COVID-19 transmission. These include poorly ventilated indoor environments. This includes indoor spaces with little/no air movement and spaces with unfiltered or poorly filtered re-circulated air (e.g., fans in enclosed spaces or air conditioning, with no external air source and/or exhaust) [3-6]. A key disruptor to COVID-19 transmission in these environments is to make the air less viable for virus carrying aerosols to accumulate [7-15]. 

Findings consistently point to natural ventilation (e.g., open doors & windows) as the most effective and low cost strategy.  When it comes to mechnical ventilation, such as HVAC systems, most are not designed to optimize infection control strategies. Using high rated filters (e.g., MERV 13 or higher), optimizing fresh air input/output & knowing which systems are only designed to filter air to protect the system (e.g., ductless central air/ heating systems) vs improve indoor air quality are important starting points [18-20]. When it comes to COVID-19 control, recent recommendations suggest a target of 5-6 changes of air in a room per hour (see figure 2). But, just how strong is the evidence of aerosol spread related to COVID-19 & how much can ventilation help? We examined early COVID-19, TB, influenza and SARS evidence to provide insight to this question. 

COVID-19 Aerosol Risk Navigation

The epidemiologic evidence to date implicates indoor settings but also provides evidence to indicate outdoors poses less risk, where there are no crowds. A review of transmission for 7,324 cases in 120 Chinese cities identified only 2 incidents related to outdoor transmission (one village outbreak and one individual transmission) [4]. But, the influence of crowds to dial up risk outdoors has been suggested. Among 35 aerosol samples taken from clinical settings in China, low concentrations of viral RNA were identified in all outdoor sampling locations. The exception to this was an outdoor sample location that was also a major contact mixing point between a department store and hospital entrance (1 meter away from hospital) [5].

In contrast, evidence reflect that indoors poses a risk, whether a crowd is present or not. An observational study (N=110; 11 clusters & isolated cases) in Japan found the odds of a primary case transmitting COVID-19 in a closed environment was 18.7 times greater than open air environments (95% CI: 6.0-57.9) [6]. In a 10-person restaurant outbreak investigation in China, customers sitting at tables within the line of air flow between an AC unit and a glass wall were implicated. However, customers sitting in the same room but outside of the line of air flow, remained uninfected [3]. More recently, COVID-19 findings confirm aerosols are not just present, but have infectious capacity. 

Jones and colleagues clarify these parameters and visualize this notion of dialing up and down of COVID-19 aerosol risk in Figure 1.  Key parameters used to assess COVID-19 aerosol risks include: level of ventilation, how many people are present, length of exposure time, and type of activity.

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Figure 1. Risk of SARS-CoV-2 from asymptomatic individuals from Jones Nicholas R, Qureshi Zeshan U, Temple Robert J, Larwood Jessica P J, Greenhalgh Trisha, Bourouiba Lydia et al. Two metres or one: What is the evidence for physical distancing in COVID-19? BMJ 2020; 370: m3223.


How much can ventilation help?

The evidence of ventilation as an infection control strategy is not another rabbit hole of mixed findings. In fact, ventilation as an infection control strategy has consistently demonstrated an outsized effect to disrupt transmission of SARS, TB and influenza across different settings (e.g., schools, transport, clinical, households) [7-8]. 

In households, where windows and doors were closed, had 60 times higher risk of TB transmission compared with homes where windows and doors were kept open. This translated into an air exchange per hour of 3 versus 20 [9]. 

In the context of public transport, transmission risks do not simply correlate with crowding as one might expect. Instead, spaces with the poorest ventilation have been most implicated. Some of these experiments used a clever proxy to quantify the difference in ventilation —the level of carbon dioxide-- where crowded trains had a carbon dioxide mean of 1,000 ppm compared to minibus shared taxis with a carbon dioxide mean of 1,800 ppm [10]. 

In clinical settings, risk of TB and SARS infections in health workers have varied significantly by ventilation type in hospital wards [11-14]. Transmission risk in 8 Peruvian hospitals was highest in closed unventilated rooms (97% risk), followed by negative pressure room (39%), and lowest in rooms with natural ventilation. Notably, the risk of transmission in newer building (33%) was higher than natural ventilation in older buildings (11%), where older buildings had higher ceilings and larger windows [11]. Similarly, in hospital wards treating SARS patients, health workers on wards using natural ventilation with electric exhaust fans had a compelling protective effect— a 73% decrease in odds of contracting SARS. In contrast, there was no protective effect for those working on wards with mechanical ventilation [13]. 

In schools, most classrooms suffer from poor ventilation, with many operating at 0.5 air exchanges per hour but studies demonstrate important strategies to improve air flow and in turn, reduce risks of disease transmission. For example, experimental influenza studies--  using real world contact tracking data for 789 US students--  indicate upgrading the air exchange in just 25% of rooms could reduce influenza outbreak sizes to those analogous with 30-40% flu vaccination coverage. Upgrading all rooms to 3 air exchanges* per hour reduced outbreak levels to sizes expected with 50-60% flu vaccination coverage. The authors concluded that selecting rooms to upgrade based on the number of students and room size was optimal, prioritizes small rooms with high occupancy [15].   

In other indoor venues with limited natural ventilation, such as dental offices using air purifiers, proximity to the infection source was not enough to reduce aerosol spread. Instead, both air flow and placement were essential for effective air filtration [16]. 

*5-6 air changes per hour are identified as targets for indoor control COVID-19. 

How can the evidence from SARS, TB & influenza inform ventilation for COVID-19?

There are key guiding principles consistent across the research. First, whether it’s natural, mechanical or a hybrid strategy—the goal is creating a flow of frequent air exchanges indoors. Fresh air actively moving into indoors dilutes virus-carrying aerosols. 

Second, just as ventilation can improve protection, it can also facilitate spread. Attention to fresh air flow direction can avoid moving infectious aerosols from one space to another or being directed towards susceptible individuals (see figure 3). 

Third, natural ventilation is almost always more protective, where there is ample cross movement of air through spaces [18]. Where limited natural ventilation exists, supplementing with simple electric exhaust fans has also shown to provide a significant protective effect in high risk settings [13]. 

Fourth, most HVAC systems are designed to improve indoor air quality, instead of infection control. Guidance from industry experts like ASHRAE and REHVA offer explicit guidance, including use of HEPA or MERV 13 or higher filter, optimizing fresh air intake and exhaust, troubleshooting barriers to air flow or air filter bypass problems for a start [19-20]. 

But, not all air systems are created equal. Most ductless air systems are not designed to improve air quality at all but instead maintain filters to protect the system itself [18] (See specific REHVA guidance for safe operating plan). In addition, air purifiers vary in effectiveness-- based on how quickly (e.g., clean air delivery score) and how much air exchange occurs [19-20]. 

These principles have been frequently omitted from COVID-19 prevention messages, largely due to key assumptions based on droplet models of disease transmission originating in the early 1900s. But, advances in technology have provided deeper insight into the behavior or aerosols.

Confirming this science further is the COVID-19 progress of countries such as Japan, where ventilation has been acknowledged early on to the public. The messaging-- known as the 3 C's-- have been simple yet effective for daily navigation of COVID-19 aerosol risk: Closed spaces with poor ventilation, crowded places, and close-contact settings where conversations are taking place. Fortunately, it's not context specific to Japan. It works in any country. Just like COVID-19.  

Figure 2. For Health, Healthy Buildings Program,
Harvard Chan School of Public Health



Figure 3. For Health, Healthy Buildings Program,
Harvard Chan School of Public Health

COVID-19 Aerosol & Ventilation Guidance

1. Collaboration of Aerosol Scientists (Marr, Miller, Prather, Haas, Bahnfleth, Corsi, Tang, Herrmann, Jimenez). FAQs on Protecting Yourself from Aerosols. 2020.

An extensive general overview of aerosols transmission and advice to reduce COVID-19 risks in daily navigation, including dining out, playing music, dental offices, among other scenarios. From a collaboration of leading aerosol experts. 

2. For Health, Harvard Chan School of Public Health, Guide to Measure Ventilation in Schools, The Healthy Buildings Program. Aug 2020.

Detailed step by step methodology to test ventilation capacity and recommendations for air change per hour targets to control COVID-19 spread in school settings. Applicable to any indoor building spaces.

3. Yale School of Public Health, Public Health Guidance for Reopening Schools for 2020, Ventilation Key to Reducing Risk. 

Guidance for multiple mechanical & natural ventilation scenarios for school re-opening but applicable to any indoor building spaces. 

4. ASHRAE. Guidance for re-opening of schools. 20 Aug 2020. 

5. ASHRAE. Guidance for polling place HVAC systems. 19 Aug 2020. 

6. ASHRAE. Building Readiness Guide. 19 Aug 2020. 

1. Wölfel, R., Corman, V. M., Guggemos, W., Seilmaier, M., Zange, S., Müller, M. A., ... & Hoelscher, M. (2020). Virological assessment of hospitalized patients with COVID-2019. Nature, 581(7809), 465-469.

2. Kimball, A., Hatfield, K. M., Arons, M., James, A., Taylor, J., Spicer, K., ... & Bell, J. M. (2020). Asymptomatic and presymptomatic SARS-CoV-2 infections in residents of a long-term care skilled nursing facility—King County, Washington, March 2020. Morbidity and Mortality Weekly Report, 69(13), 377.


3. Lu, J., Gu, J., Li, K., Xu, C., Su, W., Lai, Z., ... & Yang, Z. (2020). COVID-19 outbreak associated with air conditioning in restaurant, Guangzhou, China, 2020. Emerging infectious diseases, 26(7).

4. Qian, Miao, Liu Qian, H., Miao, T., Li, L. I. U., Zheng, X., Luo, D., & Li, Y. (2020). Indoor transmission of SARS-CoV-2. medRxiv.

5. Liu, Ning, Chen Liu, Y., Ning, Z., Chen, Y., Guo, M., Liu, Y., Gali, N. K., ... & Liu, X. (2020). Aerodynamic characteristics and RNA concentration of SARS-CoV-2 aerosol in Wuhan hospitals during COVID-19 outbreak. BioRxiv.

6. Nishiura, Oshitani et al., Nishiura, H., Oshitani, H., Kobayashi, T., Saito, T., Sunagawa, T., Matsui, T., ... & Suzuki, M. (2020). Closed environments facilitate secondary transmission of coronavirus disease 2019 (COVID-19). medRxiv.

7. Li, Y., Leung, G. M., Tang, J. W., Yang, X., Chao, C. Y., Lin, J. Z., ... & Sleigh, A. C. (2007). Role of ventilation in airborne transmission of infectious agents in the built environment-a multidisciplinary systematic review. Indoor air, 17(1), 2-18.

8. Luongo, J. C., Fennelly, K. P., Keen, J. A., Zhai, Z. J., Jones, B. W., & Miller, S. L. (2016). Role of mechanical ventilation in the airborne transmission of infectious agents in buildings. Indoor air, 26(5), 666-678.

9. Lygizos, M., Shenoi, S. V., Brooks, R. P., Bhushan, A., Brust, J. C., Zelterman, D., ... & Friedland, G. H. (2013). Natural ventilation reduces high TB transmission risk in traditional homes in rural KwaZulu-Natal, South Africa. BMC infectious diseases, 13(1), 300.

10. Andrews, J. R., Morrow, C., & Wood, R. (2013). Modeling the role of public transportation in sustaining tuberculosis transmission in South Africa. American journal of epidemiology, 177(6), 556-561.

11. Escombe, A. R., Oeser, C. C., Gilman, R. H., Navincopa, M., Ticona, E., Pan, W., ... & Friedland, J. S. (2007). Natural ventilation for the prevention of airborne contagion. PLoS Med

12. Jiang, S., Huang, L., Chen, X., Wang, J., Wu, W., Yin, S., ... & Li, J. (2003). Ventilation of wards and nosocomial outbreak of severe acute respiratory syndrome among healthcare workers. Chinese Medical Journal, 116(9), 1293-1297.

13. Chen, Ling, Lu Chen, W. Q., Ling, W. H., Lu, C. Y., Hao, Y. T., Lin, Z. N., Ling, L., ... & Yan, G. M. (2009). Which preventive measures might protect health care workers from SARS?. BMC Public Health, 9(1), 81.

14. Menzies, D., Fanning, A., Yuan, L., & FitzGerald, J. M. (2000). Hospital ventilation and risk for tuberculosis infection in Canadian health care workers. Annals of Internal Medicine, 133(10), 779-789.

15. Smieszek, Lazzari & Salathe Smieszek, T., Lazzari, G., & Salathé, M. (2019). Assessing the dynamics and control of droplet-and aerosol-transmitted influenza using an indoor positioning system. Scientific reports, 9(1), 1-10.

16. Chen, C., Zhao, B., Cui, W., Dong, L., An, N., & Ouyang, X. (2010). The effectiveness of an air cleaner in controlling droplet/aerosol particle dispersion emitted from a patient's mouth in the indoor environment of dental clinics. Journal of the Royal Society Interface, 7(48), 1105-1118.

17. Welch, D., Buonanno, M., Grilj, V., Shuryak, I., Crickmore, C., Bigelow, A. W., ... & Brenner, D. J. (2018). Far-UVC light: A new tool to control the spread of airborne-mediated microbial diseases. Scientific Reports, 8(1), 1-7.

18. Qian, H., & Zheng, X. (2018). Ventilation control for airborne transmission of human exhaled bio-aerosols in buildings. Journal of thoracic disease, 10(Suppl 19), S2295.

19. Harriman, L., Stephens, B., & Brennan, T. (2019). New Guidance for Residential Air Cleaners. ASHRAE Journal, 61(9), 14-23.

20. Kurnitski J, Boerstra A, Franchimon F, Mazzarella L, Hogeling J, Hovorka F, et al. REHVA COVID-19 guidance document , March 17 , 2020, How to operate and use building services in order to prevent the spread of the. 2020;2020(i): 1–6. 

21. Zhang, R., Li, Y., Zhang, A. L., Wang, Y., & Molina, M. J. (2020). Identifying airborne transmission as the dominant route for the spread of COVID-19. Proceedings of the National Academy of Sciences.

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