key: cord-0893390-751h8daj
authors: Myers, Nirmala T.; Laumbach, Robert J.; Black, Kathleen G.; Ohman‐Strickland, Pamela; Alimokhtari, Shahnaz; Legard, Alicia; De Resende, Adriana; Calderón, Leonardo; Lu, Frederic T.; Mainelis, Gediminas; Kipen, Howard M.
title: Portable air cleaners and residential exposure to SARS‐CoV‐2 aerosols: A real‐world study
date: 2022-04-19
journal: Indoor Air
DOI: 10.1111/ina.13029
sha: 67ea730cde55f3640831a523004b501c9b455d4e
doc_id: 893390
cord_uid: 751h8daj

Individuals with COVID‐19 who do not require hospitalization are instructed to self‐isolate in their residences. Due to high secondary infection rates in household members, there is a need to understand airborne transmission of SARS‐CoV‐2 within residences. We report the first naturalistic intervention study suggesting a reduction of such transmission risk using portable air cleaners (PACs) with HEPA filters. Seventeen individuals with newly diagnosed COVID‐19 infection completed this single‐blind, crossover, randomized study. Total and size‐fractionated aerosol samples were collected simultaneously in the self‐isolation room with the PAC (primary) and another room (secondary) for two consecutive 24‐h periods, one period with HEPA filtration and the other with the filter removed (sham). Seven out of sixteen (44%) air samples in primary rooms were positive for SARS‐CoV‐2 RNA during the sham period. With the PAC operated at its lowest setting (clean air delivery rate [CADR] = 263 cfm) to minimize noise, positive aerosol samples decreased to four out of sixteen residences (25%; p = 0.229). A slight decrease in positive aerosol samples was also observed in the secondary room. As the world confronts both new variants and limited vaccination rates, our study supports this practical intervention to reduce the presence of viral aerosols in a real‐world setting.

from the respiratory tract have a bimodal size distribution, [8] [9] [10] which underlies two primary pathways for airborne transmission. Relatively large respiratory droplets (e.g., from ~10 to 100 µm and larger) rapidly settle onto surfaces, 11 typically within 1-2 m of the source.

They are amenable to protection by traditional techniques such as hand hygiene, social distancing, and face masks. Smaller particles, from ~100 nm to a few microns, can remain suspended in the air for hours, [12] [13] [14] move with air currents, and require additional control measures such as high-efficiency masks and respirators, ventilation, or air filtration. 15, 16 Epidemiological studies have found that transmission can occur at distances greater than 2 m away from an infectious source. [17] [18] [19] [20] [21] The potential importance of fine particles in COVID-19 transmission is supported by studies finding SARS-CoV-2 RNA in indoor air samples in healthcare settings 22, 23 and more recently in residences. [24] [25] [26] Individuals newly infected with SARS-CoV-2 are directed to isolate themselves at home, with necessary care (e.g., food and assistance with hygiene) provided by household members. Yet, unlike in healthcare settings, the presence of airborne SARS-CoV-2 RNA has not been systematically evaluated in residences. In a recent review, Dinoi et al. reported that more than 75% of studies of airborne SARS-CoV-2 RNA were conducted in hospitals, while only 13% were in community-based indoor environments, 27 and three studies were in homes of infected individuals. [28] [29] [30] The CDC recommends maintaining "good air flow" and opening the window in a space shared with an infected household member, but this advice may be difficult to follow due to limited ventilation, security concerns, and adverse weather conditions. Moreover, isolation from others may be difficult to achieve and maintain for 10-14 days (or shorter as per the latest Omicron-variant-based CDC guidance 31 ).

These challenges are likely to have contributed to the high rate of secondary infections (e.g., up to 55%) observed among household members. [32] [33] [34] Air filtration using portable air cleaners (PACs) is a practical intervention that could lower airborne viral particle concentrations and improve air exchange rates (AER) in homes, thereby reducing infection risk via fine aerosol and even droplets among close contacts and caregivers. [35] [36] [37] High efficiency particulate air (HEPA) filters, commonly used in PAC, capture at least 99.97% of particles of the maximum penetrating size (i.e., 0.3 µm in diameter). 38 Furthermore, the effectiveness of PACs to reduce the presence of aerosols, including PM 2.5 , PM 10, fungal spores, and black carbon, due to traffic, cooking, wildfires, and other sources, has been shown in residential settings. [39] [40] [41] [42] A typical PAC with a clean air delivery rate (CADR) of 300 cfm operating in a 15 x 15 x 8 ft. room provides clean air equivalent to 10 air changes per hour (ACH). 43 ACH in typical US homes without PAC is markedly lower, ranging only from 0.5 to 1.5. 37, 44 While the combination of vaccines and boosters prevents se- 3. Determine whether residential exposure to airborne SARS-CoV-2 can be reduced by PACs.

The study was a randomized crossover trial using air filtration with PACs as the intervention. Sampling was conducted in participants' residences for two consecutive 24-h periods (Day 1 and Day 2) with the PAC operated in "filtration" (HEPA filter installed) or "sham" (HEPA filter removed) modes. The participant was blinded to the order of treatments, which was randomized. The study took place between November 2020 and May 2021, during the time when Alpha (B.1.1.7), Iota (B.1.526), Gamma (P.1), and Delta (B.1.617.2) SARS-CoV-2 variants were dominant in the US. [46] [47] [48] The study was approved by the Rutgers University Institutional Review Board (Pro2020001323), and the participants provided informed consent.

• SARS-CoV-2 RNA was detected in aerosol samples collected in residences, further strengthening the thesis that the airborne transmission route is key for COVID-19 spread and deserves attention.

• Interventions in residences such as the use of portable air cleaners should be considered to reduce airborne viral levels and thus transmission of COVID-19.

• Lower viral loads in saliva samples (higher Ct values) are associated with a reduced probability of detecting SARS-CoV-2 RNA in the air.

• The presence of respiratory (e.g., cough, shortness of breath, and sore throat) and gastrointestinal symptoms may inform the likelihood of airborne transmission and direct preventive measures.

Participants were recruited primarily through Rutgers University Employee Health Services (New Jersey, US). Employees who received or reported a positive clinical test for SARS-CoV-2 were electronically given a study flyer and asked to contact the study team. Subjects were also recruited through a partnership with Vault Health (New York City, NY), a virtual healthcare platform that provides COVID-19 testing.

Vault's users testing positive for COVID-19 received an email informing them about the study and directing them to the study website with relevant contact information. Responding volunteers were screened by phone, and only adults who had received a positive clinical test within the last 7 days were eligible. At the beginning of the first 24-h period, participants provided saliva for COVID-19 PCR testing.

We sampled the air in two rooms (primary and secondary) in each residence. Participants (i.e., infected persons) chose the primary room as the space where they intended to spend most of their time and planned to isolate during the two sampling days. The secondary room was any other room of the participants' choice in the home, most often a living or dining room. Floor and room plans with dimensions (e.g., height, width, length) were created using Magicplan (Sensopia Inc., 2011-2018; Version 9.1.2; retrieved from http://itunes.apple.com); the data were used to determine the room volumes. Since our study was naturalistic, the participants were not given any specific instructions about isolating or any other behavioral changes. The words "residence" and "homes" are used interchangeably throughout the paper.

All participants completed three interviews with a member of the sampling team: at 0 h, 24 h (Day 1), and 48 h (Day 2) into field sampling. At the first interview, the participant provided demographic information, the type of residence, HVAC system, symptoms, choice of primary and secondary rooms, number of days since COVID-19 diagnosis and onset of symptoms, the total number of residents, and if other residents recently tested positive for COVID-19 or reported any symptoms (Table 1 and Table SI .1). In the two follow-up interviews, the number of hours the participant spent in the primary and secondary rooms for both sampling periods, door and window-opening behaviors (Table   SI. 2), and symptoms for every 24 h (Table SI. 3) were documented. 49 Briefly, the filter sample was placed in a microcentrifuge tube with 1 ml sterile RNA-free water (ThermoFisher Scientific) and vortexed three times for 10 s each. The eluate was then used for RNA extraction and analyses.

Virus RNA was extracted from the filters and saliva samples using the To validate the identity of amplified PCR products, pairs of clinical (i.e., saliva) and aerosol samples from 3 randomly selected homes were sequenced with the respective amplicon primers at IBX LLC using next-generation sequencing by the Illumina platform.

Study data were collected and managed using REDCap electronic 

Participants were tested for COVID-19 using a saliva test administered at the start of Day 1 (n = 23; Figure 1 ). Five participants tested negative on Day 1 and were excluded from the study. One home where equipment malfunctioned during sampling was also excluded from further analysis. Overall, seventeen participants completed the study. Two subjects were fully vaccinated (vaccines were just being deployed at the time of the study). Additionally, all participants had reported at least one symptom on Day 1 (discussed in more detail below).

The majority of participants lived in single-family detached homes (58.8%) and multi-apartment townhouses (29.4%), while only two participants lived in apartment buildings (11.8%). Frequency and percentages of demographic data, residence types, and survey data are presented in Table 1 59, 60 Similar to our study, Bal et al. 61 reported the S-gene target failure in the three-target RT-PCR assay when using the TaqPath kit.

The detection of SARS-CoV-2 RNA in non-fractionated aerosol samples is shown in Figure 2 and Table 3 . Out of the 17 residences, aerosol samples for ID 8 in the primary room and IDs 1 and 2 in the secondary room were analyzed using alternate analytical protocols and thus excluded from this report. 43.8% of the aerosol samples 

Only participants who tested positively for COVID-19 either from saliva or nasal swab samples within the last seven days were included in the study. They were stratified into two groups by the median diagnosis time (50th percentile = 3 days; IQR = 2 days): detection "within three days" or "from four to seven days" to investigate whether the number of days since the positive COVID-19 test affects SARS-CoV-2 RNA detection in the air. We found a similar proportion of positive aerosol samples between the two groups (45.5%, 5/11 residences vs. 40%, 2/5 residences), and the difference was not statistically different (p = 0.635).

CoV-2 RNA in saliva and aerosol samples We investigated the association between the source strength and the presence of SARS-CoV-2 RNA in the air. Clinical studies have shown an inverse correlation between higher SARS-CoV-2 Ct values and lower quantitative viral loads, for example, RNA copies/ml. 60, 62 We used saliva Ct values to stratify homes into "Low Ct" (<25th percentile saliva) and "High Ct" (>25 th percentile) saliva source strength groups (Figure 3 ). For aerosol samples collected in the primary room, 3/4 homes (75%) in the "Low Ct" group and 4/12 homes (33%) in the "High Ct" group tested positive for SARS-CoV-2 RNA. The association between detecting SARS-CoV-2 RNA in the air and Ct values in saliva samples was inverse and strong (G = −0.714; p = 0.070; Figure 3A ).

For the secondary room, 3 and 12 homes were stratified in the "Low Ct" and "High Ct" groups, respectively, with the 25th percen- In addition to individual symptoms, we also grouped related symptoms and analyzed their association with the detection of SARS-CoV-2 RNA in aerosol samples (Figure 4 ). If participants reported at least one respiratory symptom (e.g., cough, sore throat, shortness of breath), 50% (6/12 homes) had positive aerosol samples for SARS-CoV-2 RNA compared to 25% (1/4 homes) where no respiratory symptoms were reported (p = 0.392; Figure 4A ). When participants reported at least one symptom of fever, cough, or sore throat, there was also a positive but non-significant association with SARS-CoV-2 RNA in aerosol samples (54.5% (6/11 homes) vs. 20%

(1/5 homes); p = 0.231; Figure 4B ). whereas the values were slightly higher (i.e., less virus) during the "filtration" period (30.68-39.75; Figure 2B ,D). In the primary room (with the PAC), 43.8% of the samples (7/16 residences) were positive for SARS-CoV-2 RNA during the "sham" period, whereas only 25% of the samples (4/16 residences) tested positive during the "filtration" period (Table 3 ; p = 0.229). All rooms positive during filtration were also positive during sham.

In the secondary room (without the PAC), a higher proportion of positive aerosol samples for SARS-CoV-2 RNA was detected during both periods compared to the primary room: 46.7% (7/15 residences) during the "sham" period and 40% (6/15 residences) during the "filtration" period (p = 0.500). Similar to the primary room, all six secondary rooms that were positive during the "filtration" period were also positive during the "sham" period.

The effectiveness of PACs to remove airborne particles containing viruses is mainly dependent on room volumes, air mixing patterns, and clean air delivery rate (CADR). 65 Since rooms differed in their types and volumes, we analyzed the detection of airborne viral RNA as a function of those variables for both primary and secondary rooms: spaces. 43 

This project is the first blinded crossover randomized study to investigate whether air cleaners effectively reduce SARS-CoV-2 transmission in homes under real-world conditions, that is, without any behavior changes in residents. Our initial findings show that the rate of positive aerosol samples in homes of infected patients was reduced when comparing "filtration" to "sham" periods in the primary did not seek to control in this naturalistic study, as well as the small sample size, we had limited statistical power to detect differences between "filtration" and "sham" periods. We verified that SARS-CoV-2 RNA in aerosols is detectable in a substantial proportion of homes with infected residents, consistent with concerns that aerosol transmission may be important in secondary infection in homes.

As predicted, room volume appeared to be an important variable in analyzing the effectiveness of the PAC. Virus-negative TSP samples were more frequent in self-isolation rooms with higher ACH.

Scientific and public interest in using PACs with HEPA filters in residences has reemerged over the last decade to reduce combustion-derived 40 and indoor-generated air pollutants (e.g., from smoking, cooking, and cleaning) 70-72 as a means to decrease cardiorespiratory diseases, 73, 74 and asthma in adults and children. 75, 76 During the COVID-19 pandemic, PACs have been widely advertised and used to reduce exposure to viral aerosols, albeit without extensive data to support these claims. 30, 67 Since PACs are effective in removing airborne PM, by extension, they should be effective in removing viral aerosols and PM-associated viral particles, thereby minimizing the risk of airborne virus transmission in a cost-effective way.

They could at least partially address COVD-19 disparities in disadvantaged communities, where personal space is at a premium, a "sick room" might not be an option, window use is often constrained due to security concerns or poor outdoor air quality, and central HVAC 

This is the first blinded randomized intervention study using PACs to suggest the reduction of risk of airborne transmission of COVID-19 in residences without any experimental manipulation of residents' behavior or activity. Our findings reflect a real-world scenario where the acceptability and the usage of a candidate intervention were high among the participants. It provides a basis for additional studies designed to investigate the control of viral aerosols in residences, including in multiple rooms. SARS-CoV-2 RNA was detected in aerosols in residences using long-term filter sampling, and there were some associations between this detection and commonly reported COVID-19 symptoms and salivary viral load. We also found some evidence of reduction in SARS-CoV-2 aerosol exposure using PACs. The same virus lineage in the clinical and aerosol sample pair supports the now widely held belief that aerosols play a key role in SARS-CoV-2 transmission and further stresses the need for infected persons to isolate.

The use of air cleaners to reduce SARS-CoV-2 exposure should be considered for future guidance on how to care for COVID-19

patients in residential and community-based indoor environments, especially in situations of limited space and resources.

and NIH/CATS (UL1TR003017). Dr. Nirmala T. Myers was supported by NIEHS Training Grant in Exposure Science (1T32ES019854). Dr.

Frederic T. Lu was supported by NIOSH ERC (T42OH008422). We thank our referring physicians and Vault Health for participant referrals. We sincerely thank all the participants who were screened and allowed us into their homes.

No conflict of interest declared. 

Study data are available from the corresponding author upon request.

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