Evaluation of SARS-COV-2 transmission through indoor air in hospitals and prevention methods: A systematic review.

Hospitals are the places for COVID-19 treatment but on the other hand, they are a dangerous source for SARS-COV-2 transmission. If we assume that the SARS-COV-2 is transmitted by air to hospitals, what are the strategies to reduce the SARS-COV-2 transmission and its removal? Therefore, this study aimed to evaluate SARS-COV-2 transmission through indoor air in hospitals and its prevention methods.This study is a systematic review by searching among published articles in reputable international databases such as Scopus, Google scholar, PubMed, Science Direct and ISI (Web of Science). Data were collected according to inclusion and exclusion criteria and by searching for relevant keywords. Qualitative data were collected using the PRISMA standard checklist. Information was entered into the checklist, such as the name of the first author, the year of the study publication, the country, the type of study, the number of samples, the type of air sample, the results, the methods for SARS-COV-2 transmission prevention in the hospital. After reviewing the information and quality of articles, 11 articles were included in this study. An analysis of the articles showed that Asian countries (Iran, China, Singapore) were more concerned with the SARS-COV-2 transmission through hospital air. Four articles did not confirm SARS-COV-2 in the air, but seven articles reported the SARS-COV-2 from air samples. The results of this study showed that many factors could affect the positive or negative SARS-COV-2 detection in the air, such as environmental conditions in hospitals, sampling methods, sampling height and distance from patients, flow rate and sampling time, efficiency and functionality of ventilation systems, use of disinfectants.Therefore, due to the possibility of SARS-COV-2 in the air of hospitals, preventive measures should be taken such as physical distance, personal hygiene, ventilation, and air filtration. We hope that this research will help to reduce the transmission of SARS-COV-2 and cut the airborne transmission pathway of SARS-COV-2 in hospitals.

Introduction

Since December 2019, cases of severe respiratory infections were reported in Wuhan, Hubei Province, China, which had been termed as COVID-19 caused by the severe acute respiratory syndrome coronavirus2 (SARS-COV-2) (Zhu et al., 2020; Adhikari et al., 2020). On January 30, 2020, the World Health Organization declared the SARS-COV-2 as a global epidemic (Zhou et al., 2020). The SARS-COV-2 is a member of the Coronaviridae family of the nidoviral order and is a large single-stranded RNA virus (Kai-Wang To et al., 2020).

Some studies introduced the most common COVID-19 transmission to humans: direct transfer via respiratory droplets, when coughing or sneezing, saliva, person to person transmission, and transmission by handling the mucous membranes from mouth, nose and eyes (Lu et al., 2020; Kai-Wang To et al., 2020).Indirect transmission through contaminated surfaces (metal, glass and plastic) on which the virus may remain for several days. COVID-19 lasts 3–4 h in aerosols, 24 h on cardboard, and 2–3 days on plastics and steel (Van Doremalen et al., 2020; Morawska et al., 2020).

Airborne SARS-COV-2 transmission had been reported in several studies (Rothe et al., 2020; Tang et al., 2020; Setti et al., 2020a,b). Different factors are involved in the duration the virus can remain in the air, the most important are the size of the droplets and environmental factors (Pica et al., 2012). Larger droplets fall faster, but smaller droplets can remain suspended in the air for some time, where airflow and ventilation can reduce its concentration in the air and contamination of surfaces removes it from the air. Atmospheric factors such as high temperature and humidity are associated with a decreased viral transmission (similar to the effect on influenza-like respiratory diseases), but there is still no scientific evidence for this assumption and more studies are still needed (Karin et al., 2020; Liu et al., 2011; Heidari et al., 2018). A study conducted in Wuhan, China showed that the main route for SARS-COV-2 transmission was closed contact and respiratory droplets, but the coronavirus presence in hospital air, environment and hospital equipment are also the causes of the high prevalence of the virus (Guo et al., 2020).

Hospitals are useful for SARS-COV-2 treatment, but on the other hand they are a dangerous source for SARS-COV-2 transmission (Wang et al., 2020). Probably patients with coronavirus spread the SARS-COV-2 to health care workers, family members, and equipment in the hospital through the air. (Fig. 1 ).

Fig. 1

Possible pathways for SARS-COV-2 transmission through air in hospitals.

In recent decades, health professionals have paid special attention to indoor air quality (Aghalari et al., 2019; Amouei et al., 2019), especially the air quality from medical environments such as hospitals. People with diversed diseases are admitted to hospital wards and during their hospitalization; they may spread several viruses and bacteria through air and environment to other people, such as health care workers. Many studies had been conducted on the effects from indoor air pollutants in hospitals such as carbon dioxide, carbon monoxide, formaldehyde, fungi and mold (Gola et al., 2019; Slama et al., 2019; El-Sharkawy et al., 2014), but there is very little research on viruses in the hospitals air. The world is currently struggling with the SARS-COV-2 epidemic. If we assume that the SARS-COV-2 can be spread through the hospitals air, what strategies to reduce the SARS-COV-2 transmission and removal are being performed? There are a few studies on how to prevent airborne SARS-COV-2 transmission. Therefore, this study aimed to evaluate the SARS-COV-2 transmission through indoor air in hospitals and its prevention methods.

Methods

Study protocol

This is a systematic review study that was performed to evaluate the SARS-COV-2 transmission through indoor air in hospitals and its prevention practices by searching among published articles in reputable international databases such as Scopus and Google scholar, PubMed, Science Direct, ISI (Web of Science). The search ranged from the first SARS-COV-2 report in China (December 2019) to October 1, 2020. The search was performed by two researchers in this article. Article references were reviewed to ensure that all articles related to the research objectives were included.

Search strategy

Inquired information was collected by searching for keywords; ‘SARS-COV-2’ OR ‘COVID-19’ OR ‘COVID-2019’ OR ‘Coronavirus’ AND ‘Hospital’ AND ‘Transmission’ OR ‘Transmission of SARS-COV-2’ OR ‘Transmission of Coronavirus’ OR ‘Transmission of COVID-19’ OR ‘Transmission of COVID-2019’ AND ‘Air’ OR ‘Air pollution’ OR ‘Airborn’ OR ‘Indoor air pollution’ OR ‘Hospital air pollution’ AND ‘Prevention’ OR ‘Prevention of air pollution’ OR ‘Prevention of SARS-COV-2’OR ‘Prevention of Coronavirus’ OR ‘Prevention of COVID-19’ OR ‘Prevention of COVID-2019’.

A manual search was performed by checking the list of all published articles. First, the abstracts of all articles were studied and then, if necessary, the complete articles were reviewed.

Inclusion criteria

Inclusion criteria for this study included diverse items: article published in English, year of the article publication, positive or negative report of SARS-COV-2 in hospital air, hospital as the study environment, article full text availability.

Exclusion criteria

Criteria for articles exclusion in this study included: lack of full access to the article, mismatch of the subject, lack of the published method, review article, letter to the editor.

Quality assessment articles

The articles quality was assessed based on the standard checklist PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-analyzes). The US-based National Institute of Health Quality Assessment Tool for Observational Cohort and Cross-Sectional Studies (National health, lung, and blood institute, 2020) for qualitative studies was used (Table 1 ).

Table 1

Check list of Quality Assessment Tool for Observational Cohort and Cross-Sectional Studies .

Criteria
1. Was the research question or objective in this paper clearly stated?
2. Was the study population clearly specified and defined?
3. Was the participation rate of eligible persons at least 50%?
4. Were all the subjects selected or recruited from the same or similar populations (including the same time period)? Were inclusion and exclusion criteria for being in the study prespecified and applied uniformly to all participants?
5. Was a sample size justification, power description, or variance and effect estimates provided?
6. For the analyses in this paper, were the exposure(s) of interest measured prior to the outcome(s) being measured?
7. Was the timeframe sufficient so that one could reasonably expect to see an association between exposure and outcome if it existed?
8. For exposures that can vary in amount or level, did the study examine different levels of the exposure as related to the outcome (e.g., categories of exposure, or exposure measured as continuous variable)?
9. Were the exposure measures (independent variables) clearly defined, valid, reliable, and implemented consistently across all study participants?
10. Was the exposure(s) assessed more than once over time?
11. Were the outcome measures (dependent variables) clearly defined, valid, reliable, and implemented consistently across all study participants?
12. Were the outcome assessors blinded to the exposure status of participants?
13. Was loss to follow-up after baseline 20% or less?
14. Were key potential confounding variables measured and adjusted statistically for their impact on the relationship between exposure(s) and outcome(s)?

Extract information from articles

To extract the information, all articles were independently evaluated by two reviewers based on inclusion and exclusion criteria. Both reviewer summarized information and in the cases where the information had contradictory opinions a third author was used. After confirming the articles quality, the information extracted from the articles entered the checklist used in other previous researches from the authors of this article (Tirgar et al., 2019, 2020; Aghalari et al., 2020). Information were entered into the checklist, such as the name of the first author, the year of the study publication, the country, the type of study, the number of samples, the type of air sample, the results, the methods for SARS-COV-2 transmission prevention in the hospital.

Findings

Search results

Using the listed keywords in combination or alone, 714 articles were found. After deleting irrelevant and duplicated articles, and deleting articles based on the inclusion and exclusion criteria of this study, 11 articles remained and were used for the systematic review (Fig. 2 ).

Fig. 2

PRISMA flow diagram showing the identification, screening, and inclusion of studies.

Quality assessment of articles

According to the PRISMA standard checklist and Table 1, 11 high quality articles were included in this study. All reviewed articles were published in 2020. The countries that studied air pollution in the hospital environment were 4 countries (Iran, China, USA, Singapore) with the highest number of articles (5 articles) related to China. All articles were original and sampled the hospital air. Most studies have examined SARS-COV-2 in the air of an intensive care unit (ICU) and isolation rooms, such as Masoumbeigi et al. (2020), Faridi et al. (2020), Li et al. (2020). The highest sample size (135 samples) was related to Li et al. (2020) in China hospital. ( Table 2 ).

Table 2

Information from articles on the SARS-COV-2 transmission through indoor air in hospitals and prevention methods.

Author/Year/Ref	Country of Origin	Sample Size	Sampling locations	Type of samples	Results of SARS-COV-2 in the air	Results reported in studies	Proposed methods to prevent SARS-COV-2 transmission
Masoumbeigi et al. (2020)	Iran	31 Samples	Emergency, bedridden, ICU, CT-SCAN, laundry wards	Air, Temperature, Relative, humidity	No	The SARS-COV-2 was not detected in air samples.	Use of natural and mechanical air conditioning system with positive pressure to clean the air in hospitals
Faridi et al. (2020)	Iran	10 Samples	ICU, ICU-General,ICU-Heart surgery, Thorax, Internal	Air, CO2, Temperature, Relative humidity	No	The SARS-COV-2 was not detected in air samples.	Use precautions for health care workers in hospitals
Li et al. (2020)	China	135 Samples	ICU, General isolation wards, Fever clinic, Storage room for medical waste, Conference rooms, Public area	Air, Aerosol	No	All aerosol samples were negative for the SARS-COV-2 detection.	Isolation ward with ‘three zones and two channels’, namely, clean, buffer and contaminated zones, with doctor and patient channels. The isolation ward should have negative pressure ventilation with 12 or more air changes per hour
Cheng et al. (2020)	China	8 Samples	Patients' room	Air, Aerosol	No	The SARS-COV-2 was not detected in air samples.	Use appropriate hospital infection control measures
Kenarkoohi et al. (2020)	Iran	14 Samples	ICU, ICU entrance hall, Hospital entrance hall, Laboratory ward, CT scan, Radiology, Men internal ward, Woman internal ward, Emergency ward	Air, Bioaerosol, Temperature, Relative humidity, CO2, Particulate matter	Yes	Possibility of airborne transmission of SARS-COV-2	Use the highest levels of Personal Protective Equipment (PPE) precautions
Lednicky et al. (2020)	USA	9 Samples	Patients' room	Air, Aerosol	Yes	The SARS-COV-2 in aerosols can be viable, and there is an inhalation risk with coughs, sneezes, and speaking.	Physical distance, wearing of face-coverings and hand-washing
Chia et al. (2020)	Singapore	6 Samples	Airborne infection isolation rooms, General ward	Air, Bioaerosol, Temperature, Relative humidity	Yes	SARS-COV-2 >4 μm and 1–4 μm sizes PCR-positive particles in two rooms	Not mentioned.
Ong et al. (2020)	Singapore	3 rooms	Isolation rooms	Air	No	All aerosol samples were negative for the SARS-COV-2 detection	Strict adherence to environmental and hand hygiene
Liu et al. (2020)	China	35 Samples	The intensive care units, coronary care units, ward rooms inside Renmin Hospital, Toilet, Staff workstations inside Fangcang Hospital, Medical staff areas, Public areas	Air, Total suspended particles	Yes	Very low concentration of SARS-COV-2 RNA in aerosols of isolated wards and ventilated patient rooms, higher concentration of SARS-COV-2 RNA in toilet	Room ventilation, sanitization of protective apparel, and proper use and disinfection of toilet areas
Guo et al. (2020)	China	40 Samples	ICU, GW	Air, Aerosol	Yes	SARS-COV-2 was widely distributed in the air, the SARS-COV-2 transmission distance might be 4 m	Stricter protective measures by medical staff.
Ding et al. (2020)	China	46 Samples	Isolation rooms, cleaner's storage, Nursing station, Corridor	Air, Bioaerosol, CO2	Yes	One air sample from a corridor was weakly positive to SARS-COV-2 detection	Pay attention to hygiene in both private and public toilets

Article features

In a study by Masoumbeigi et al. (2020) with 630 beds for admitting of COVID-19 patients, 31 air samples considering volumes from 100 to 1000 L were taken from different wards of a hospital accommodating and the amount of SARS-COV-2 in the hospital air was evaluated. The results showed that SARS-COV-2 was not detected in any of the air samples. In the study by Masoumbeigi et al. (2020), it was reported that different wards of the hospital were equipped with central, mechanical, and positive pressure ventilation systems.

In a study by Faridi et al. (2020) from Iran it was found that the SARS-COV-2 was not was not detected in air samples within 2–5 m from patients' beds and the results were negative. In this study, it was reported that mechanical/natural ventilation was used in different wards of the hospital.

In a study by Li et al. (2020), aerosol sampling and hospital environment were performed to detect the SARS-COV-2. The hospital wards were equipped with heating, ventilation and air conditioning (HVAC) systems. The ICU had 12 air inlets with 16 discharges per hour and an isolation room with 8 air inlets with 12 discharges per hour. After disinfecting the air 4 times, air sampling was performed through a plasma air sterilizer. COVID-19 patients were at least 1.5 m apart. The results showed that all aerosol samples were negative for SARS-COV-2 RNA detection.

In a study by Cheng et al. (2020) air samples were taken at a distance of 10 cm from the SARS-COV-2 patient at different conditions (normal breathing, deep breathing, speaking “1, 2, 3″ continuously, and coughing continuously). There was no SARS-COV-2 in the air samples but there was SARS-COV-2 detected in the environmental samples.

In a study by Kenarkoohi et al. (2020), bioaerosol sampling was performed in different wards of the hospital. The results showed that out of 14 bioaerosol samples, SARS-COV-2 detection was positive in 2 samples that were from ICU air. In the ICU, the ventilation system was mechanical. In air samples collected from different wards of the hospital, temperature, humidity, and carbon dioxide concentration were 24–27 °C, 40–50%, 341–390 ppm, respectively.

In a study by Lednicky et al. (2020), air samples were collected in the SARS-COV-2 patients' room at a distance of 2–4.8 m. Despite that air sampling was performed at the patients' hospital room, which changed its air 6 times per hour and UV sterilization was used for air purification, SARS-COV-2 were detected in the air. The results of above study showed that measures such as a physical distance of 6 feet in an indoor environment are not sufficient and create a false sense of safety and lead to exposure and spread of the SARS-COV-2.

In a study by Chia et al. (2020), air sampling was performed from three of the 27 AIIRs in the general ward for several days. The results showed that air samples from two of three AIIRs tested positive for SARS-COV-2, particles sized 1–4 μm and >4 μm were detected with SARS-COV-2. Surface contamination was also detected in rooms where SARS-COV-2 was detected in the air. It is noteworthy that in the rooms where air sampling was done, the air was changed 12 times per hour.

In a study by Ong et al. (2020) air sampling was performed from isolation rooms with 12 air exchangers per hour. The results showed that air samples from two rooms after disinfection with 5000 ppm of sodium dichloroisocyanurate and one room before disinfection were negative for SARS-COV-2 detection. But the air outlet fans from the room that was not disinfected were positive for the SARS-COV-2 detection.

In a study by Liu et al. (2020) air samples were taken at 30 points from two hospitals (Renmin Hospital of Wuhan University and Wuchang Fangcang Field Hospital in China. The results showed that the concentration of SARS-COV-2 RNA in aerosols of different wards and patient rooms was very low, but in the toilet room air that was used by patients had a higher concentration of SARS-COV-2 RNA. Patient toilet air was reported to be a highly contaminated source for SARS-COV-2 transmission. The SARS-COV-2 aerosol deposition at 30 sites in two designated hospitals and then quantified the copy counts of SARS-COV-2 in aerosol samples using a robust droplet-digital-PCR-based detection method and The study found that the SARS-COV-2 in the air could be transmitted to people through contamination of health care workers, surfaces and clothing.

In a study by Guo et al. (2020), sampling of different surfaces such as of floors, computer mice, trashcans, sickbed handrails, patient masks, personal protective equipment and hospital air was performed. Air sampling was performed through SASS 2300 Wetted Wall Cyclone Sampler. The SARS-COV-2 particles were widespread in the air and on different surfaces in the ICU and GW. The results of the study reported that one of the possible reasons for the high number of positive floor swab samples was due to gravity and air flow, which caused more SARS-COV-2 droplets to float in the air and fall on surfaces and ground. The study found that walking by medical staff around the ward could spread the virus to different wards of the hospital.

In a study by Ding et al. (2020), sampling of air and different surfaces were performed at different wards of the hospital. The results showed that out of 46 air samples in one corridor sample close to the patients' isolation rooms, the SARS-COV-2 detection was weakly positive. It was reported that the possible cause of the SARS-COV-2 in the corridor air close to the patients' isolation rooms was due to the transfer of the virus from the patients’ room to the corridor or the transfer of the virus from the Personal Protective Equipment (PPE) of the healthcare workers. Stool aerosols were further detected in the toilets used by patients SARS-COV-2 ( Table 2 ).

Discussion

The findings of this article demonstrated that there were more studies related to SARS-COV-2 transmission from hospital air from Asian countries (Iran, China, Singapore) and the highest number of articles was related to China. This is because the SARS-COV-2 was first observed in China and the SARS-COV-2 epidemic began in China (Phan et al., 2020; Xu et al., 2020; Ahmadi et al., 2020). Asian countries that are geographically closer to China are more concerned about the spread of the SARS-COV-2, for this reason, after the outbreak of the SARS-COV-2, many countries around the world, especially Asian countries, banned any transportation and entry into China and placed travelers returning from China in a 14-day quarantine (Mackenzie et al., 2020; Zhang et al., 2020). Therefore, researchers in Asian countries, along with health professionals in developed countries, should try to find new aspects of the SARS-COV-2 prevention through extensive research.

Based on the findings of this study, most articles were examining SARS-COV-2 in the air of ICU and isolation rooms, such as studies by Faridi et al. (2020), Masoumbeigi et al. (2020), and Li et al. (2020). The ICU is a hospital ward dedicated to the care of acute illnesses or serious injuries that requires closer and constant monitoring and support by specialized equipment and medications to maintain the body's normal functions. Therefore, clean and pollution-free air in the ICU is important and research is needed on SARS-COV-2 presence, density, and pathways in the air of ICU's.

Based on the findings of this article, four articles by Masoumbeigi et al. (2020) and Faridi et al. (2020) and Li et al. (2020) and Ong et al. (2020) reported that there was no SARS-COV-2 detection in the air samples and in 7 studies at least one air sample was reported to have the SARS-COV-2. The possible cause of negative SARS-COV-2 detection in the air could be attributed to the use of ventilation systems. The studies of Masoumbeigi et al. (2020) and Faridi et al. (2020) demonstrated that mechanical/natural systems were used in hospitals. In a study by Li et al. (2020), different hospital wards were equipped with heating, ventilation and air conditioning (HVAC) systems. In a study by Kenarkoohi et al. (2020), although ventilation system (mechanically) was used in the ICU, the SARS-COV-2 was detected in two air samples. Different results between studies may have different factors, such as sampling methods, sampling height, sampling distance to SARS-COV-2 patient, sampling locations, flow rate and sampling duration, efficiency and performance of ventilation systems, use of disinfectants before air sampling and the amount of particles (PM2.5 and PM10) in the air. For example in a study by Setti et al., (2020a,b) showed that high levels of PM10 spread the SARS-COV-2 in the air. Therefore, to find the answer to the question of whether different ventilation systems can be used to remove the SARS-COV-2 in the air, tests should be performed in different wards from the hospital and an extensive research should be performed in different hospitals with the same sampling and testing conditions.

In a study by Liu et al. (2020) proper ventilation and in a study by Li et al. (2020) the use of separate ventilation devices for SARS-COV-2 patients were introduced as effective methods to prevent the SARS-COV-2 transmission. In a study by Correia et al. (2020), heating, ventilation and air conditioning (HVAC) systems were introduced as a measure for primary infection control, but if not properly used, they may lead to the transmission and spreading of airborne diseases. In a study by Morawska et al. (2020), the measures mentioned to prevent the SARS-COV-2 transmission through air included: improved ventilation, natural ventilation and personalized-ventilations personalized-exhaust system (PV-PE). Although these measures might be good in countries with tropical and temperate climates, the use of ventilation will vary depending on the climate from most arid countries such as the Middle East (Amoatey et al., 2020). Therefore, to answer the question of whether ventilation systems can have a positive effect on reducing the transmission of SARS-COV-2 or not, depends on the environmental and climatic conditions of the region, which requires more extensive research.

Based on the findings from this article, other methods to prevent SARS-COV-2 transmission in the studies of Faridi et al. (2020) and Kenarkoohi et al. (2020) were reported; the use of personal protective equipment (PPE) for health care workers in hospitals. In a study by Ong et al. (2020), following precautionary measures such as environmental health and hand hygiene, in a study by Lednicky et al. (2020), Physical distance, face-coverings wearing were effective methods to prevent SARS-COV-2 transmission from air pollution and hospital environments. According to the EPA, recommended precautions to reduce the potential for airborne SARS-COV-2 transmission include: a distance of 2 m or 6 feet, personal hygiene, wearing a mask and hand washing, increasing air conditioning and outdoor air filtration, cleaning and disinfecting surfaces. These measures are not enough to reduce SARS-COV-2 exposure to air, as airborne transmission is not the only way we are exposed to SARS-COV-2, the SARS-COV-2 may be exposed to various levels through the air (EPA, 2020; Vardoulakis et al., 2020).

One of the strengths of this report is the SARS-COV-2 study in hospital air, which is a new topic and it had received less attention in research on the SARS-COV-2 transmission. One of the study weaknesses was the lack of comparison of SARS-COV-2 spreading in other closed environments with a high population density such as indoor recreation centers, kindergartens, schools, etc. It is suggested that researchers in the future should investigate the SARS-COV-2 detection in these places.

Conclusion

The results of this study showed that several factors can affect the positive or negative SARS-COV-2 detection in air samples, such as environmental conditions in hospitals, sampling methods, sampling height and distance from patients, flow rate and sampling time, efficiency and functionality of ventilation systems, use of disinfectants. Therefore, due to the possibility of SARS-COV-2 presence in the hospitals air, preventive measures should be taken such as physical distance, personal hygiene, ventilation, and air filtration. It is recommended to explore the effectiveness of different protection methods, such as air conditioning to prevent SARS-COV-2 transmission.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Credit author statement

Zahra Aghalari: Conceptualization, Data curation, Formal analysis, Methodology, Writing – original draft. Hans-Uwe Dahms: Validation, Writing – review & editing. Juan Eduardo Sosa-Hernandez, Writing – review & editing, Mariel A. Oyervides-Muñoz, Writing – review & editing, Roberto Parra-Saldívar: Writing – review & editing.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.