Kampf (J Hosp Infect 2020, see below) reviewed the literature on the persistence of human and veterinary coronaviruses on inanimate surfaces as well as inactivation strategies with biocidal agents used for chemical disinfection, e.g. in healthcare facilities. This analysis revealed that human coronaviruses such as SARS and MERS CoVs or endemic human CoVs can persist on inanimate surfaces like metal, glass or plastic for up to 9 days, but can be efficiently inactivated by surface disinfection procedures with 62-71% ethanol, 0.5% hydrogen peroxide or 0.1%
sodium hypochlorite within 1 minute. Other biocidal agents such as 0.05-0.2% benzalkonium chloride or 0.02%
chlorhexidine digluconate were found less effective.
Similarly, Yeo (Lancet Gastroenterol Hepatol 2020, see below) indicated that observations made with SARS and MERS CoVs support a relatively good viability of these viruses on surfaces depending on temperature and humidity.
SARS-CoV RNA was found in the sewage water of two hospitals in Beijing treating patients with SARS. When SARS-SARS-CoV was seeded into sewage water obtained from the hospitals in a separate experiment, the virus was found to remain infectious for 14 days at 4°C, but for only 2 days at 20°C.
Environmental sampling
A report by Ong (JAMA 2020, see below) described the detection of virus RNA in the environment of 3 COVID-19 cases in isolation in Singapore. Samples from the environment of one of the patients yielded positive results by RT-PCR, with 13 (87%) of 15 room sites (including air outlet fans) and 3 (60%) of 5 toilet sites (toilet bowl, sink, and door handle) positive. The patient had upper respiratory tract involvement with no pneumonia and had 2 positive stool samples for SARS-CoV-2 on RT-PCR. Of note, only one personal protective equipment (PPE) swab, from the surface of a shoe front, was positive. All other PPE swabs were negative. All air samples were negative. In a subsequent study, the same authors (Ong Infect Control Hosp Epidemiol 2020, see below) conducted a one-day PPE sampling study on 30 HCWs (doctors, nurses, and cleaners) caring for 15 confirmed SARS-CoV-2 infected patients with varying characteristics (i.e.
day of illness, presence/absence of symptoms, RT-PCR Ct value). None was requiring ventilatory support and no aerosol generating procedures were carried out prior to or during sampling. Median time spent in the patient’s room was 6 minutes for activities ranging from casual contact (e.g. administering medications, cleaning) to closer contact (e.g. physical examination, collection of respiratory samples). All samples (swabs from the entire front of goggles, front surface of N95 respirator, and front surface of shoes) were negative.
Environmental surveillance was also performed by Cheng (Inf Contr Hosp Epidem 2020, see below) in a patient with viral load of 3.3x106 copies/ml (pooled nasopharyngeal/ throat swab) and 5.9x106 copies/ml (saliva) respectively.
SARS-CoV-2 was revealed in 1 (7.7%) of 13 environmental samples, but not in 8 air samples collected at a distance of 10 cm from patient’s chin with or without wearing a surgical mask.
Another important study was conducted by Guo in a hospital in Wuhan (Em Inf Dis 2020, see below) and showed that SARS-CoV-2 was widely distributed in the air and on object surfaces, implying a potentially high infection risk for medical staff and other close contacts. The environmental contamination was greater in the ICU than in the general COVID-19 ward. Moreover, SARS-CoV-2 aerosol distribution characteristics indicated that the transmission distance of SARS-CoV-2 might be 4 m. As of March 30, no staff members at this hospital had been infected with SARS-CoV-2, indicating that appropriate precautions could effectively prevent infection. In addition, these findings suggested that home isolation of persons with suspected COVID-19 might not be a good control strategy.
Liu (Nature 2020, see below) measured viral RNA in aerosols in different areas of two Wuhan hospitals during the COVID-19 outbreak in February and March 2020. The concentration of SARS-CoV-2 RNA in aerosols detected in isolation wards and ventilated patient rooms was very low, but it was elevated in the patients' toilet areas. Airborne SARS-CoV-2 RNA in the majority of public areas was undetectable except in two areas prone to crowding. The authors suggested that SARS-CoV-2 may have the potential to be transmitted via aerosols.
During the initial isolation of 13 individuals with COVID-19 at the University of Nebraska Medical Center in the U.S.A., Santarpia (Sci Rep 2020, see below) collected air and surface samples to examine viral shedding from isolated individuals. The authors detected viral contamination among all samples.
Failure to isolate viable (infectious) virus in aerosols has been commonly reported, and there has been controversy in the first months of the epidemic whether SARS-CoV-2 can be transmitted through aerosols. According to Lednicky (Int J Infect Dis 2020, see below), this conundrum occurs because common air samplers can inactivate virions through their harsh collection processes. The authors then sought to resolve the question whether viable SARS-CoV-2 can occur in aerosols using VIVAS air samplers that operate on a gentle water-vapor condensation principle. Air samples were collected in the hospital room of two COVID-19 patients, one ready for discharge, the other newly admitted. Viable
SARS-CoV-2 was isolated from air samples collected 2 to 4.8 m away from the patients. The genome sequence of the SARS-CoV-2 strain isolated from the material collected by the air samplers was identical to that isolated from the newly admitted patient. Estimates of viable viral concentrations ranged from 6 to 74 TCID50 units/L of air. The data therefore indicated that patients with respiratory manifestations of COVID-19 produce aerosols in the absence of aerosol-generating procedures that contain viable SARS-CoV-2, and that these aerosols may serve as a source of transmission of the virus.
In a study by Wang (Int J Inf Dis 2020, see below), sewage samples were positive from inlets of the sewage disinfection pool, but negative from the outlet of the last sewage disinfection pool. Moreover, no viable virus was detected by culture. The monitoring data in this study suggested that strict disinfection and hand hygiene measures could decrease the hospital-associated COVID-19 infection risk of the staffs in isolation wards.
La Rosa (Water Res 2020, see below) reviewed available information on other coronaviruses in water environments.
12 publications were included. The data suggested that: i) CoV seems to have a low stability in the environment and is very sensitive to oxidants, like chlorine; ii) CoV appears to be inactivated significantly faster in water than non-enveloped human enteric viruses with known waterborne transmission; iii) temperature is an important factor influencing viral survival (the titer of infectious virus declines more rapidly at 23°C-25 °C than at 4 °C); iv) there is no current evidence that human coronaviruses are present in surface or ground waters or are transmitted through contaminated drinking-water. Ahmed (Sci Total Envir 2020, see below) reported the first confirmed detection of SARS-CoV-2 in untreated wastewater in Australia. SARS-SARS-CoV-2 RNA was concentrated from wastewater in a catchment in Australia and viral RNA copies were enumerated using RT-qPCR, resulting in two positive detections within a six-day period from the same wastewater treatment plant.
Experimental conditions
van Doremalen (NEJM 2020, see below) found that SARS-CoV-2 remained viable in aerosols (generated with the use of a three-jet Collison nebulizer and fed into a Goldberg drum to create an aerosolized environment) for at least 180 minutes, with a reduction in infectious titer 3 hours post-aerosolization from 103.5 to 102.7 CID50/L (mean across three replicates). This reduction in viable virus titer was relatively similar to the reduction observed in aerosols containing SARS-CoV-1. A subsequent report by Fear (Em Inf Dis 2020, see below) agreed with these conclusions. In this study, the authors analysed the virus dynamic aerosol efficiency using 3 different nebulizers to generate viral aerosols. The aerosol size distributions produced by the generators used, in mass median aerodynamic diameter, were 1–3 μm and had a geometric heterodispersity of ≈1.2–1.4. The data suggested retained infectivity and virion integrity for up to 16 hours. Of note, a fraction of naturally generated aerosols falls within the size distribution used in the experimental studies (<5 μm), which leads us to conclude that SARS-CoV-2-infected persons may produce viral bioaerosols that remain infectious for long periods after production through human shedding and airborne transport.
The virus was found most stable on plastic and stainless steel (van Doremalen NEJM 2020, see below). Viable virus could be detected up to 72 hours post application, though by then the virus titer was greatly reduced (polypropylene from 103.7 to 100.6 TCID50/mL after 72 hours, stainless steel from 103.7 to 100.6 TCID50/mL after 48 hours).
Since the beginning of the pandemics, few authors have attempted to test a wider array of environmental and climatological conditions (temperature, humidity, surface texture) conducive to SARS-CoV-2 survival. This was even more required as summer-winter transition and colder temperatures coincided with school and factories re-opening and an easing of restrictive isolation measures in the Northern hemisphere. Kwon (manuscript on bioRxiv : https://doi.org/10.1101/2020.08.30.274241) tested SARS-CoV-2 stability on 12 material surfaces including nitrile glove, Tyvek, N95 mask, cloth, Styrofoam, cardboard, concrete, rubber, glass, polypropylene, stainless steel and galvanized steel under 3 conditions based on Midwestern U.S. weather. SARS-CoV-2 remained viable and infectious on surfaces for 1 to 4 days at indoor conditions (21°C/60% relative humidity, RH), 1 to 3 days during summer conditions
(25°C/70% RH) and over 7 days during spring/fall conditions (13°C/66% RH). They provide experimental evidence that the virus is significantly more stable on all surfaces under the outdoor spring/fall condition and suggests that virus stability on surfaces is highly dependent on temperature and RH. They conclude that prolonged virus survival on surfaces in spring/fall and winter might support SARS-CoV-2 transmission through contaminated fomites and potentially contribute to new outbreaks and/or seasonal occurrence in the post-pandemic era, a scenario described for influenza virus and other human coronaviruses (Kissler Science 2020, see below).